Comparative Mapping Between Coho Salmon (Oncorhynchus kisutch) and Three Other Salmonids Suggests a Role for Chromosomal Rearrangements in the Retention of Duplicated Regions Following a Whole Genome Duplication Event

Miyako Kodama; Marine S O Brieuc; Robert H Devlin; Jeffrey J Hard; Kerry A Naish

doi:10.1534/g3.114.012294

Comparative Mapping Between Coho Salmon (Oncorhynchus kisutch) and Three Other Salmonids Suggests a Role for Chromosomal Rearrangements in the Retention of Duplicated Regions Following a Whole Genome Duplication Event

Kodama, Miyako; Brieuc, Marine S O; Devlin, Robert H; Hard, Jeffrey J; Naish, Kerry A 2014-09-01 00:00:00 Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 INVESTIGATION Comparative Mapping Between Coho Salmon (Oncorhynchus kisutch) and Three Other Salmonids Suggests a Role for Chromosomal Rearrangements in the Retention of Duplicated Regions Following a Whole Genome Duplication Event ,1 † ‡ ,1 Miyako Kodama,* Marine S. O. Brieuc,* Robert H. Devlin, Jeffrey J. Hard, and Kerry A. Naish* *School of Aquatic and Fishery Sciences, University of Washington, Seattle, Washington 98105, Fisheries and Oceans Canada, West Vancouver, British Columbia, V7K 1N6, Canada, and National Marine Fisheries Service, Northwest Fisheries Science Center, Seattle, Washington 98112 ORCID ID: 0000-0002-3275-8778 (K.A.N.) ABSTRACT Whole genome duplication has been implicated in evolutionary innovation and rapid diversiﬁcation. KEYWORDS In salmonid ﬁshes, however, whole genome duplication signiﬁcantly pre-dates major transitions across the family, chromsome and re-diploidization has been a gradual process between genomes that have remained essentially collinear. rearrangements Nevertheless, pairs of duplicated chromosome arms have diverged at different rates from each other, suggesting comparative that the retention of duplicated regions through occasional pairing between homeologous chromosomes may genome have played an evolutionary role across species pairs. Extensive chromosomal arm rearrangements have been mapping a key mechanism involved in re-dipliodization of the salmonid genome; therefore, we investigated their inﬂuence RAD sequencing on degree of differentiation between homeologs across salmon species. We derived a linkage map for coho salmon salmon and performed comparative mapping across syntenic arms within the genus Oncorhynchus, and with the whole genome genus Salmo, to determine the phylogenetic relationship between chromosome arrangements and the retention duplication of undifferentiated duplicated regions. A 6596.7 cM female coho salmon map, comprising 30 linkage groups with 7415 and 1266 nonduplicated and duplicated loci, respectively, revealed uneven distribution of duplicated loci along and between chromosome arms. These duplicated regions were conserved across syntenic arms across Oncorhynchus species and were identiﬁed in metacentric chromosomes likely formed ancestrally to the diver- gence of Oncorhynchus from Salmo. These ﬁndings support previous studies in which observed pairings involved at least one metacentric chromosome. Re-diploidization in salmon may have been prevented or retarded by the formation of metacentric chromosomes after the whole genome duplication event and may explain lineage- speciﬁc innovations in salmon species if functional genes are found in these regions. Whole genome duplication (WGD) is a mutational mechanism that can Copyright © 2014 Kodama et al. serve as a primary driver of evolutionary novelty (Ohno 1970; Zhang doi: 10.1534/g3.114.012294 Manuscript received May 22, 2014; accepted for publication July 13, 2014; 2003; Crow and Wagner 2006; Lynch 2007; Edger and Pires 2009). published Early Online July 21, 2014. Changes in ploidy levels after WGD can lead to dramatic alterations This is an open-access article distributed under the terms of the Creative at the cellular and phenotypic level (Mayﬁeld-Jones et al. 2013) and Commons Attribution Unported License (http://creativecommons.org/licenses/ provide additional genetic variation for mutation, drift, and selection by/3.0/), which permits unrestricted use, distribution, and reproduction in any to act on. These evolutionary processes can result in new adaptations medium, provided the original work is properly cited. Supporting information is available online at http://www.g3journal.org/lookup/ and species diversiﬁcation (Van De Peer et al. 2009; Storz et al. 2013). suppl/doi:10.1534/g3.114.012294/-/DC1 Genome sequencing projects are increasingly revealing that WGD is Corresponding authors: School of Aquatic and Fishery Sciences, University of widespread in many key lineages, such as ﬂowering plants and verte- Washington, Seattle, Washington 98105. E-mail: [email protected]; and School brates, and represents an ongoing phenomenon in many species (Otto of Aquatic and Fishery Sciences, University of Washington, Seattle, Washington 98105. E-mail: [email protected] and Whitton 2000; Van De Peer et al. 2009). Understanding the Volume 4 | September 2014 | 1717 Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 processes governing the return to a diploid mode—diploidization—by lineages so that it will be possible to understand how duplication played comparing the genomes of species descended from a WGD event can a role in evolution of salmon, and whether key genomic regions might provide insights into the event’s role in evolutionary innovation and explain innovation across a subset of species. persistence of duplicated regions (Jaillon et al. 2009; Mayﬁeld-Jones It has been known for some time that one of the key mechanisms et al. 2013). for diploidization within the subfamilies Coregoninae and Salmoninae The stabilization of the duplicated genome through diploidization (which includes Salmo, Salvelinus, and Oncorhynchus) has occurred can be achieved by rearrangements (such as translocations, ﬁssions, through Robertsonian rearrangements of whole chromosome arms fusions, and transpositions), gene loss, and sequence deletion and (Ohno 1999; Phillips and Ráb 2001). Most chromosome arms are divergence (Hufton and Panopoulou 2009; Schubert and Lysak 2011). syntenic between Salmoninae species, and the combined efforts of These processes tend to reduce the similarity of the duplicated ohnologs genome mapping and karyotyping have permitted alignment of chro- (Wolfe 2001), and the homeologous chromosomes resulting from mosome arms among several species within this subfamily (Danzmann WGD, but the exact mechanisms vary across lineages (Hufton and et al. 2005; Phillips et al. 2009; Lubieniecki et al. 2010; Lien et al. Panopoulou 2009). Whole genome duplication has been frequently 2011; Timusk et al. 2011; Guyomard et al. 2012; Naish et al. 2013; implicated in evolutionary innovation in eukaryotic genomes of Phillips et al. 2013). Chromosome arm number is largely conserved paleopolyploids (ancient polyploids) (Ohno 1999; Lynch and Conery (NF = approximately 100) but the numbers of chromosomes vary 2000; Jaillon et al. 2004; Cañestro et al. 2013), but evidence in plants substantially across species as a result of the Robertsonian rearrange- suggests that the rate of diversiﬁcation and extinction of neopolyploids ments (Phillips and Ráb 2001). The exception is Atlantic salmon, can be lower than that of related diploid lineages (Mayrose et al. with reduced chromosome arm number compared with the other 2011). Increasing the number of studies on mesopolyploids— species (NF = 72–74). However, large syntentic blocks within the organisms in the intermediate process of diploidization (Mayﬁeld-Jones arms of this species correspond to whole arms in other members of et al. 2013)—will provide a clearer understanding of contribution of the Salmoninae, making comparative studies feasible across this sub- WGD events to evolutionary innovation. family as a whole. Salmonid ﬁshes are descended from a whole genome duplication Comparative mapping between Chinook salmon (O. tshawytscha) event in an autotetraploid ancestor (Allendorf and Thorgaard 1984), and rainbow trout (O. mykiss) has revealed evidence for the retention distinct from the second round of duplication (2R) that occurred basal of at least eight metacentric chromosomes and four acrocentric chro- to the vertebrate tree and the third round (3R) early in the evolution of mosomes that are ancestral to species divergence within the genus the teleosts 225 to 333 million years ago (Hurley et al. 2007; Postlethwait Oncorhynchus (Naish et al. 2013; Phillips et al. 2013). One of the eight 2007; Santini et al. 2009; Near et al. 2012). This fourth round (4R) of metacentric chromosomes and one of the acrocentric chromosomes duplication was recently estimated as occurring 88–103 million years are also ancestral to the divergence between Salmo and Oncorhynchus. ago (Macqueen and Johnston 2014; see also Crête-Lafrenière et al. 2012; There is also further evidence for another ancestral metacentric and Alexandrou et al. 2013; Berthelot et al. 2014). Although the genomes of an ancestral acrocentric chromosome, but these have undergone sub- these species are returning to a stable diploid state through chromo- sequent rearrangements within at least one descendant species (Naish somal rearrangements and divergence of homeologous chromosomes, et al. 2013; Ostberg et al. 2013; Brieuc et al. 2014). High-density evidence of tetrasomic inheritance in males and extensive rearrange- linkage maps have revealed that recently diverged or undifferentiated ments among chromosomes has shown that restoration of diploidy is duplicated loci are not uniformly distributed among chromosomes not yet complete (Wright et al. 1983; Allendorf and Thorgaard 1984; (Atlantic salmon, Lien et al. 2011; Chinook salmon, Brieuc et al. Allendorf and Danzmann 1997). Comparative genome sequencing 2014), and the biased distribution of duplicated loci along chromo- between ohnologs in rainbow trout has revealed extensive collinearity some arms provides evidence that pairs of homeologous arms have between the duplicated chromosomes, characterized by loss of ap- diverged at different rates from each other (Brieuc et al. 2014). This proximately half the protein-coding regions through pseudogenization ﬁnding conﬁrms observations from previous studies conducted with but retention of most of the duplicated miRNA genes (Berthelot lower marker densities (for example, Danzmann et al. 2005; Guyomard et al. 2014). et al. 2012). Intriguingly, homeologous pairings have been observed The role of the WGD event in salmonid trait innovation and to include at least one metacentric chromosome (Wright et al. 1983), diversiﬁcation is unclear. Recent evidence based on molecular clock and duplicated markers map to such chromosomes (Brieuc et al. estimates suggest that duplication is unlinked to a major transition in 2014), supporting the view that metacentric chromosomes play an life history, anadromy (Alexandrou et al. 2013; Macqueen and Johnston important role in homeologous pairing (Phillips et al. 2009; Brieuc 2014), and preceded rapid species diversiﬁcation by several million years et al. 2014). These observations raise the interesting possibility that (Berthelot et al. 2014; Macqueen and Johnston 2014). Rather, both the evolutionary timing of metacentric chromosome formation dur- transitions appear to correspond with climate cooling (Macqueen and ing re-diploidization after the WGD event might inﬂuence the re- Johnston 2014). Re-diploidization has been subsequently characterized tention, and hence the evolutionary role, of duplicated regions across as a gradual process unlinked to signiﬁcant genome rearrangements species. Therefore, by comparing chromosomal arrangements and (Berthelot et al. 2014). However, it has also been argued that the du- distribution of duplicated regions across salmon species, we aim to plication event might have provided the raw material for evolution to provide a contextual framework for the further investigation of loci act on, and that differential divergence of duplicated regions might have involved in species diversiﬁcation. promoted speciation at varying time points (Macqueen and Johnston The development of a high-density linkage map for a less-described 2014). Large-scale genome characterization in the salmonids is increas- salmon species will contribute further information regarding chromo- ingly revealing the location of genes or regions that may have played some rearrangements that have already been deﬁned in several salmon a role in adaptation and diversiﬁcation (Davidson et al. 2010; Bourret species and enhance our understanding of the timing of these et al. 2013; Larson et al. 2013). Therefore, it is important to combine arrangements in a phylogenetic context. Examining the distribution these studies with an understanding of the mechanism and timing of of duplicated regions across individual chromosome arms in a second divergence between homeologous chromosome arms across salmon species—beyond Chinook salmon (Brieuc et al. 2014)—will also 1718 | M. Kodama et al. Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 facilitate an understanding of the relationship between timing of meta- Satsop River in the Southwest Washington Coast/Lower Columbia centric chromosome formation and diversiﬁcation between homeologs. ESU; and (4) Chehalis River located in British Columbia, Canada Coho salmon (Oncorhynchus kisutch) is a species whose genome has (49299N, 121949W). not been extensively described to date. A low-density linkage map of An initial framework map was constructed using two haploid coho salmon has been constructed using microsatellites (McClelland crosses (haploid family 1 and 2) comprising 64 and 62 individuals, and Naish 2008), but this map is not sufﬁciently resolved to study the respectively. These types of crosses have the advantage of identifying consequences of WGD because there is a low number of duplicated duplicated loci, because these loci will appear as heterozygotes in loci mapped. A high-density map in this species is feasible, given re- the offspring if they are polymorphic, while nonduplicated loci will cently emerged sequencing technologies (for example, Baird et al. be homozygous. Haploid families were created at the University of 2008). Coho and Chinook salmon are sister species (Crête-Lafrenière Washington hatchery facility (47659N, 122319W), following the pro- et al. 2012); therefore, comparative mapping across coho and Chinook tocol of Thorgaard et al. (1983). Embryos were collected before hatch- salmon, as well as more divergent species in the genus Oncorhynchus ing and preserved in 100% ethanol. and Salmo, will help validate the hypotheses and provide more robust Sex-speciﬁc maps were created using two F3 outbred diploid evidence on the process of chromosomal evolution following WGD. crosses and one outbred diploid cross. Speciﬁcally, F3 diploid crosses The aim of our research is to determine the relationship between were created from a cultured line originally derived from an outbred chromosome arrangements and the retention of recently diverged or cross between two populations in Washington State (McClelland and undifferentiated duplicated regions by deriving a linkage map for coho Naish 2010). F0 males were collected from Bingham Creek in South- salmon and comparing this map with those of Chinook salmon, west Washington (47159N, 123409W). F0 females were obtained rainbow trout, and Atlantic salmon. We therefore constructed high- from the Domsea broodstock farm. Two F3 crosses were established density linkage maps for coho salmon using restriction site–associated in December 2010 by mating two F2 full-sibs to create one family, and DNA (RAD) sequencing (Baird et al. 2008). By achieving this objec- two F2 half-sibs to create the other. The two families comprised 55 tive, we also produced a reference database of RAD markers that can and 67 offspring, respectively, (diploid family 1 and 2). An additional be used for alignment of sequences generated in future work, and diploid outbred cross was created from an aquaculture population described in detail the properties of the coho linkage map. Coho using coho salmon derived from the Chehalis River located in British salmon chromosome arms were identiﬁed by comparative mapping Columbia, Canada (49299N, 121949W). Speciﬁcally, cultured indi- with Chinook salmon using markers in common between the species, viduals were repeatedly backcrossed with wild individuals from the and whole chromosome arm homologies were described across spe- Chehalis River for six generations, and diploid crosses were created in cies to improve our current understanding of chromosome arm rear- January 2011. One diploid family from these crosses comprising 99 rangement within the genera Oncorhynchus and Salmo.Linkage individuals was used for further analyses (diploid family 3). groups representing homeologous chromosome arms in coho salmon DNA extraction, sequencing, and ampliﬁcation of were discovered using duplicated markers, and regions of duplicated sex-linked markers markers were compared across species to determine the extent to Genomic DNA from the sampled individuals was extracted using which these regions were conserved across lineages. By identifying the DNeasy extraction kit (QIAGEN, Valencia, CA) following the genomic regions that are in the process of diploidization and linking manufacturer’s procedures. The DNA was digested with SbfI, and these regions to chromosomal rearrangements, we aim to provide a 6-nucleotide barcode was added to each sample for individual iden- the basis for determining the role of duplication in maintaining tiﬁcation following protocols described by Baird et al. (2008). Between ongoing polymorphisms and explaining processes of diversiﬁcation 24 and 36 individuals were pooled in a single library and sequenced across Salmoninae species. with 100-bp single-read lengths using the Illumina HiSequation 2000 sequencer. The sequences were separated by individual using MATERIALS AND METHODS PROCESS_RADTAGS implemented in STACKS (Catchen et al. Justiﬁcation and description of sample collection and 2011, 2013). Because the quality score of sequences decreased be- experimental crosses yond 74 nucleotides, sequences were trimmed to 74 nucleotides to remove low-quality sequences. A locus was deﬁned as a 74-nucleotide A two-step approach was used to develop genomic resources and RAD sequence for the purpose of this study. construct linkage maps. First, RAD sequences from individuals sampled Genetic sex was determined in the two diploid families (diploid from multiple populations were used to construct a reference da- family 1 and 2) using a Y-linked growth hormone pseudogene (GH5 tabase for aligning loci across mapping families. This reference and GH6) (Devlin et al. 2001) and sex-determining gene, sdY (sdY database was screened for errors, duplicated loci, and repeat regions E2S1 and sdY E2AS4) (Yano et al. 2012). Polymerase chain reactions following approaches described by Brieuc et al. (2014), and loci were were performed for each set of primers using a QIAGEN Multiplex subsequently named to ensure consistency across mapping families. PCR kit. Speciﬁcally, reaction mixtures consisted of 10–200 ng geno- Second, speciﬁc cross types were used to perform the mapping: mic DNA, 1· QIAGEN Multiplex PCR Master Mix, 0.25 mMofGH5 gynogenetic haploid crosses were used to map both duplicated and and GH6, or 0.4 mM of sdY E2S1 and sdY E2AS4, comprising a total nonduplicated loci, and diploid crosses were used to construct sex- volume of 10 ml. Cycling conditions consisted of a 15-min initial speciﬁc maps. activation step at 95, 30 cycles of 30-s denaturing step at 94,90-s The reference database of RAD loci was constructed using annealing step at 60, a 60-s extension step at 72, and a 10-min ﬁnal sequences from 583 individuals representing four populations in extension step at 72. the Paciﬁc Northwest of the United States and Canada: (1) the Washington Department of Fish and Wildlife’s(WDFW) Wallace Reference database of RAD loci River Hatchery (47879N, 121719W); (2) the Domsea broodstock population, which originated in 1973 and 1974 from Wallace River RAD loci that are found within repeat regions, and loci containing Hatchery; (3) Bingham Creek (47159N, 123409W), a tributary to the repeat units, can confound the identiﬁcation of unique loci. Therefore, Volume 4 September 2014 | Coho Salmon Genome Map | 1719 Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 a reference sequence database comprising a set of pre-screened RAD a maximum of three nucleotide mismatches per locus. Subsequently, loci was ﬁrst created from the survey of four populations following polymorphic loci were identiﬁed in each diploid family using STACKS, bioinformatic procedures fully described by Brieuc et al. (2014). This and genotypes at these loci were determined when alleles were se- database served as a resource for aligning loci across studies. In brief, quenced with a depth greater than 10· per individual. sequences from all 583 individuals sampled across the four popula- STACKS uses a maximum likelihood statistical model to identi- tions described previously were extracted using STACKS 0.9995 fy sequence polymorphisms and determine individual genotypes (Catchen et al. 2011). Both monomorphic and polymorphic loci that (Catchen et al. 2011, 2013). This approach can be biased toward were sequenced with a depth greater than 5· in more than 496 indi- heterozygous genotypes when sequence depths differ between the viduals (85%) were retained in a temporary database and used for two alleles. To correct this bias against heterozygous genotypes, geno- further screening. types were corrected after running STACKS with the Python script Loci in the temporary database that corresponded to repeat regions developed by Brieuc et al. (2014). Speciﬁcally, individuals were de- and loci containing repeat units were removed using two alignment- termined as heterozygotes at a locus if both alleles had a depth of more based strategies following the protocol of Brieuc et al. (2014). First, than two and the total read depth was 10· or greater. loci in the temporary database were aligned against themselves using Linkage mapping BOWTIE (Langmead et al. 2009) by allowing a maximum of three nucleotide mismatches per locus. A locus that aligned to several loci, Linkage maps in all haploid and diploid families were constructed or a locus that did not align to itself, was removed from the temporary using software for genetic mapping, ONEMAP 2.0-3 (Margarido et al. database. Then, a BLAST search (Altschul et al. 1990) of the tempo- 2007), implemented in R version 3.0.2 (R Development Core Team rary database was conducted against itself. Loci that did not return 2013). Because coho salmon have 30 chromosome pairs (Phillips and a match, or loci where the best matches were not themselves, were Ráb 2001), each mapping family was expected to have at least 30 removed from the temporary database. linkage groups. Linkage groups were named “Co,” following the con- Using the updated temporary database of RAD loci, polymorphic vention used in mapping studies in salmonids; this practice uses ab- duplicated loci were identiﬁed based on two haploid families. First, breviated common names for groups that are not yet anchored to sequences from these haploid families were aligned to the temporary chromosomes (Danzmann et al. 2005; Naish et al. 2013). RAD loci database using BOWTIE, allowing a maximum of three nucleotide with 20% or less missing values among individuals within a family mismatches per locus. Sequences from the haploid individuals that were used for linkage analyses, and these loci were assigned to linkage aligned to more than one locus in the database could not be con- groups in each family separately using a minimum log of odd ratio ﬁdently relied on in further analyses; they were thus identiﬁed as (LOD) score of 4.0 and a maximum recombination fraction of 0.25. “black-listed” loci and removed from the temporary database. Sub- The LOD score was subsequently increased by 1.0 until the number of sequently, polymorphic loci sequenced with a depth greater than 10· linkage groups reached 30 or higher. An integrated haploid map was per haploid individual were identiﬁed using STACKS and retained for ﬁrst constructed from the two haploid families using MERGEMAP further screening. Among these polymorphic loci, a locus was identi- (Wu et al. 2011) because genotypes at duplicated loci were only de- ﬁed as being putatively duplicated when more than one haploid off- termined in these families. This integrated haploid map was later used spring in a family was heterozygous at this particular locus (Brieuc to examine the distribution of duplicated loci across all linkage groups et al. 2014). A ﬁnal reference database comprising named duplicated and identify linkage groups involved in recent or ongoing homeologous and nonduplicated loci, as well as loci removed from the alignment- pairing. based screening steps and “black-listed” loci, was created. Recombination rates in male salmonids tend to be lower than those observed for females (Sakamoto et al. 2000; Ostberg et al. 2013), Genotyping of individuals in map crosses but these differences tend to decrease with high marker density and Haploid individuals were genotyped at both nonduplicated and genome coverage (Rexroad et al. 2008; Lien et al. 2011). We used the duplicated loci. Sequences from all haploid individuals were aligned female meiosis from the three diploid families to estimate marker to the nonduplicated and duplicated loci from the ﬁnal reference order in these crosses. The data from all haploid and diploid female database using BOWTIE by allowing a maximum of three nucleotide parents were then combined to calculate an integrated female haploid/ mismatches per locus. In haploids, we have shown reliable identiﬁ- diploid map using MERGEMAP. cation of single loci that have up to three SNPs; we have conﬁrmed Ordering markers in the diploid male map was computationally this result with genome mapping. To remain consistent, we used up to difﬁcult, potentially due to reduced recombination and occasional three mismatches so that we could differentiate between nonduplicated tetrasomic inheritance in males (Allendorf and Danzmann 1997). loci and duplicated loci. Both this study and a previous one (Brieuc et al. Therefore, information from the integrated female map constructed 2014) have shown that very reliable linkage results can be obtained in with haploid and diploid mothers was used to infer the order and map haploids using these criteria. Polymorphic loci sequenced with a depth the male meiosis in the three diploid families (diploid family 1, 2, 3). greaterthan10· per individual were identiﬁed using STACKS. Both Polymorphic loci in common between the male parents and the inte- nonduplicated and duplicated markers in the haploid families were used grated female map, as well as the Y-linked growth hormone pseudogene for mapping, described below and following the protocol of Brieuc et al. and sex-determining gene, sdY, were grouped using a log of odd (2014). Polymorphic duplicated loci were mapped when one of the ratio (LOD) score of 4.0 and a maximum recombination fraction of paralogs was polymorphic (OPP: one paralog polymorphic, parental 0.25 using ONEMAP. The LOD score was subsequently increased genotypes aa and ab or aa and bc) or when both paralogs were poly- by 1.0 until the number of linkage groups reached 30 or higher. morphic (BPP: parental genotypes ab and ac or ab and cd; see Table 1 Grouped loci were then ordered based on the known order on the in Brieuc et al. 2014). integrated female map using the make.seq and map functions imple- Diploid individuals were only genotyped at nonduplicated loci. mented in ONEMAP. The position of a Y-linked growth hormone Sequences from all diploid individuals were aligned to the nonduplicated pseudogene and sex-determining gene, sdY, on the male map was loci identiﬁed in the ﬁnal reference database using BOWTIE by allowing estimated in the two diploid families (diploid family 1 and 2) using 1720 | M. Kodama et al. Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 the try.seq and map functions implemented in ONEMAP. The data ﬁnal reference database comprising 52,936 nonduplicated loci and from all diploid male parents were then combined to calculate an 7235 duplicated loci, as well as the 9866 loci that were removed by integrated male map using MERGEMAP. screening, are given in Supporting Information, File S1. Linkage mapping Comparative mapping with Chinook salmon and An initial framework map was constructed with two haploid families. comparison with other salmonid species Haploid family 1 and 2 had 3976 and 4048 biallelic polymorphic RAD The reference database for coho salmon containing duplicated and loci, respectively, comprising a total of 6652 unique RAD loci. Among nonduplicated RAD loci was aligned to the 54,937 ﬁltered RAD loci these loci, a mixture of duplicated and nonduplicated loci (3897 loci in identiﬁed in Chinook salmon (Brieuc et al. 2014) using BOWTIE, haploid family 1; 3996 loci in haploid family 2) were successfully allowing no more than three nucleotide mismatches per locus. Ho- assigned to 30 linkage groups with a LOD score of 5.0 to 7.0. The total mologies between Chinook and coho salmon were determined by map length for the haploid family 1 and 2 was 3040.1 cM and 3185.5 examining the chromosomal arm locations of shared loci between cM, respectively. The integrated haploid map had 5377 nonduplicated the two species. Putative centromere positions on coho linkage groups markers and 1266 duplicated markers with a total map length of were estimated based on markers mapped in the gynogenetic diploid 3602.6 cM (File S2). families in Chinook salmon (Brieuc et al. 2014). The order of mapped Linkage analyses were conducted in the diploid families following loci between the Chinook and coho salmon map was compared to the construction of the integrated haploid map. Diploid family 1, 2, determine if marker orders for chromosomes or chromosomal arms and 3 had 1360, 1176, and 1931 biallelic nonduplicated loci that were between the species were conserved. Finally, homologies identiﬁed polymorphic in each female parent, respectively. Among these loci, between Chinook and coho salmon were used to infer homologies a set of loci (1214 loci in diploid family 1; 1138 loci in diploid family 2; across coho salmon, rainbow trout, and Atlantic salmon using molec- 1765 loci in diploid family 3) were successfully assigned to 30 linkage ular markers in common between published maps (Phillips et al. 2009; groups with a LOD score of 4.0 to 8.0. The total map length for the Lien et al. 2011; Miller et al. 2012; Brieuc et al. 2014). diploid family 1, 2, and 3 was 3714.1 cM, 3068.9 cM, and 5047.2 cM, respectively. Although the diploid family 3 had the largest total map Homeologous relationships and the distribution of length, it also had the highest number of markers mapped. Because duplicated loci across genomes more recombination events are captured with more markers (Liu As we pointed out, two categories of duplicated loci were identiﬁed in 1998), it is not surprising that the diploid family 3 had the largest this study, where one of the paralogs was polymorphic (OPP) or both total map length. Finally, data from the haploid parents and dip- paralogs were polymorphic (BPP). Duplicated loci with both paralogs loid female parents were combined; an integrated haploid/diploid polymorphic (BPP) were used to infer homeologous linkage groups female mapmeasured6596.7cM, and it comprised 7415 non- because both paralogs could be mapped. The positions of duplicated duplicated markers and 1266 duplicated markers (Table 1; Figure 1; loci were subsequently examined on the integrated haploid map to File S2). determine whether there was a bias in the distribution of these loci The male meioses were mapped using linkage analyses in the across linkage groups. A kernel smoothing approach using a sliding diploid families. Among the 8681 loci placed on the integrated window of 2 cM was used to determine whether there was a regional haploid/diploid female map, diploid family 1, 2, and 3 had 846, 814, bias in distribution of these loci for each linkage group following and 879 polymorphic loci in common for each male parent. Among methods described by Brieuc et al. (2014). Homeologous relationships these loci, a set of loci (792 loci in diploid family 1; 790 loci in diploid detected in coho salmon were also compared with those identiﬁed in family 2; 851 loci in diploid family 3), as well as the Y-linked growth Chinook and Atlantic salmon (Lien et al. 2011; Brieuc et al. 2014). hormone pseudogene and sex-determining gene, sdY, were success- fully assigned to 30 linkage groups with a LOD score of 4.0 to 7.0. Both the growth hormone pseudogene and sdY mapped to the RESULTS telomeric region of the linkage group, Co30. All linkage groups were Reference database of RAD loci successfully merged, except for Co22, which was split into two A reference database comprising a unique set of RAD loci was created linkage groups (Co22_1 and Co22_2) (File S2). The number of for the purpose of sequence alignment and identiﬁcation of poly- markers in common between the integrated male and female maps morphisms across individuals. A total of 70,037 loci were sequenced varied for each linkage group, ranging from 25 to 106 markers per with a depth greater than 5· per individual in at least 496 individuals. linkage group (File S3). The male map had a total map length of These loci formed the temporary reference database of RAD loci, and 4141.76 cM (File S3). they were retained for further screening. Sequence alignment using The comparison between the male and female linkage groups BOWTIE showed that 4075 loci did not align uniquely to themselves reﬂected different recombination patterns between the sexes (Figure 2; and likely corresponded with repeat regions; therefore, these loci were File S4). Although telomeres were not mapped in males due to a lack removed from the temporary database. After performing the BLAST of duplicated markers, many male linkage groups were expanded in search of the temporary reference database against itself, 2085 loci did size toward the terminal regions relative to the female, as seen by the not return a match or the best match score was not the locus itself. It increased distance in these regions reﬂecting more recombination was possible that these loci contained repeat sequences; therefore, events. Such patterns were particularly prominent for several linkage these loci were also removed from the temporary reference database. groups (Co02, Co04, Co05, Co08–Co10, Co13–Co15, Co17–Co19, Sequences from the haploid individuals were aligned to the reference Co21–Co29). Although qualitative, there was also evidence of sup- database using BOWTIE; 3706 loci from the haploid individuals pressed recombination around the region containing the centromere aligned to several other loci, and these loci were thus black-listed in the male map compared with female integrated map for all linkage and removed from the reference database. Additionally, 7235 loci were groups. The male map had reduced distance in these regions com- identiﬁed as polymorphic duplicated loci in the haploid families. The pared to the female map. Volume 4 September 2014 | Coho Salmon Genome Map | 1721 Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 n Table 1 Description of the Coho salmon consensus linkage map constructed with haploid and diploid female parents and comparison with chromosome arms of Chinook salmon, rainbow trout, and Atlantic salmon Chinook Rainbow Trout Atlantic Salmon Chromosomal Coho Coho Chromosome Chromosome Chromosome Rearrangement Linkage Number of Linkage (Philips et al. 2013; (Philips et al. 2009; (Danzmann et al. 2008; Conserved Group Size (cM) Markers Arms Brieuc et al. 2014) Brieuc et al. 2014) Philips et al. 2009) Across Species Co01 267.51 393 Co01a Ots02p Omy17p Ssa02q B, metacentric Co01b Ots02q Omy17q Ssa12qb Co02 248.6 344 Co02a Ots03p Omy03p Ssa02p B, metacentric Co02b Ots03q Omy03q Ssa25 Co03 274.51 360 Co03a Ots04p Omy06p Ssa24 B, metacentric Co03b Ots04q Omy06q Ssa26 Co04 250.26 395 Co04a Ots06p Omy01p Ssa16qa B, metacentric Co04b Ots06q Omy01q Ssa18qa Co05 268.59 376 Co05a Ots07p Omy07p Ssa17qb B, metacentric Co05b Ots07q Omy07q Ssa22 Co06 267.8 415 Co06a Ots09p Omy12p Ssa13qb B, metacentric Co06b Ots09q Omy12q Ssa03q Co07 211.09 241 Co07a Ots11p Omy19p Ssa04p B, metacentric Co07b Ots11q Omy19q Ssa01p Co08 295.21 382 Co08a Ots12p Omy11p&q Ssa20qa C, metacentric Co08b Ots12q Omy26 Ssa11qb Co09 196.03 207 Co09a Ots15p Omy21p Ssa07p A, metacentric Co09b Ots15q Omy21q Ssa07q Co10 239.27 346 Co10a Ots01p Omy04p Ssa23 — Co10b Ots27 Omy13q Ssa06q Co11 280.26 419 Co11a Ots01q Omy23 Ssa01qa — Co11b Ots29 Omy15p Ssa29 Co12 215.12 286 Co12a Ots05p Omy08p Ssa15qa — Co12b Ots34 Omy10q Ssa08q Co13 288.32 350 Co13a Ots05q Omy05q Ssa10qa — Co13b Ots23 Omy02p Ssa05q Co14 270.54 356 Co14a Ots08p Omy25p Ssa09qa — Co14b Ots31 Omy14p Ssa14qb Co15 282.89 355 Co15a Ots08q Omy25q (Omy29) Ssa09qb — Co15b Ots13q Omy27 Ssa20qb Co16 211.31 220 Co16a Ots10p Omy09p Ssa18qb — Co16b Ots14p Omy18p Ssa16qb Co17 181.92 292 Co17a Ots13p Omy18q Ssa27 — Co17b Ots16q Omy09q Ssa15qb Co18 209.02 323 Co18a Ots14q Omy24 Ssa09qc — Co18b Ots16p Omy11p Ssa19qa Co19 217.65 315 Co19a Ots17 Omy15q Ssa17qa — Co19b Ots21 Omy14q Ssa05p Co20 203.33 247 Co20a Ots24 Omy16p Ssa19qb — Co20b Ots32 Omy13p Ssa12qa Co21 130.25 184 Co21 Ots18 Omy04q Ssa06p C, acrocentric Co22 194.97 243 Co22 Ots19 Omy02q Ssa10qb C, acrocentric Co23 212.27 213 Co23 Ots20 Omy05p Ssa01qb C, acrocentric Co24 127.18 187 Co24 Ots22 Omy16q Ssa13qa C, acrocentric Co25 171.35 196 Co25 Ots25 Omy20p+q SSa08p & Ssa28 A, acrocentric Co26 184.21 225 Co26 Ots26 Omy22 Ssa21 A, acrocentric Co27 164.56 198 Co27 Ots28 Omy28 Ssa03p B, acrocentric Co28 169.82 214 Co28 Ots30 Omy10p Ssa04q C, acrocentric Co29 173.74 181 Co29 Ots33 OmySex Ssa11qa B, acrocentric Co30 189.15 218 Co30 Ots10q Omy08q Ssa14qa — Total 6596.7 8681 Linkage groups (Co) were randomly assigned numbers, and arm names are given as “a” and “b.” Homologous arms in Chinook salmon, rainbow trout, and Atlantic salmon are based on chromosome names for each species (Ots, Omy, and Ssa, respectively), with known orientations (p is the short arm, q is the long arm). and denote inferred relationship. There were no markers in common between Co07a and Ots11p( ), and there are markers in common between Co12b and Ots34/Ots11p( ). A chromosomal arm that is composed entirely of ribosomal DNA. The ﬁnal column designates chromosomal rearrangements conserved across species; letter corresponds to phylogenetic placement in Figure 5. Incompletely resolved relationships between Atlantic salmon and rainbow trout according to published studies. might include a section of Ssa19qa. 1722 | M. Kodama et al. Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 Figure 1 Graphical representation of 30 consensus linkage groups in haploid and diploid female coho salmon. Co01 to Co20 are metacentric, and Co21 to Co30 are acrocentric, inferred from comparative mapping. The size of linkage groups ranges from 127.18 to 295.21 cM (Kosambi), and each line corresponds to the location of one or more markers. The putative location of the centromere, estimated by comparative mapping with Chinook salmon, is represented in red. Comparative mapping with Chinook salmon and chromosome in Chinook salmon. Four metacentric linkage groups comparisons with other salmonid species in coho salmon (Co15–Co18) comprise arms that are found in two separate metacentric chromosome pairs in Chinook salmon. Two We mapped 664 RAD loci in coho salmon that had been previously metacentric linkage groups (Co19, Co20) comprise two acrocentric placed on the Chinook salmon map, which permitted the identiﬁ- chromosome pairs in Chinook salmon. Finally, one acrocentric link- cation of homologous chromosomal arms between the two species age group (Co30) corresponds to an arm that is a part of a meta- (Table 1). On the basis of this comparison, we also identiﬁed the centric chromosome pair in Chinook salmon. putative locations of centromeres within coho salmon linkage groups The orders of the RAD loci on the Chinook and coho salmon maps (Figure 1). Two homologous relationships between the species were were compared across each linkage group or for each chromosome inferred. An arm of the linkage group Co07a had three markers that arm to determine whether any chromosomal inversions occurred after mapped to Ots34 in Chinook salmon. However, Co12b had six divergence between the species. There was a strong linear relationship markers that mapped to Ots34 and three markers that mapped to among mapped loci for all the linkage groups or arms (File S5), suggest- Ots11p. Ots11p and Ots34 are likely involved in recent or ongoing ingthatmarkerorderswereconserved forall chromosomesorchro- homeologous pairing in Chinook salmon (Brieuc et al. 2014); there- mosomal arms. Such analyses provide additional evidence for the fore, it was not surprising that loci on Ots34 mapped to both homol- occurrence of centrometric inversion in Omy20 in rainbow trout after ogous arms in coho salmon. In this case, we assumed that Co07a was divergence between rainbow trout and Chinook/coho salmon, and homologous to Ots11p, and Co12b was homologous to Ots34 for this chromosomal inversion may be exclusive to rainbow trout (Naish reasons given in the Discussion. et al. 2013; Ostberg et al. 2013; Brieuc et al. 2014). Comparative mapping with Chinook salmon permitted inference The homologies we observed between Chinook and coho salmon of the structure of coho linkage groups. Twenty linkage groups in coho permitted alignment of coho linkage groups to those of rainbow trout salmon corresponded to putative bi-armed metacentric chromosomes, and the Atlantic salmon, and the results are summarized in Table 1. and 10 linkage groups corresponded to putative uni-armed acrocentric Three acrocentric and eight metacentric chromosomes were con- chromosomes (Figure 1). These inferred structures are in agreement served among coho salmon, Chinook salmon, and rainbow trout. with the known chromosome structures in coho salmon (Phillips and Comparison between the Oncorhynchus species and the Atlantic Ráb 2001). The short (p) arm of an acrocentric chromosome is usually salmon revealed that one metacentric chromosome and one acrocen- uncharacterized in mapping studies because there are often insufﬁcient tric chromosome were conserved across all compared species. markers describing this region (Brieuc et al. 2014). In this study, we identiﬁed the small arm for two putative acrocentric chromosomes Homeologous relationships and the distribution of (Co22, Co29) through comparative mapping with Chinook salmon. duplicated loci across linkage groups Comparative mapping between the Chinook and coho salmon The identiﬁcation of linkage groups involved in homeologous pairing, maps also provided information on chromosomal arrangements that as well as the localization of duplicated loci across individual linkage are shared between the two species. Eighteen chromosomes are con- groups, was examined using the integrated haploid female map. A served between the species (Table 1); speciﬁcally, nine metacentric total of 1266 duplicated loci (1066 OPP and 200 BPP) were placed on chromosomes and nine acrocentric chromosomes were conserved this map. These loci were not distributed evenly among the linkage between the species. The remaining chromosome structures likely support independent Robertsonian rearrangements that occurred after groups (x test for uniform distribution across linkage groups, after descent from a common ancestor. correction for the number of markers per linkage group: p-value 0, Five metacentric linkage groups in coho salmon (Co10–Co14) con- df = 29); 87.0% of the duplicated loci were located on 16 linkage sist of one acrocentric chromosome and one arm from a metacentric groups (Figure 3). There was a bias in distribution of these loci along Volume 4 September 2014 | Coho Salmon Genome Map | 1723 Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 Figure 2 Comparison of map distances between com- mon markers mapped in male and female coho salmon. Linkage groups Co04 (A), Co17 (B), Co18 (C), and Co26 (D) are given as examples. The putative region contain- ing the centromere is represented by the cross-hatched area. All linkage groups are presented in File S4. the 16 linkage groups; duplicated loci were mostly found in the distal homeologous pairs diverged from each other at different rates following regions of all 16 linkage groups (Figure 4). Homeologies were identi- the whole genome duplication event. Regions of the genome with poly- ﬁed between putative chromosome arms using marker pairs in which morphic duplicated markers were found on the same eight pairs of both paralogs were polymorphic (Table 2). All eight homeologous homologous chromosome arms (16 arms in total) across coho and arm pairs with a high retention of duplicated loci detected in coho Chinook salmon. Each of the eight pairs of chromosomes likely involved salmon were also observed in Chinook salmon, and four homeologous in ongoing or recent homeologous pairing included at least one of the arm pairs were conserved in Atlantic salmon (Table 2). All of these ancestral metacentric chromosomes that are conserved between the two chromosome arms, likely involved in recent or ongoing homeologous species. The other chromosome arm involved in the pairing may be part pairing, involved at least one metacentric chromosome ancestral to the of either an acrocentric chromosome or a metacentric chromosome. The divergence between Paciﬁcsalmonspecies. data suggest that Robertsonian rearrangements that result in metacentric chromosome formation prior to the diversiﬁcation of homeologous pairs DISCUSSION might partly explain the uneven retention of duplicated regions across Here, we aimed to examine the relationship between chromosomal the genome, at least within Paciﬁcsalmon. evolution and retention of duplicated regions within the genus The consensus male map, constructed with three diploid families, Oncorhynchus, and between this genus and Salmo, by deriving a link- was signiﬁcantly smaller (4141.7 cM) than the consensus female map age map for coho salmon and comparing this map with that of (6596.7 cM) constructed with two haploid families and three diploid Chinook salmon, rainbow trout, and Atlantic salmon. Thirty linkage families. There are three main reasons that might explain the reduced groups including 20 putative metacentric and 10 putative acrocentric map size in the male compared with the female map. First, the chromosomes were described across two haploid and three diploid difference could simply be a function of more markers being placed families. Chromosomal rearrangements were identiﬁed by compar- on the female map (8681 for the female and 2043 for the male), ing homologous arms between coho salmon, Chinook salmon, rain- because map size tends to increase when more markers are added (Liu bow trout, and Atlantic salmon. Results conﬁrmed the conservation 1998). Second, some male linkage groups only represented a portion of at least one metacentric chromosome between Oncorhynchus and of those in females; for example, in three metacentric chromosomes Salmo (Co09) and seven metacentric chromosomes across the genus (Co07, Co09, Co13) only one arm and a region containing the cen- Oncorhynchus (Co01–Co07) (Naish et al. 2013; Phillips et al. 2013; tromere were mapped, the duplicated markers were not mapped in Brieuc et al. 2014), and detected a polymorphism in another across males. Third, recombination in males is suppressed relative to females, coho and Chinook salmon and rainbow trout (Co14 and Co15). and male maps in salmonids often tend to be smaller. Comparisons Another metacentric chromosome was detected as ancestral to coho between the consensus male map and the consensus (haploid and and Chinook salmon only (Co08). The placement of 1266 duplicated diploid) female map indicated that recombination in the males was loci on the consensus haploid map of 6643 markers revealed that these suppressed around the region containing the centromere in some loci were not evenly distributed across all linkage groups, supporting linkage groups, whereas recombination in females seemed suppressed aprevious ﬁnding in Chinook salmon (Brieuc et al. 2014), namely, that toward telomeric regions. 1724 | M. Kodama et al. Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 Figure 3 Number of markers and distribution of duplicated markers across each coho salmon linkage group. Nonduplicated loci are represented in light gray. Duplicated loci are represented in dark gray (loci with only one paralog polymorphic) or black (both paralogs polymorphic). Accurate identiﬁcation of chromosome structure in coho salmon has been repeatedly transposed to different chromosomes in differ- relied on aligning homologous chromosome arms with Chinook ent salmon species (Phillips et al. 2001; Woram et al. 2003; Yano salmon. In addition, regions containing the centromere were inferred et al. 2012) and can be polymorphic within a species (Eisbrenner through comparative mapping between coho and Chinook salmon as et al. 2014). no gynogenetic diploid families were used for this study to identify the Our results showed that suppressed recombination around the exact location of the centromere. Homology of Co07a and Co12b with region containing the centromere in males was widely apparent, Chinook salmon chromosome arms Ots11p and Ots34 was not whereas higher recombination was observed in telomeric regions for completely resolved. These arms are homeologous to each other some male linkage groups relative to female. The results are in within both species, and markers on Ots34 mapped to both Co07a agreement with a number of studies performed on other salmonid and Co12b in coho salmon. We inferred that Co07a was homologous species (Sakamoto et al. 2000; Moen et al. 2008; Rexroad et al. 2008; to Ots11p, as the arm Co07a is part of a metacentric chromosome that Lien et al. 2011). Male recombination rate in telomeric regions of is conserved in Chinook salmon (Ots11) and rainbow trout (Omy19) a subset of rainbow trout linkage groups has been shown to be higher (Table 1). In fact, Naish et al. (2013) speculate that these are conserved than that of females, but lower in centromeric regions (Sakamoto across the genus because Chinook salmon and rainbow trout are et al. 2000). Such different recombination patterns might be partly distantly related. In contrast, the metacentric chromosome Co12 is explained by occasional multivalent formation during male meiosis, not conserved in Chinook salmon and rainbow trout. We assumed in which crossovers between homeologous chromosomes are in- these structures in the subsequent discussion. creased in the telomeric regions while crossovers between homologous chromosomes are hindered in the centromeric regions through struc- Coho salmon map coverage, size, and differences in tural constraints (Sakamoto et al. 2000). In our study, however, sex-speciﬁc recombination suppressed recombination around the centromere and increased The coho salmon linkage map constructed in this study has 8681 recombination in telomeric regions were apparent for most male markers, spanning all predicted 30 linkage groups. This coverage is linkage groups, including the ones not likely involved in homeologous comparable with recently published maps across a number of salmon pairing. Some studies have also found notable clustering of markers in species (Lien et al. 2011; Everett et al. 2012; Miller et al. 2012; Brieuc centromeric regions for many male linkage groups (Nichols et al. et al. 2014; Gonen et al. 2014). We observed different map sizes in the 2003; Lien et al. 2011; Miller et al. 2012). In Atlantic salmon, high consensus female maps; the map constructed with combined haploid marker densities were also involved in regions close to the centromere and diploid families had a size of 6596.7 cM, which is signiﬁcantly for male linkage groups with a lower frequency of duplicated markers larger than the coho map created with haploids alone (3602.6 cM). (Lien et al. 2011). Recombination rates are known to differ between There are several reasons that might explain the differences such as the sexes in a wide range of species (Lenormand and Dutheil 2005); nonrandom missing values (Jorgenson et al. 2005), genotyping errors although homeologous chromosome pairing during male meiosis (Hackett and Broadfoot 2003), and numbers of markers mapped. could certainly account for some of the differences, the origin of the Potential bias against heterozygotes in RAD sequencing (Brieuc sex differences observed in this study still remains unclear. et al. 2014) may also partly explain the inﬂated map distances in Comparative genome mapping the haploid/diploid map, especially because the size of the map created with only haploid families in this study was much smaller. Comparative mapping provided insights into the process of chromo- Male salmonids are the heterogametic sex (Allendorf and Thorgaard somal evolution occurring after the whole genome duplication event, 1984). In this study, both the Y-linked growth hormone pseudogene and thisisthe ﬁrst study that characterizes chromosomal evolution and sex-determining gene, sdY, mapped to the telomeric region on between coho and Chinook salmon. Nine metacentric and nine the acrocentric chromosome, Co30. This ﬁnding is in agreement acrocentric chromosomes appear to be conserved between these two with previous ﬁndings (Phillips et al. 2005). Mapping has shown species. Among these conserved chromosomes, one metacentric that the sex chromosome is not conserved across the species, and (Co08 in coho and Ots12 in Chinook) and ﬁve acrocentric chro- that a small male-speciﬁc region including the sex determining gene mosomes are unique to coho and Chinook salmon, suggesting that Volume 4 September 2014 | Coho Salmon Genome Map | 1725 Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 Figure 4 Distribution of duplicated and nonduplicated loci along the 16 linkage groups with a high proportion of duplicated loci. Nonduplicated loci are represented in light gray. Duplicated loci are represented in dark gray (loci with one paralog polymorphic) or in black (loci with both paralogs polymorphic). The putative region containing the centromere is represented by the cross-hatched area. the structure of these linkage groups is ancestral to the divergence of served among all three species (Co01–Co07, Co09). The results these species relative to rainbow trout and Atlantic salmon. The support the hypothesis of Naish et al. (2013) that the arm rearrange- remaining linkage groups are not conserved, reﬂecting extensive ments that resulted in these metacentric chromosomes are ancestral to chromosomal rearrangements since coho and Chinook salmon the divergence of the species and could be conserved across the genus diverged. Oncorhynchus. There is one interesting extension to these earlier Syntenic relationships between the Chinook salmon and rainbow observations. One metacentric chromosome in Chinook salmon, trout maps permitted comparisons across the genus Oncorhynchus Ots08, sometimes occurs as a metacentric chromosome (Omy25p (Naish et al. 2013; Phillips et al. 2013). There are four acrocentric and q) or as two acrocentric arms (Omy25 and Omy 29) in rainbow chromosomes that are conserved across all three Oncorhynchus spe- trout (Figure 5). Here, we found that the homologous arms in coho cies (Co26–Co29). Similarly, eight metacentric chromosomes are con- salmon occur in two separate unrelated metacentric linkage groups 1726 | M. Kodama et al. Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 n Table 2 Homeologous chromosome arm pairs identiﬁed in coho salmon and the number of marker pairs supporting the homeologous relationship Number of Marker Homeology in Homeology in Homeology in Homeology in Known Phylogenetic Placement Pairs Supporting Chinook Salmon Rainbow Trout Atlantic Salmon Coho Salmon of Metacentric Arrangement Homeolog Pairings (Brieuc et al. 2014) (Phillips et al. 2006) (Lien et al. 2011) ‡ † Co01b–Co20b 15 Ots02q–Ots32 Omy17q –Omy13p Ssa02q–Ssa12qa B Co02a–Co13b 11 Ots03p–Ots23 Omy03p–Omy02p Ssa02p–Ssa05q B Co03b–Co08b 15 Ots04q–Ots12q Omy06q–Omy26 Ssa26–Ssa11qa B, C Co04b–Co11a 17 Ots06q–Ots01q Omy01q–Omy23 Ssa18qa–Ssa01qa B Co05a–Co16b 10 Ots07p–Ots14p Omy07p–Omy18p Ssa17qa–Ssa16qb B Co06b–Co10b 7 Ots09q–Ots27 Omy12q–Omy13q Ssa03q–Ssa06p B Co07a–Co12b 9 Ots11p–Ots34 Omy19p–Omy10q Ssa04p–Ssa08q B Co09a–Co19a 16 Ots15p–Ots17 Omy21p–Omy15q Ssa07p–Ssa17qa A Corresponding known homeologous relationships in Chinook salmon, rainbow trout, and Atlantic salmon are shown. The ﬁnal column designates known conservation of metacentric chromosome with high frequency of duplicated markers. Letter corresponds to phylogenetic placement in Figure 5. Possible earlier chromosomal arrangement (A) and subsequent rearrangement. Homeologous relationships with little or no support in Atlantic salmon (Lien et al. 2011). We have corrected the homeologous relationship between Omy17q and Omy13p; evidence suggests that this relationship was incorrectly reported as being between Omy17p and Omy13p in previous studies. (Co14a and Co15a) (Figure 5). In Atlantic salmon, these two arms are previous results provided evidence for the occurrence of centromet- fused together along with a third arm to form a large acrocentric ric inversion in Omy20 in rainbow trout following divergence be- chromosome (Figure 5). Robertsonian fusions are common and can tween rainbow trout and Chinook/coho salmon, and this also form acrocentric chromosomes; this outcome is likely more fre- chromosomal inversion may be exclusive to rainbow trout (Naish quent in Atlantic salmon than in Paciﬁc salmon (Phillips and Ráb et al. 2013; Ostberg et al. 2013; Brieuc et al. 2014). In the current 2001). Taken together, the conﬁgurations of these particular chromo- study, marker orders are fully conserved between coho and Chinook somes suggest they may have undergone recurrent fusions and ﬁssions salmon chromosome arms, Co25 and Ots25, respectively, further across species. supporting this previous observation (File S5). One metacentric and one acrocentric chromosome, Co09 and Co26, respectively, appear to be conserved across coho salmon, Conservation of reduced divergence between Chinook salmon, rainbow trout, and Atlantic salmon (Phillips et al. homeologous chromosomes across species 2009; Brieuc et al. 2014). Our study supports the previous ﬁndings Although our results conﬁrm that the divergence rates of homeologs that this metacentric chromosome is likely ancestral to the diver- following the whole genome duplication event have not been uniform gence of the two genera, Salmo and Oncorhynchus. It also appears (Brieuc et al. 2014), the key ﬁnding of this study is that the ancestral that this chromosome is conserved in Arctic charr and Brook charr metacentric chromosomes retain recently diverged duplicates and are within the genus Salvelinus (Timusk et al. 2011), both of which share the ones likely involved in recent or ongoing homeologous pairing a more recent common ancestor with Oncorhynchus. In addition, (Co01–Co07, conserved among all three Oncorhynchus species; Co09, Figure 5 Phylogenetic tree showing the orientation of homologous arms Ssa09qab, Omy25/29, Co14a, Co15a, and Ots08 in Atlantic salmon, rainbow trout, coho salmon, and Chinook salmon, respectively. Chromosomal rearrangements and homeologous relationships con- served across species at phylogenetic nodes A, B, C are summarized in Table 1 and Table 2. Volume 4 September 2014 | Coho Salmon Genome Map | 1727 Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 conserved among all four species). Such ﬁndings suggest that these ancestral metacentric chromosomes following the whole geno- homeologies may be preferentially retained between larger meta- me duplication event. The resources developed here will facilitate centric chromosomes (Phillips et al. 2009), and the involvement genome-wide studies in coho salmon, such as genome scans, QTL of at least one metacentric chromosome provides the stability mapping, and genome-wide association studies (Naish and Hard required for the formation of multivalents (Wright et al. 1980, 2008), as well as provide resources for studies concerning ecology 1983; Brieuc et al. 2014). These results support the hypothesis of and evolution in related salmon species. Phillips et al. (2009), which suggested that diploidization of chro- mosomes not involved in homeologous parings may have occurred ACKNOWLEDGMENTS in the ancestral salmonid before thedivergencebetween Salmo and We thank Isadora Jimenez-Hidalgo for assistance with genomic Oncorhynchus. We speculate that this process also differed to some data processing. Dan Drinan provided thoughtful discussions and extent following the divergence of the two genera. Although the helpful suggestions. We also thank Linda Park and Jim Myers for exact distribution of duplicated markers along chromosome arms help in setting up the initial crosses and David Rose for main- in Atlantic salmon has not yet been described (Lien et al. 2011), taining the lines. Finally, we are grateful to two anonymous only four out of eight homeologous pairings appear to share poly- referees and the Associate Editor for their very helpful comments morphic duplicated loci between the Atlantic salmon and Chinook regarding the ﬁrst draft of the manuscript. Initial experimental and coho salmon grouping (Table 2). lines were obtained from SweetSpring Salmon/Aquaseed Corpo- The implications of our ﬁndings for species divergence within the ration, suppliers of the Domsea broodstock and we thank Per subfamily Salmoninae will become clearer once we gain a greater Heggelund, Greg Hudson and Patty Munsell for providing these understanding of the role of duplicated regions in evolution. If lines. Funding for this study was provided by NOAA Fisheries/ the duplicated regions we detected have genes that permit greater Federal Columbia River Power System (FCRPS) Biological Opinion ﬂexibility for adaptation by providing the opportunity to acquire Remand Funds (to K.A.N. and J.J.H.), School of Aquatic and additional or novel functions (Soltis and Soltis 2000; Koop and Fishery Sciences, and Graduate Opportunities and Minority Davidson 2008; Van De Peer et al. 2009; Feldman et al. 2012; Alexandrou Achievement Program (GO-MAP, University of Washington) et al. 2013; Macqueen and Johnston 2014), then retention of particular award (to M.K.). The authors declare that they have no competing duplicated regions within certain lineages may explain their subse- interests. quent innovation and diversiﬁcation. However, the physical formation of metacentric chromosomes may inhibit diploidization because of LITERATURE CITED ongoing recombination; such chromosomes may continue to exhibit Alexandrou,M.A., B. A. Swartz, N.J.Matzke, andT.H.Oakley, 2013 Genome tetrasomic inheritance, thus becoming “evolutionary dead ends.” duplication and multiple evolutionary origins of complex migratory behavior Whole genome sequencing of duplicated chromosome arms in rain- in Salmonidae. Mol. Phylogenet. Evol. 69: 514–523. bow trout points toward the fact that duplicated protein coding loci Allendorf, F. W., and G. H. Thorgaard, 1984 Tetraploidy and the evolution of salmonid ﬁshes, pp. 1–27 in Evolutionary Genetics of Fishes, edited by have simply become lost through gradual change (Berthelot et al. B. J. Turner Plenum Press, New York. 2014); the conserved metacentric chromosomes may continue exhib- Allendorf, F. W., and R. G. 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Copyright: Copyright © 2022 Genetics Society of America
eISSN: 2160-1836
DOI: 10.1534/g3.114.012294
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Abstract

Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 INVESTIGATION Comparative Mapping Between Coho Salmon (Oncorhynchus kisutch) and Three Other Salmonids Suggests a Role for Chromosomal Rearrangements in the Retention of Duplicated Regions Following a Whole Genome Duplication Event ,1 † ‡ ,1 Miyako Kodama,* Marine S. O. Brieuc,* Robert H. Devlin, Jeffrey J. Hard, and Kerry A. Naish* *School of Aquatic and Fishery Sciences, University of Washington, Seattle, Washington 98105, Fisheries and Oceans Canada, West Vancouver, British Columbia, V7K 1N6, Canada, and National Marine Fisheries Service, Northwest Fisheries Science Center, Seattle, Washington 98112 ORCID ID: 0000-0002-3275-8778 (K.A.N.) ABSTRACT Whole genome duplication has been implicated in evolutionary innovation and rapid diversiﬁcation. KEYWORDS In salmonid ﬁshes, however, whole genome duplication signiﬁcantly pre-dates major transitions across the family, chromsome and re-diploidization has been a gradual process between genomes that have remained essentially collinear. rearrangements Nevertheless, pairs of duplicated chromosome arms have diverged at different rates from each other, suggesting comparative that the retention of duplicated regions through occasional pairing between homeologous chromosomes may genome have played an evolutionary role across species pairs. Extensive chromosomal arm rearrangements have been mapping a key mechanism involved in re-dipliodization of the salmonid genome; therefore, we investigated their inﬂuence RAD sequencing on degree of differentiation between homeologs across salmon species. We derived a linkage map for coho salmon salmon and performed comparative mapping across syntenic arms within the genus Oncorhynchus, and with the whole genome genus Salmo, to determine the phylogenetic relationship between chromosome arrangements and the retention duplication of undifferentiated duplicated regions. A 6596.7 cM female coho salmon map, comprising 30 linkage groups with 7415 and 1266 nonduplicated and duplicated loci, respectively, revealed uneven distribution of duplicated loci along and between chromosome arms. These duplicated regions were conserved across syntenic arms across Oncorhynchus species and were identiﬁed in metacentric chromosomes likely formed ancestrally to the diver- gence of Oncorhynchus from Salmo. These ﬁndings support previous studies in which observed pairings involved at least one metacentric chromosome. Re-diploidization in salmon may have been prevented or retarded by the formation of metacentric chromosomes after the whole genome duplication event and may explain lineage- speciﬁc innovations in salmon species if functional genes are found in these regions. Whole genome duplication (WGD) is a mutational mechanism that can Copyright © 2014 Kodama et al. serve as a primary driver of evolutionary novelty (Ohno 1970; Zhang doi: 10.1534/g3.114.012294 Manuscript received May 22, 2014; accepted for publication July 13, 2014; 2003; Crow and Wagner 2006; Lynch 2007; Edger and Pires 2009). published Early Online July 21, 2014. Changes in ploidy levels after WGD can lead to dramatic alterations This is an open-access article distributed under the terms of the Creative at the cellular and phenotypic level (Mayﬁeld-Jones et al. 2013) and Commons Attribution Unported License (http://creativecommons.org/licenses/ provide additional genetic variation for mutation, drift, and selection by/3.0/), which permits unrestricted use, distribution, and reproduction in any to act on. These evolutionary processes can result in new adaptations medium, provided the original work is properly cited. Supporting information is available online at http://www.g3journal.org/lookup/ and species diversiﬁcation (Van De Peer et al. 2009; Storz et al. 2013). suppl/doi:10.1534/g3.114.012294/-/DC1 Genome sequencing projects are increasingly revealing that WGD is Corresponding authors: School of Aquatic and Fishery Sciences, University of widespread in many key lineages, such as ﬂowering plants and verte- Washington, Seattle, Washington 98105. E-mail: [email protected]; and School brates, and represents an ongoing phenomenon in many species (Otto of Aquatic and Fishery Sciences, University of Washington, Seattle, Washington 98105. E-mail: [email protected] and Whitton 2000; Van De Peer et al. 2009). Understanding the Volume 4 | September 2014 | 1717 Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 processes governing the return to a diploid mode—diploidization—by lineages so that it will be possible to understand how duplication played comparing the genomes of species descended from a WGD event can a role in evolution of salmon, and whether key genomic regions might provide insights into the event’s role in evolutionary innovation and explain innovation across a subset of species. persistence of duplicated regions (Jaillon et al. 2009; Mayﬁeld-Jones It has been known for some time that one of the key mechanisms et al. 2013). for diploidization within the subfamilies Coregoninae and Salmoninae The stabilization of the duplicated genome through diploidization (which includes Salmo, Salvelinus, and Oncorhynchus) has occurred can be achieved by rearrangements (such as translocations, ﬁssions, through Robertsonian rearrangements of whole chromosome arms fusions, and transpositions), gene loss, and sequence deletion and (Ohno 1999; Phillips and Ráb 2001). Most chromosome arms are divergence (Hufton and Panopoulou 2009; Schubert and Lysak 2011). syntenic between Salmoninae species, and the combined efforts of These processes tend to reduce the similarity of the duplicated ohnologs genome mapping and karyotyping have permitted alignment of chro- (Wolfe 2001), and the homeologous chromosomes resulting from mosome arms among several species within this subfamily (Danzmann WGD, but the exact mechanisms vary across lineages (Hufton and et al. 2005; Phillips et al. 2009; Lubieniecki et al. 2010; Lien et al. Panopoulou 2009). Whole genome duplication has been frequently 2011; Timusk et al. 2011; Guyomard et al. 2012; Naish et al. 2013; implicated in evolutionary innovation in eukaryotic genomes of Phillips et al. 2013). Chromosome arm number is largely conserved paleopolyploids (ancient polyploids) (Ohno 1999; Lynch and Conery (NF = approximately 100) but the numbers of chromosomes vary 2000; Jaillon et al. 2004; Cañestro et al. 2013), but evidence in plants substantially across species as a result of the Robertsonian rearrange- suggests that the rate of diversiﬁcation and extinction of neopolyploids ments (Phillips and Ráb 2001). The exception is Atlantic salmon, can be lower than that of related diploid lineages (Mayrose et al. with reduced chromosome arm number compared with the other 2011). Increasing the number of studies on mesopolyploids— species (NF = 72–74). However, large syntentic blocks within the organisms in the intermediate process of diploidization (Mayﬁeld-Jones arms of this species correspond to whole arms in other members of et al. 2013)—will provide a clearer understanding of contribution of the Salmoninae, making comparative studies feasible across this sub- WGD events to evolutionary innovation. family as a whole. Salmonid ﬁshes are descended from a whole genome duplication Comparative mapping between Chinook salmon (O. tshawytscha) event in an autotetraploid ancestor (Allendorf and Thorgaard 1984), and rainbow trout (O. mykiss) has revealed evidence for the retention distinct from the second round of duplication (2R) that occurred basal of at least eight metacentric chromosomes and four acrocentric chro- to the vertebrate tree and the third round (3R) early in the evolution of mosomes that are ancestral to species divergence within the genus the teleosts 225 to 333 million years ago (Hurley et al. 2007; Postlethwait Oncorhynchus (Naish et al. 2013; Phillips et al. 2013). One of the eight 2007; Santini et al. 2009; Near et al. 2012). This fourth round (4R) of metacentric chromosomes and one of the acrocentric chromosomes duplication was recently estimated as occurring 88–103 million years are also ancestral to the divergence between Salmo and Oncorhynchus. ago (Macqueen and Johnston 2014; see also Crête-Lafrenière et al. 2012; There is also further evidence for another ancestral metacentric and Alexandrou et al. 2013; Berthelot et al. 2014). Although the genomes of an ancestral acrocentric chromosome, but these have undergone sub- these species are returning to a stable diploid state through chromo- sequent rearrangements within at least one descendant species (Naish somal rearrangements and divergence of homeologous chromosomes, et al. 2013; Ostberg et al. 2013; Brieuc et al. 2014). High-density evidence of tetrasomic inheritance in males and extensive rearrange- linkage maps have revealed that recently diverged or undifferentiated ments among chromosomes has shown that restoration of diploidy is duplicated loci are not uniformly distributed among chromosomes not yet complete (Wright et al. 1983; Allendorf and Thorgaard 1984; (Atlantic salmon, Lien et al. 2011; Chinook salmon, Brieuc et al. Allendorf and Danzmann 1997). Comparative genome sequencing 2014), and the biased distribution of duplicated loci along chromo- between ohnologs in rainbow trout has revealed extensive collinearity some arms provides evidence that pairs of homeologous arms have between the duplicated chromosomes, characterized by loss of ap- diverged at different rates from each other (Brieuc et al. 2014). This proximately half the protein-coding regions through pseudogenization ﬁnding conﬁrms observations from previous studies conducted with but retention of most of the duplicated miRNA genes (Berthelot lower marker densities (for example, Danzmann et al. 2005; Guyomard et al. 2014). et al. 2012). Intriguingly, homeologous pairings have been observed The role of the WGD event in salmonid trait innovation and to include at least one metacentric chromosome (Wright et al. 1983), diversiﬁcation is unclear. Recent evidence based on molecular clock and duplicated markers map to such chromosomes (Brieuc et al. estimates suggest that duplication is unlinked to a major transition in 2014), supporting the view that metacentric chromosomes play an life history, anadromy (Alexandrou et al. 2013; Macqueen and Johnston important role in homeologous pairing (Phillips et al. 2009; Brieuc 2014), and preceded rapid species diversiﬁcation by several million years et al. 2014). These observations raise the interesting possibility that (Berthelot et al. 2014; Macqueen and Johnston 2014). Rather, both the evolutionary timing of metacentric chromosome formation dur- transitions appear to correspond with climate cooling (Macqueen and ing re-diploidization after the WGD event might inﬂuence the re- Johnston 2014). Re-diploidization has been subsequently characterized tention, and hence the evolutionary role, of duplicated regions across as a gradual process unlinked to signiﬁcant genome rearrangements species. Therefore, by comparing chromosomal arrangements and (Berthelot et al. 2014). However, it has also been argued that the du- distribution of duplicated regions across salmon species, we aim to plication event might have provided the raw material for evolution to provide a contextual framework for the further investigation of loci act on, and that differential divergence of duplicated regions might have involved in species diversiﬁcation. promoted speciation at varying time points (Macqueen and Johnston The development of a high-density linkage map for a less-described 2014). Large-scale genome characterization in the salmonids is increas- salmon species will contribute further information regarding chromo- ingly revealing the location of genes or regions that may have played some rearrangements that have already been deﬁned in several salmon a role in adaptation and diversiﬁcation (Davidson et al. 2010; Bourret species and enhance our understanding of the timing of these et al. 2013; Larson et al. 2013). Therefore, it is important to combine arrangements in a phylogenetic context. Examining the distribution these studies with an understanding of the mechanism and timing of of duplicated regions across individual chromosome arms in a second divergence between homeologous chromosome arms across salmon species—beyond Chinook salmon (Brieuc et al. 2014)—will also 1718 | M. Kodama et al. Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 facilitate an understanding of the relationship between timing of meta- Satsop River in the Southwest Washington Coast/Lower Columbia centric chromosome formation and diversiﬁcation between homeologs. ESU; and (4) Chehalis River located in British Columbia, Canada Coho salmon (Oncorhynchus kisutch) is a species whose genome has (49299N, 121949W). not been extensively described to date. A low-density linkage map of An initial framework map was constructed using two haploid coho salmon has been constructed using microsatellites (McClelland crosses (haploid family 1 and 2) comprising 64 and 62 individuals, and Naish 2008), but this map is not sufﬁciently resolved to study the respectively. These types of crosses have the advantage of identifying consequences of WGD because there is a low number of duplicated duplicated loci, because these loci will appear as heterozygotes in loci mapped. A high-density map in this species is feasible, given re- the offspring if they are polymorphic, while nonduplicated loci will cently emerged sequencing technologies (for example, Baird et al. be homozygous. Haploid families were created at the University of 2008). Coho and Chinook salmon are sister species (Crête-Lafrenière Washington hatchery facility (47659N, 122319W), following the pro- et al. 2012); therefore, comparative mapping across coho and Chinook tocol of Thorgaard et al. (1983). Embryos were collected before hatch- salmon, as well as more divergent species in the genus Oncorhynchus ing and preserved in 100% ethanol. and Salmo, will help validate the hypotheses and provide more robust Sex-speciﬁc maps were created using two F3 outbred diploid evidence on the process of chromosomal evolution following WGD. crosses and one outbred diploid cross. Speciﬁcally, F3 diploid crosses The aim of our research is to determine the relationship between were created from a cultured line originally derived from an outbred chromosome arrangements and the retention of recently diverged or cross between two populations in Washington State (McClelland and undifferentiated duplicated regions by deriving a linkage map for coho Naish 2010). F0 males were collected from Bingham Creek in South- salmon and comparing this map with those of Chinook salmon, west Washington (47159N, 123409W). F0 females were obtained rainbow trout, and Atlantic salmon. We therefore constructed high- from the Domsea broodstock farm. Two F3 crosses were established density linkage maps for coho salmon using restriction site–associated in December 2010 by mating two F2 full-sibs to create one family, and DNA (RAD) sequencing (Baird et al. 2008). By achieving this objec- two F2 half-sibs to create the other. The two families comprised 55 tive, we also produced a reference database of RAD markers that can and 67 offspring, respectively, (diploid family 1 and 2). An additional be used for alignment of sequences generated in future work, and diploid outbred cross was created from an aquaculture population described in detail the properties of the coho linkage map. Coho using coho salmon derived from the Chehalis River located in British salmon chromosome arms were identiﬁed by comparative mapping Columbia, Canada (49299N, 121949W). Speciﬁcally, cultured indi- with Chinook salmon using markers in common between the species, viduals were repeatedly backcrossed with wild individuals from the and whole chromosome arm homologies were described across spe- Chehalis River for six generations, and diploid crosses were created in cies to improve our current understanding of chromosome arm rear- January 2011. One diploid family from these crosses comprising 99 rangement within the genera Oncorhynchus and Salmo.Linkage individuals was used for further analyses (diploid family 3). groups representing homeologous chromosome arms in coho salmon DNA extraction, sequencing, and ampliﬁcation of were discovered using duplicated markers, and regions of duplicated sex-linked markers markers were compared across species to determine the extent to Genomic DNA from the sampled individuals was extracted using which these regions were conserved across lineages. By identifying the DNeasy extraction kit (QIAGEN, Valencia, CA) following the genomic regions that are in the process of diploidization and linking manufacturer’s procedures. The DNA was digested with SbfI, and these regions to chromosomal rearrangements, we aim to provide a 6-nucleotide barcode was added to each sample for individual iden- the basis for determining the role of duplication in maintaining tiﬁcation following protocols described by Baird et al. (2008). Between ongoing polymorphisms and explaining processes of diversiﬁcation 24 and 36 individuals were pooled in a single library and sequenced across Salmoninae species. with 100-bp single-read lengths using the Illumina HiSequation 2000 sequencer. The sequences were separated by individual using MATERIALS AND METHODS PROCESS_RADTAGS implemented in STACKS (Catchen et al. Justiﬁcation and description of sample collection and 2011, 2013). Because the quality score of sequences decreased be- experimental crosses yond 74 nucleotides, sequences were trimmed to 74 nucleotides to remove low-quality sequences. A locus was deﬁned as a 74-nucleotide A two-step approach was used to develop genomic resources and RAD sequence for the purpose of this study. construct linkage maps. First, RAD sequences from individuals sampled Genetic sex was determined in the two diploid families (diploid from multiple populations were used to construct a reference da- family 1 and 2) using a Y-linked growth hormone pseudogene (GH5 tabase for aligning loci across mapping families. This reference and GH6) (Devlin et al. 2001) and sex-determining gene, sdY (sdY database was screened for errors, duplicated loci, and repeat regions E2S1 and sdY E2AS4) (Yano et al. 2012). Polymerase chain reactions following approaches described by Brieuc et al. (2014), and loci were were performed for each set of primers using a QIAGEN Multiplex subsequently named to ensure consistency across mapping families. PCR kit. Speciﬁcally, reaction mixtures consisted of 10–200 ng geno- Second, speciﬁc cross types were used to perform the mapping: mic DNA, 1· QIAGEN Multiplex PCR Master Mix, 0.25 mMofGH5 gynogenetic haploid crosses were used to map both duplicated and and GH6, or 0.4 mM of sdY E2S1 and sdY E2AS4, comprising a total nonduplicated loci, and diploid crosses were used to construct sex- volume of 10 ml. Cycling conditions consisted of a 15-min initial speciﬁc maps. activation step at 95, 30 cycles of 30-s denaturing step at 94,90-s The reference database of RAD loci was constructed using annealing step at 60, a 60-s extension step at 72, and a 10-min ﬁnal sequences from 583 individuals representing four populations in extension step at 72. the Paciﬁc Northwest of the United States and Canada: (1) the Washington Department of Fish and Wildlife’s(WDFW) Wallace Reference database of RAD loci River Hatchery (47879N, 121719W); (2) the Domsea broodstock population, which originated in 1973 and 1974 from Wallace River RAD loci that are found within repeat regions, and loci containing Hatchery; (3) Bingham Creek (47159N, 123409W), a tributary to the repeat units, can confound the identiﬁcation of unique loci. Therefore, Volume 4 September 2014 | Coho Salmon Genome Map | 1719 Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 a reference sequence database comprising a set of pre-screened RAD a maximum of three nucleotide mismatches per locus. Subsequently, loci was ﬁrst created from the survey of four populations following polymorphic loci were identiﬁed in each diploid family using STACKS, bioinformatic procedures fully described by Brieuc et al. (2014). This and genotypes at these loci were determined when alleles were se- database served as a resource for aligning loci across studies. In brief, quenced with a depth greater than 10· per individual. sequences from all 583 individuals sampled across the four popula- STACKS uses a maximum likelihood statistical model to identi- tions described previously were extracted using STACKS 0.9995 fy sequence polymorphisms and determine individual genotypes (Catchen et al. 2011). Both monomorphic and polymorphic loci that (Catchen et al. 2011, 2013). This approach can be biased toward were sequenced with a depth greater than 5· in more than 496 indi- heterozygous genotypes when sequence depths differ between the viduals (85%) were retained in a temporary database and used for two alleles. To correct this bias against heterozygous genotypes, geno- further screening. types were corrected after running STACKS with the Python script Loci in the temporary database that corresponded to repeat regions developed by Brieuc et al. (2014). Speciﬁcally, individuals were de- and loci containing repeat units were removed using two alignment- termined as heterozygotes at a locus if both alleles had a depth of more based strategies following the protocol of Brieuc et al. (2014). First, than two and the total read depth was 10· or greater. loci in the temporary database were aligned against themselves using Linkage mapping BOWTIE (Langmead et al. 2009) by allowing a maximum of three nucleotide mismatches per locus. A locus that aligned to several loci, Linkage maps in all haploid and diploid families were constructed or a locus that did not align to itself, was removed from the temporary using software for genetic mapping, ONEMAP 2.0-3 (Margarido et al. database. Then, a BLAST search (Altschul et al. 1990) of the tempo- 2007), implemented in R version 3.0.2 (R Development Core Team rary database was conducted against itself. Loci that did not return 2013). Because coho salmon have 30 chromosome pairs (Phillips and a match, or loci where the best matches were not themselves, were Ráb 2001), each mapping family was expected to have at least 30 removed from the temporary database. linkage groups. Linkage groups were named “Co,” following the con- Using the updated temporary database of RAD loci, polymorphic vention used in mapping studies in salmonids; this practice uses ab- duplicated loci were identiﬁed based on two haploid families. First, breviated common names for groups that are not yet anchored to sequences from these haploid families were aligned to the temporary chromosomes (Danzmann et al. 2005; Naish et al. 2013). RAD loci database using BOWTIE, allowing a maximum of three nucleotide with 20% or less missing values among individuals within a family mismatches per locus. Sequences from the haploid individuals that were used for linkage analyses, and these loci were assigned to linkage aligned to more than one locus in the database could not be con- groups in each family separately using a minimum log of odd ratio ﬁdently relied on in further analyses; they were thus identiﬁed as (LOD) score of 4.0 and a maximum recombination fraction of 0.25. “black-listed” loci and removed from the temporary database. Sub- The LOD score was subsequently increased by 1.0 until the number of sequently, polymorphic loci sequenced with a depth greater than 10· linkage groups reached 30 or higher. An integrated haploid map was per haploid individual were identiﬁed using STACKS and retained for ﬁrst constructed from the two haploid families using MERGEMAP further screening. Among these polymorphic loci, a locus was identi- (Wu et al. 2011) because genotypes at duplicated loci were only de- ﬁed as being putatively duplicated when more than one haploid off- termined in these families. This integrated haploid map was later used spring in a family was heterozygous at this particular locus (Brieuc to examine the distribution of duplicated loci across all linkage groups et al. 2014). A ﬁnal reference database comprising named duplicated and identify linkage groups involved in recent or ongoing homeologous and nonduplicated loci, as well as loci removed from the alignment- pairing. based screening steps and “black-listed” loci, was created. Recombination rates in male salmonids tend to be lower than those observed for females (Sakamoto et al. 2000; Ostberg et al. 2013), Genotyping of individuals in map crosses but these differences tend to decrease with high marker density and Haploid individuals were genotyped at both nonduplicated and genome coverage (Rexroad et al. 2008; Lien et al. 2011). We used the duplicated loci. Sequences from all haploid individuals were aligned female meiosis from the three diploid families to estimate marker to the nonduplicated and duplicated loci from the ﬁnal reference order in these crosses. The data from all haploid and diploid female database using BOWTIE by allowing a maximum of three nucleotide parents were then combined to calculate an integrated female haploid/ mismatches per locus. In haploids, we have shown reliable identiﬁ- diploid map using MERGEMAP. cation of single loci that have up to three SNPs; we have conﬁrmed Ordering markers in the diploid male map was computationally this result with genome mapping. To remain consistent, we used up to difﬁcult, potentially due to reduced recombination and occasional three mismatches so that we could differentiate between nonduplicated tetrasomic inheritance in males (Allendorf and Danzmann 1997). loci and duplicated loci. Both this study and a previous one (Brieuc et al. Therefore, information from the integrated female map constructed 2014) have shown that very reliable linkage results can be obtained in with haploid and diploid mothers was used to infer the order and map haploids using these criteria. Polymorphic loci sequenced with a depth the male meiosis in the three diploid families (diploid family 1, 2, 3). greaterthan10· per individual were identiﬁed using STACKS. Both Polymorphic loci in common between the male parents and the inte- nonduplicated and duplicated markers in the haploid families were used grated female map, as well as the Y-linked growth hormone pseudogene for mapping, described below and following the protocol of Brieuc et al. and sex-determining gene, sdY, were grouped using a log of odd (2014). Polymorphic duplicated loci were mapped when one of the ratio (LOD) score of 4.0 and a maximum recombination fraction of paralogs was polymorphic (OPP: one paralog polymorphic, parental 0.25 using ONEMAP. The LOD score was subsequently increased genotypes aa and ab or aa and bc) or when both paralogs were poly- by 1.0 until the number of linkage groups reached 30 or higher. morphic (BPP: parental genotypes ab and ac or ab and cd; see Table 1 Grouped loci were then ordered based on the known order on the in Brieuc et al. 2014). integrated female map using the make.seq and map functions imple- Diploid individuals were only genotyped at nonduplicated loci. mented in ONEMAP. The position of a Y-linked growth hormone Sequences from all diploid individuals were aligned to the nonduplicated pseudogene and sex-determining gene, sdY, on the male map was loci identiﬁed in the ﬁnal reference database using BOWTIE by allowing estimated in the two diploid families (diploid family 1 and 2) using 1720 | M. Kodama et al. Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 the try.seq and map functions implemented in ONEMAP. The data ﬁnal reference database comprising 52,936 nonduplicated loci and from all diploid male parents were then combined to calculate an 7235 duplicated loci, as well as the 9866 loci that were removed by integrated male map using MERGEMAP. screening, are given in Supporting Information, File S1. Linkage mapping Comparative mapping with Chinook salmon and An initial framework map was constructed with two haploid families. comparison with other salmonid species Haploid family 1 and 2 had 3976 and 4048 biallelic polymorphic RAD The reference database for coho salmon containing duplicated and loci, respectively, comprising a total of 6652 unique RAD loci. Among nonduplicated RAD loci was aligned to the 54,937 ﬁltered RAD loci these loci, a mixture of duplicated and nonduplicated loci (3897 loci in identiﬁed in Chinook salmon (Brieuc et al. 2014) using BOWTIE, haploid family 1; 3996 loci in haploid family 2) were successfully allowing no more than three nucleotide mismatches per locus. Ho- assigned to 30 linkage groups with a LOD score of 5.0 to 7.0. The total mologies between Chinook and coho salmon were determined by map length for the haploid family 1 and 2 was 3040.1 cM and 3185.5 examining the chromosomal arm locations of shared loci between cM, respectively. The integrated haploid map had 5377 nonduplicated the two species. Putative centromere positions on coho linkage groups markers and 1266 duplicated markers with a total map length of were estimated based on markers mapped in the gynogenetic diploid 3602.6 cM (File S2). families in Chinook salmon (Brieuc et al. 2014). The order of mapped Linkage analyses were conducted in the diploid families following loci between the Chinook and coho salmon map was compared to the construction of the integrated haploid map. Diploid family 1, 2, determine if marker orders for chromosomes or chromosomal arms and 3 had 1360, 1176, and 1931 biallelic nonduplicated loci that were between the species were conserved. Finally, homologies identiﬁed polymorphic in each female parent, respectively. Among these loci, between Chinook and coho salmon were used to infer homologies a set of loci (1214 loci in diploid family 1; 1138 loci in diploid family 2; across coho salmon, rainbow trout, and Atlantic salmon using molec- 1765 loci in diploid family 3) were successfully assigned to 30 linkage ular markers in common between published maps (Phillips et al. 2009; groups with a LOD score of 4.0 to 8.0. The total map length for the Lien et al. 2011; Miller et al. 2012; Brieuc et al. 2014). diploid family 1, 2, and 3 was 3714.1 cM, 3068.9 cM, and 5047.2 cM, respectively. Although the diploid family 3 had the largest total map Homeologous relationships and the distribution of length, it also had the highest number of markers mapped. Because duplicated loci across genomes more recombination events are captured with more markers (Liu As we pointed out, two categories of duplicated loci were identiﬁed in 1998), it is not surprising that the diploid family 3 had the largest this study, where one of the paralogs was polymorphic (OPP) or both total map length. Finally, data from the haploid parents and dip- paralogs were polymorphic (BPP). Duplicated loci with both paralogs loid female parents were combined; an integrated haploid/diploid polymorphic (BPP) were used to infer homeologous linkage groups female mapmeasured6596.7cM, and it comprised 7415 non- because both paralogs could be mapped. The positions of duplicated duplicated markers and 1266 duplicated markers (Table 1; Figure 1; loci were subsequently examined on the integrated haploid map to File S2). determine whether there was a bias in the distribution of these loci The male meioses were mapped using linkage analyses in the across linkage groups. A kernel smoothing approach using a sliding diploid families. Among the 8681 loci placed on the integrated window of 2 cM was used to determine whether there was a regional haploid/diploid female map, diploid family 1, 2, and 3 had 846, 814, bias in distribution of these loci for each linkage group following and 879 polymorphic loci in common for each male parent. Among methods described by Brieuc et al. (2014). Homeologous relationships these loci, a set of loci (792 loci in diploid family 1; 790 loci in diploid detected in coho salmon were also compared with those identiﬁed in family 2; 851 loci in diploid family 3), as well as the Y-linked growth Chinook and Atlantic salmon (Lien et al. 2011; Brieuc et al. 2014). hormone pseudogene and sex-determining gene, sdY, were success- fully assigned to 30 linkage groups with a LOD score of 4.0 to 7.0. Both the growth hormone pseudogene and sdY mapped to the RESULTS telomeric region of the linkage group, Co30. All linkage groups were Reference database of RAD loci successfully merged, except for Co22, which was split into two A reference database comprising a unique set of RAD loci was created linkage groups (Co22_1 and Co22_2) (File S2). The number of for the purpose of sequence alignment and identiﬁcation of poly- markers in common between the integrated male and female maps morphisms across individuals. A total of 70,037 loci were sequenced varied for each linkage group, ranging from 25 to 106 markers per with a depth greater than 5· per individual in at least 496 individuals. linkage group (File S3). The male map had a total map length of These loci formed the temporary reference database of RAD loci, and 4141.76 cM (File S3). they were retained for further screening. Sequence alignment using The comparison between the male and female linkage groups BOWTIE showed that 4075 loci did not align uniquely to themselves reﬂected different recombination patterns between the sexes (Figure 2; and likely corresponded with repeat regions; therefore, these loci were File S4). Although telomeres were not mapped in males due to a lack removed from the temporary database. After performing the BLAST of duplicated markers, many male linkage groups were expanded in search of the temporary reference database against itself, 2085 loci did size toward the terminal regions relative to the female, as seen by the not return a match or the best match score was not the locus itself. It increased distance in these regions reﬂecting more recombination was possible that these loci contained repeat sequences; therefore, events. Such patterns were particularly prominent for several linkage these loci were also removed from the temporary reference database. groups (Co02, Co04, Co05, Co08–Co10, Co13–Co15, Co17–Co19, Sequences from the haploid individuals were aligned to the reference Co21–Co29). Although qualitative, there was also evidence of sup- database using BOWTIE; 3706 loci from the haploid individuals pressed recombination around the region containing the centromere aligned to several other loci, and these loci were thus black-listed in the male map compared with female integrated map for all linkage and removed from the reference database. Additionally, 7235 loci were groups. The male map had reduced distance in these regions com- identiﬁed as polymorphic duplicated loci in the haploid families. The pared to the female map. Volume 4 September 2014 | Coho Salmon Genome Map | 1721 Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 n Table 1 Description of the Coho salmon consensus linkage map constructed with haploid and diploid female parents and comparison with chromosome arms of Chinook salmon, rainbow trout, and Atlantic salmon Chinook Rainbow Trout Atlantic Salmon Chromosomal Coho Coho Chromosome Chromosome Chromosome Rearrangement Linkage Number of Linkage (Philips et al. 2013; (Philips et al. 2009; (Danzmann et al. 2008; Conserved Group Size (cM) Markers Arms Brieuc et al. 2014) Brieuc et al. 2014) Philips et al. 2009) Across Species Co01 267.51 393 Co01a Ots02p Omy17p Ssa02q B, metacentric Co01b Ots02q Omy17q Ssa12qb Co02 248.6 344 Co02a Ots03p Omy03p Ssa02p B, metacentric Co02b Ots03q Omy03q Ssa25 Co03 274.51 360 Co03a Ots04p Omy06p Ssa24 B, metacentric Co03b Ots04q Omy06q Ssa26 Co04 250.26 395 Co04a Ots06p Omy01p Ssa16qa B, metacentric Co04b Ots06q Omy01q Ssa18qa Co05 268.59 376 Co05a Ots07p Omy07p Ssa17qb B, metacentric Co05b Ots07q Omy07q Ssa22 Co06 267.8 415 Co06a Ots09p Omy12p Ssa13qb B, metacentric Co06b Ots09q Omy12q Ssa03q Co07 211.09 241 Co07a Ots11p Omy19p Ssa04p B, metacentric Co07b Ots11q Omy19q Ssa01p Co08 295.21 382 Co08a Ots12p Omy11p&q Ssa20qa C, metacentric Co08b Ots12q Omy26 Ssa11qb Co09 196.03 207 Co09a Ots15p Omy21p Ssa07p A, metacentric Co09b Ots15q Omy21q Ssa07q Co10 239.27 346 Co10a Ots01p Omy04p Ssa23 — Co10b Ots27 Omy13q Ssa06q Co11 280.26 419 Co11a Ots01q Omy23 Ssa01qa — Co11b Ots29 Omy15p Ssa29 Co12 215.12 286 Co12a Ots05p Omy08p Ssa15qa — Co12b Ots34 Omy10q Ssa08q Co13 288.32 350 Co13a Ots05q Omy05q Ssa10qa — Co13b Ots23 Omy02p Ssa05q Co14 270.54 356 Co14a Ots08p Omy25p Ssa09qa — Co14b Ots31 Omy14p Ssa14qb Co15 282.89 355 Co15a Ots08q Omy25q (Omy29) Ssa09qb — Co15b Ots13q Omy27 Ssa20qb Co16 211.31 220 Co16a Ots10p Omy09p Ssa18qb — Co16b Ots14p Omy18p Ssa16qb Co17 181.92 292 Co17a Ots13p Omy18q Ssa27 — Co17b Ots16q Omy09q Ssa15qb Co18 209.02 323 Co18a Ots14q Omy24 Ssa09qc — Co18b Ots16p Omy11p Ssa19qa Co19 217.65 315 Co19a Ots17 Omy15q Ssa17qa — Co19b Ots21 Omy14q Ssa05p Co20 203.33 247 Co20a Ots24 Omy16p Ssa19qb — Co20b Ots32 Omy13p Ssa12qa Co21 130.25 184 Co21 Ots18 Omy04q Ssa06p C, acrocentric Co22 194.97 243 Co22 Ots19 Omy02q Ssa10qb C, acrocentric Co23 212.27 213 Co23 Ots20 Omy05p Ssa01qb C, acrocentric Co24 127.18 187 Co24 Ots22 Omy16q Ssa13qa C, acrocentric Co25 171.35 196 Co25 Ots25 Omy20p+q SSa08p & Ssa28 A, acrocentric Co26 184.21 225 Co26 Ots26 Omy22 Ssa21 A, acrocentric Co27 164.56 198 Co27 Ots28 Omy28 Ssa03p B, acrocentric Co28 169.82 214 Co28 Ots30 Omy10p Ssa04q C, acrocentric Co29 173.74 181 Co29 Ots33 OmySex Ssa11qa B, acrocentric Co30 189.15 218 Co30 Ots10q Omy08q Ssa14qa — Total 6596.7 8681 Linkage groups (Co) were randomly assigned numbers, and arm names are given as “a” and “b.” Homologous arms in Chinook salmon, rainbow trout, and Atlantic salmon are based on chromosome names for each species (Ots, Omy, and Ssa, respectively), with known orientations (p is the short arm, q is the long arm). and denote inferred relationship. There were no markers in common between Co07a and Ots11p( ), and there are markers in common between Co12b and Ots34/Ots11p( ). A chromosomal arm that is composed entirely of ribosomal DNA. The ﬁnal column designates chromosomal rearrangements conserved across species; letter corresponds to phylogenetic placement in Figure 5. Incompletely resolved relationships between Atlantic salmon and rainbow trout according to published studies. might include a section of Ssa19qa. 1722 | M. Kodama et al. Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 Figure 1 Graphical representation of 30 consensus linkage groups in haploid and diploid female coho salmon. Co01 to Co20 are metacentric, and Co21 to Co30 are acrocentric, inferred from comparative mapping. The size of linkage groups ranges from 127.18 to 295.21 cM (Kosambi), and each line corresponds to the location of one or more markers. The putative location of the centromere, estimated by comparative mapping with Chinook salmon, is represented in red. Comparative mapping with Chinook salmon and chromosome in Chinook salmon. Four metacentric linkage groups comparisons with other salmonid species in coho salmon (Co15–Co18) comprise arms that are found in two separate metacentric chromosome pairs in Chinook salmon. Two We mapped 664 RAD loci in coho salmon that had been previously metacentric linkage groups (Co19, Co20) comprise two acrocentric placed on the Chinook salmon map, which permitted the identiﬁ- chromosome pairs in Chinook salmon. Finally, one acrocentric link- cation of homologous chromosomal arms between the two species age group (Co30) corresponds to an arm that is a part of a meta- (Table 1). On the basis of this comparison, we also identiﬁed the centric chromosome pair in Chinook salmon. putative locations of centromeres within coho salmon linkage groups The orders of the RAD loci on the Chinook and coho salmon maps (Figure 1). Two homologous relationships between the species were were compared across each linkage group or for each chromosome inferred. An arm of the linkage group Co07a had three markers that arm to determine whether any chromosomal inversions occurred after mapped to Ots34 in Chinook salmon. However, Co12b had six divergence between the species. There was a strong linear relationship markers that mapped to Ots34 and three markers that mapped to among mapped loci for all the linkage groups or arms (File S5), suggest- Ots11p. Ots11p and Ots34 are likely involved in recent or ongoing ingthatmarkerorderswereconserved forall chromosomesorchro- homeologous pairing in Chinook salmon (Brieuc et al. 2014); there- mosomal arms. Such analyses provide additional evidence for the fore, it was not surprising that loci on Ots34 mapped to both homol- occurrence of centrometric inversion in Omy20 in rainbow trout after ogous arms in coho salmon. In this case, we assumed that Co07a was divergence between rainbow trout and Chinook/coho salmon, and homologous to Ots11p, and Co12b was homologous to Ots34 for this chromosomal inversion may be exclusive to rainbow trout (Naish reasons given in the Discussion. et al. 2013; Ostberg et al. 2013; Brieuc et al. 2014). Comparative mapping with Chinook salmon permitted inference The homologies we observed between Chinook and coho salmon of the structure of coho linkage groups. Twenty linkage groups in coho permitted alignment of coho linkage groups to those of rainbow trout salmon corresponded to putative bi-armed metacentric chromosomes, and the Atlantic salmon, and the results are summarized in Table 1. and 10 linkage groups corresponded to putative uni-armed acrocentric Three acrocentric and eight metacentric chromosomes were con- chromosomes (Figure 1). These inferred structures are in agreement served among coho salmon, Chinook salmon, and rainbow trout. with the known chromosome structures in coho salmon (Phillips and Comparison between the Oncorhynchus species and the Atlantic Ráb 2001). The short (p) arm of an acrocentric chromosome is usually salmon revealed that one metacentric chromosome and one acrocen- uncharacterized in mapping studies because there are often insufﬁcient tric chromosome were conserved across all compared species. markers describing this region (Brieuc et al. 2014). In this study, we identiﬁed the small arm for two putative acrocentric chromosomes Homeologous relationships and the distribution of (Co22, Co29) through comparative mapping with Chinook salmon. duplicated loci across linkage groups Comparative mapping between the Chinook and coho salmon The identiﬁcation of linkage groups involved in homeologous pairing, maps also provided information on chromosomal arrangements that as well as the localization of duplicated loci across individual linkage are shared between the two species. Eighteen chromosomes are con- groups, was examined using the integrated haploid female map. A served between the species (Table 1); speciﬁcally, nine metacentric total of 1266 duplicated loci (1066 OPP and 200 BPP) were placed on chromosomes and nine acrocentric chromosomes were conserved this map. These loci were not distributed evenly among the linkage between the species. The remaining chromosome structures likely support independent Robertsonian rearrangements that occurred after groups (x test for uniform distribution across linkage groups, after descent from a common ancestor. correction for the number of markers per linkage group: p-value 0, Five metacentric linkage groups in coho salmon (Co10–Co14) con- df = 29); 87.0% of the duplicated loci were located on 16 linkage sist of one acrocentric chromosome and one arm from a metacentric groups (Figure 3). There was a bias in distribution of these loci along Volume 4 September 2014 | Coho Salmon Genome Map | 1723 Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 Figure 2 Comparison of map distances between com- mon markers mapped in male and female coho salmon. Linkage groups Co04 (A), Co17 (B), Co18 (C), and Co26 (D) are given as examples. The putative region contain- ing the centromere is represented by the cross-hatched area. All linkage groups are presented in File S4. the 16 linkage groups; duplicated loci were mostly found in the distal homeologous pairs diverged from each other at different rates following regions of all 16 linkage groups (Figure 4). Homeologies were identi- the whole genome duplication event. Regions of the genome with poly- ﬁed between putative chromosome arms using marker pairs in which morphic duplicated markers were found on the same eight pairs of both paralogs were polymorphic (Table 2). All eight homeologous homologous chromosome arms (16 arms in total) across coho and arm pairs with a high retention of duplicated loci detected in coho Chinook salmon. Each of the eight pairs of chromosomes likely involved salmon were also observed in Chinook salmon, and four homeologous in ongoing or recent homeologous pairing included at least one of the arm pairs were conserved in Atlantic salmon (Table 2). All of these ancestral metacentric chromosomes that are conserved between the two chromosome arms, likely involved in recent or ongoing homeologous species. The other chromosome arm involved in the pairing may be part pairing, involved at least one metacentric chromosome ancestral to the of either an acrocentric chromosome or a metacentric chromosome. The divergence between Paciﬁcsalmonspecies. data suggest that Robertsonian rearrangements that result in metacentric chromosome formation prior to the diversiﬁcation of homeologous pairs DISCUSSION might partly explain the uneven retention of duplicated regions across Here, we aimed to examine the relationship between chromosomal the genome, at least within Paciﬁcsalmon. evolution and retention of duplicated regions within the genus The consensus male map, constructed with three diploid families, Oncorhynchus, and between this genus and Salmo, by deriving a link- was signiﬁcantly smaller (4141.7 cM) than the consensus female map age map for coho salmon and comparing this map with that of (6596.7 cM) constructed with two haploid families and three diploid Chinook salmon, rainbow trout, and Atlantic salmon. Thirty linkage families. There are three main reasons that might explain the reduced groups including 20 putative metacentric and 10 putative acrocentric map size in the male compared with the female map. First, the chromosomes were described across two haploid and three diploid difference could simply be a function of more markers being placed families. Chromosomal rearrangements were identiﬁed by compar- on the female map (8681 for the female and 2043 for the male), ing homologous arms between coho salmon, Chinook salmon, rain- because map size tends to increase when more markers are added (Liu bow trout, and Atlantic salmon. Results conﬁrmed the conservation 1998). Second, some male linkage groups only represented a portion of at least one metacentric chromosome between Oncorhynchus and of those in females; for example, in three metacentric chromosomes Salmo (Co09) and seven metacentric chromosomes across the genus (Co07, Co09, Co13) only one arm and a region containing the cen- Oncorhynchus (Co01–Co07) (Naish et al. 2013; Phillips et al. 2013; tromere were mapped, the duplicated markers were not mapped in Brieuc et al. 2014), and detected a polymorphism in another across males. Third, recombination in males is suppressed relative to females, coho and Chinook salmon and rainbow trout (Co14 and Co15). and male maps in salmonids often tend to be smaller. Comparisons Another metacentric chromosome was detected as ancestral to coho between the consensus male map and the consensus (haploid and and Chinook salmon only (Co08). The placement of 1266 duplicated diploid) female map indicated that recombination in the males was loci on the consensus haploid map of 6643 markers revealed that these suppressed around the region containing the centromere in some loci were not evenly distributed across all linkage groups, supporting linkage groups, whereas recombination in females seemed suppressed aprevious ﬁnding in Chinook salmon (Brieuc et al. 2014), namely, that toward telomeric regions. 1724 | M. Kodama et al. Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 Figure 3 Number of markers and distribution of duplicated markers across each coho salmon linkage group. Nonduplicated loci are represented in light gray. Duplicated loci are represented in dark gray (loci with only one paralog polymorphic) or black (both paralogs polymorphic). Accurate identiﬁcation of chromosome structure in coho salmon has been repeatedly transposed to different chromosomes in differ- relied on aligning homologous chromosome arms with Chinook ent salmon species (Phillips et al. 2001; Woram et al. 2003; Yano salmon. In addition, regions containing the centromere were inferred et al. 2012) and can be polymorphic within a species (Eisbrenner through comparative mapping between coho and Chinook salmon as et al. 2014). no gynogenetic diploid families were used for this study to identify the Our results showed that suppressed recombination around the exact location of the centromere. Homology of Co07a and Co12b with region containing the centromere in males was widely apparent, Chinook salmon chromosome arms Ots11p and Ots34 was not whereas higher recombination was observed in telomeric regions for completely resolved. These arms are homeologous to each other some male linkage groups relative to female. The results are in within both species, and markers on Ots34 mapped to both Co07a agreement with a number of studies performed on other salmonid and Co12b in coho salmon. We inferred that Co07a was homologous species (Sakamoto et al. 2000; Moen et al. 2008; Rexroad et al. 2008; to Ots11p, as the arm Co07a is part of a metacentric chromosome that Lien et al. 2011). Male recombination rate in telomeric regions of is conserved in Chinook salmon (Ots11) and rainbow trout (Omy19) a subset of rainbow trout linkage groups has been shown to be higher (Table 1). In fact, Naish et al. (2013) speculate that these are conserved than that of females, but lower in centromeric regions (Sakamoto across the genus because Chinook salmon and rainbow trout are et al. 2000). Such different recombination patterns might be partly distantly related. In contrast, the metacentric chromosome Co12 is explained by occasional multivalent formation during male meiosis, not conserved in Chinook salmon and rainbow trout. We assumed in which crossovers between homeologous chromosomes are in- these structures in the subsequent discussion. creased in the telomeric regions while crossovers between homologous chromosomes are hindered in the centromeric regions through struc- Coho salmon map coverage, size, and differences in tural constraints (Sakamoto et al. 2000). In our study, however, sex-speciﬁc recombination suppressed recombination around the centromere and increased The coho salmon linkage map constructed in this study has 8681 recombination in telomeric regions were apparent for most male markers, spanning all predicted 30 linkage groups. This coverage is linkage groups, including the ones not likely involved in homeologous comparable with recently published maps across a number of salmon pairing. Some studies have also found notable clustering of markers in species (Lien et al. 2011; Everett et al. 2012; Miller et al. 2012; Brieuc centromeric regions for many male linkage groups (Nichols et al. et al. 2014; Gonen et al. 2014). We observed different map sizes in the 2003; Lien et al. 2011; Miller et al. 2012). In Atlantic salmon, high consensus female maps; the map constructed with combined haploid marker densities were also involved in regions close to the centromere and diploid families had a size of 6596.7 cM, which is signiﬁcantly for male linkage groups with a lower frequency of duplicated markers larger than the coho map created with haploids alone (3602.6 cM). (Lien et al. 2011). Recombination rates are known to differ between There are several reasons that might explain the differences such as the sexes in a wide range of species (Lenormand and Dutheil 2005); nonrandom missing values (Jorgenson et al. 2005), genotyping errors although homeologous chromosome pairing during male meiosis (Hackett and Broadfoot 2003), and numbers of markers mapped. could certainly account for some of the differences, the origin of the Potential bias against heterozygotes in RAD sequencing (Brieuc sex differences observed in this study still remains unclear. et al. 2014) may also partly explain the inﬂated map distances in Comparative genome mapping the haploid/diploid map, especially because the size of the map created with only haploid families in this study was much smaller. Comparative mapping provided insights into the process of chromo- Male salmonids are the heterogametic sex (Allendorf and Thorgaard somal evolution occurring after the whole genome duplication event, 1984). In this study, both the Y-linked growth hormone pseudogene and thisisthe ﬁrst study that characterizes chromosomal evolution and sex-determining gene, sdY, mapped to the telomeric region on between coho and Chinook salmon. Nine metacentric and nine the acrocentric chromosome, Co30. This ﬁnding is in agreement acrocentric chromosomes appear to be conserved between these two with previous ﬁndings (Phillips et al. 2005). Mapping has shown species. Among these conserved chromosomes, one metacentric that the sex chromosome is not conserved across the species, and (Co08 in coho and Ots12 in Chinook) and ﬁve acrocentric chro- that a small male-speciﬁc region including the sex determining gene mosomes are unique to coho and Chinook salmon, suggesting that Volume 4 September 2014 | Coho Salmon Genome Map | 1725 Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 Figure 4 Distribution of duplicated and nonduplicated loci along the 16 linkage groups with a high proportion of duplicated loci. Nonduplicated loci are represented in light gray. Duplicated loci are represented in dark gray (loci with one paralog polymorphic) or in black (loci with both paralogs polymorphic). The putative region containing the centromere is represented by the cross-hatched area. the structure of these linkage groups is ancestral to the divergence of served among all three species (Co01–Co07, Co09). The results these species relative to rainbow trout and Atlantic salmon. The support the hypothesis of Naish et al. (2013) that the arm rearrange- remaining linkage groups are not conserved, reﬂecting extensive ments that resulted in these metacentric chromosomes are ancestral to chromosomal rearrangements since coho and Chinook salmon the divergence of the species and could be conserved across the genus diverged. Oncorhynchus. There is one interesting extension to these earlier Syntenic relationships between the Chinook salmon and rainbow observations. One metacentric chromosome in Chinook salmon, trout maps permitted comparisons across the genus Oncorhynchus Ots08, sometimes occurs as a metacentric chromosome (Omy25p (Naish et al. 2013; Phillips et al. 2013). There are four acrocentric and q) or as two acrocentric arms (Omy25 and Omy 29) in rainbow chromosomes that are conserved across all three Oncorhynchus spe- trout (Figure 5). Here, we found that the homologous arms in coho cies (Co26–Co29). Similarly, eight metacentric chromosomes are con- salmon occur in two separate unrelated metacentric linkage groups 1726 | M. Kodama et al. Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 n Table 2 Homeologous chromosome arm pairs identiﬁed in coho salmon and the number of marker pairs supporting the homeologous relationship Number of Marker Homeology in Homeology in Homeology in Homeology in Known Phylogenetic Placement Pairs Supporting Chinook Salmon Rainbow Trout Atlantic Salmon Coho Salmon of Metacentric Arrangement Homeolog Pairings (Brieuc et al. 2014) (Phillips et al. 2006) (Lien et al. 2011) ‡ † Co01b–Co20b 15 Ots02q–Ots32 Omy17q –Omy13p Ssa02q–Ssa12qa B Co02a–Co13b 11 Ots03p–Ots23 Omy03p–Omy02p Ssa02p–Ssa05q B Co03b–Co08b 15 Ots04q–Ots12q Omy06q–Omy26 Ssa26–Ssa11qa B, C Co04b–Co11a 17 Ots06q–Ots01q Omy01q–Omy23 Ssa18qa–Ssa01qa B Co05a–Co16b 10 Ots07p–Ots14p Omy07p–Omy18p Ssa17qa–Ssa16qb B Co06b–Co10b 7 Ots09q–Ots27 Omy12q–Omy13q Ssa03q–Ssa06p B Co07a–Co12b 9 Ots11p–Ots34 Omy19p–Omy10q Ssa04p–Ssa08q B Co09a–Co19a 16 Ots15p–Ots17 Omy21p–Omy15q Ssa07p–Ssa17qa A Corresponding known homeologous relationships in Chinook salmon, rainbow trout, and Atlantic salmon are shown. The ﬁnal column designates known conservation of metacentric chromosome with high frequency of duplicated markers. Letter corresponds to phylogenetic placement in Figure 5. Possible earlier chromosomal arrangement (A) and subsequent rearrangement. Homeologous relationships with little or no support in Atlantic salmon (Lien et al. 2011). We have corrected the homeologous relationship between Omy17q and Omy13p; evidence suggests that this relationship was incorrectly reported as being between Omy17p and Omy13p in previous studies. (Co14a and Co15a) (Figure 5). In Atlantic salmon, these two arms are previous results provided evidence for the occurrence of centromet- fused together along with a third arm to form a large acrocentric ric inversion in Omy20 in rainbow trout following divergence be- chromosome (Figure 5). Robertsonian fusions are common and can tween rainbow trout and Chinook/coho salmon, and this also form acrocentric chromosomes; this outcome is likely more fre- chromosomal inversion may be exclusive to rainbow trout (Naish quent in Atlantic salmon than in Paciﬁc salmon (Phillips and Ráb et al. 2013; Ostberg et al. 2013; Brieuc et al. 2014). In the current 2001). Taken together, the conﬁgurations of these particular chromo- study, marker orders are fully conserved between coho and Chinook somes suggest they may have undergone recurrent fusions and ﬁssions salmon chromosome arms, Co25 and Ots25, respectively, further across species. supporting this previous observation (File S5). One metacentric and one acrocentric chromosome, Co09 and Co26, respectively, appear to be conserved across coho salmon, Conservation of reduced divergence between Chinook salmon, rainbow trout, and Atlantic salmon (Phillips et al. homeologous chromosomes across species 2009; Brieuc et al. 2014). Our study supports the previous ﬁndings Although our results conﬁrm that the divergence rates of homeologs that this metacentric chromosome is likely ancestral to the diver- following the whole genome duplication event have not been uniform gence of the two genera, Salmo and Oncorhynchus. It also appears (Brieuc et al. 2014), the key ﬁnding of this study is that the ancestral that this chromosome is conserved in Arctic charr and Brook charr metacentric chromosomes retain recently diverged duplicates and are within the genus Salvelinus (Timusk et al. 2011), both of which share the ones likely involved in recent or ongoing homeologous pairing a more recent common ancestor with Oncorhynchus. In addition, (Co01–Co07, conserved among all three Oncorhynchus species; Co09, Figure 5 Phylogenetic tree showing the orientation of homologous arms Ssa09qab, Omy25/29, Co14a, Co15a, and Ots08 in Atlantic salmon, rainbow trout, coho salmon, and Chinook salmon, respectively. Chromosomal rearrangements and homeologous relationships con- served across species at phylogenetic nodes A, B, C are summarized in Table 1 and Table 2. Volume 4 September 2014 | Coho Salmon Genome Map | 1727 Downloaded from https://academic.oup.com/g3journal/article/4/9/1717/6025941 by DeepDyve user on 18 November 2022 conserved among all four species). Such ﬁndings suggest that these ancestral metacentric chromosomes following the whole geno- homeologies may be preferentially retained between larger meta- me duplication event. The resources developed here will facilitate centric chromosomes (Phillips et al. 2009), and the involvement genome-wide studies in coho salmon, such as genome scans, QTL of at least one metacentric chromosome provides the stability mapping, and genome-wide association studies (Naish and Hard required for the formation of multivalents (Wright et al. 1980, 2008), as well as provide resources for studies concerning ecology 1983; Brieuc et al. 2014). These results support the hypothesis of and evolution in related salmon species. Phillips et al. (2009), which suggested that diploidization of chro- mosomes not involved in homeologous parings may have occurred ACKNOWLEDGMENTS in the ancestral salmonid before thedivergencebetween Salmo and We thank Isadora Jimenez-Hidalgo for assistance with genomic Oncorhynchus. We speculate that this process also differed to some data processing. Dan Drinan provided thoughtful discussions and extent following the divergence of the two genera. Although the helpful suggestions. We also thank Linda Park and Jim Myers for exact distribution of duplicated markers along chromosome arms help in setting up the initial crosses and David Rose for main- in Atlantic salmon has not yet been described (Lien et al. 2011), taining the lines. Finally, we are grateful to two anonymous only four out of eight homeologous pairings appear to share poly- referees and the Associate Editor for their very helpful comments morphic duplicated loci between the Atlantic salmon and Chinook regarding the ﬁrst draft of the manuscript. Initial experimental and coho salmon grouping (Table 2). lines were obtained from SweetSpring Salmon/Aquaseed Corpo- The implications of our ﬁndings for species divergence within the ration, suppliers of the Domsea broodstock and we thank Per subfamily Salmoninae will become clearer once we gain a greater Heggelund, Greg Hudson and Patty Munsell for providing these understanding of the role of duplicated regions in evolution. If lines. Funding for this study was provided by NOAA Fisheries/ the duplicated regions we detected have genes that permit greater Federal Columbia River Power System (FCRPS) Biological Opinion ﬂexibility for adaptation by providing the opportunity to acquire Remand Funds (to K.A.N. and J.J.H.), School of Aquatic and additional or novel functions (Soltis and Soltis 2000; Koop and Fishery Sciences, and Graduate Opportunities and Minority Davidson 2008; Van De Peer et al. 2009; Feldman et al. 2012; Alexandrou Achievement Program (GO-MAP, University of Washington) et al. 2013; Macqueen and Johnston 2014), then retention of particular award (to M.K.). The authors declare that they have no competing duplicated regions within certain lineages may explain their subse- interests. quent innovation and diversiﬁcation. 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Comparative Mapping Between Coho Salmon (Oncorhynchus kisutch) and Three Other Salmonids Suggests a Role for Chromosomal Rearrangements in the Retention of Duplicated Regions Following a Whole Genome Duplication Event

Comparative Mapping Between Coho Salmon (Oncorhynchus kisutch) and Three Other Salmonids Suggests a Role for Chromosomal Rearrangements in the Retention of Duplicated Regions Following a Whole Genome Duplication Event

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Comparative Mapping Between Coho Salmon (Oncorhynchus kisutch) and Three Other Salmonids Suggests a Role for Chromosomal Rearrangements in the Retention of Duplicated Regions Following a Whole Genome Duplication Event

Comparative Mapping Between Coho Salmon (Oncorhynchus kisutch) and Three Other Salmonids Suggests a Role for Chromosomal Rearrangements in the Retention of Duplicated Regions Following a Whole Genome Duplication Event

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