TY - JOUR
AU1 - Fleischer, Robert, C.
AU2 - Slikas,, Beth
AU3 - Beadell,, Jon
AU4 - Atkins,, Colm
AU5 - McINTOSH, Carl, E.
AU6 - Conant,, Sheila
AB - Abstract The Millerbird (Acrocephalus familiaris) is an endemic Northwestern Hawaiian Islands reed warbler that existed until about 1923 on Laysan Island (A. f. familiaris) and currently occurs in a small population on Nihoa Island (A. f. kingi). The two populations are described as separate subspecies or species on the basis of size and plumage differences. We assessed genetic variation in blood samples from 15 individuals in the modern Nihoa population using approximately 3000 base pairs (bp) of mitochondrial DNA (mtDNA) sequence and 14 microsatellite loci. We also obtained up to 1028 bp of mtDNA sequence from the fragmented DNA of museum specimens of three birds collected on Nihoa in 1923 and five birds collected on Laysan in 1902 and 1911 (ancient samples). Genetic variation in both marker types was extremely low in the modern Nihoa population (nucleotide diversity [π]  =  0.00005 for mtDNA sequences; observed heterozygosity was 7.2% for the microsatellite loci). In contrast, we found three mtDNA haplotypes among the five Laysan individuals (π  =  0.0023), indicating substantially greater genetic variation. The Nihoa and Laysan taxa differed by 1.7% uncorrected mtDNA sequence divergence, a magnitude that would support designation at the subspecies, and perhaps species, level relative to other closely related Acrocephalus species pairs. However, in light of strong ecological similarity between the two taxa, and a need to have additional populations to prevent extinction from stochastic effects and catastrophes, we believe these genetic differences should not deter a potential translocation of individuals from Nihoa to Laysan. Resumen Acrocephalus familiaris es una especie endémica de las islas del noroeste de Hawai que existió hasta alrededor de 1923 en la Isla de Laysan (A. f. familiaris) y que existe actualmente como una pequeña población en la Isla de Nihoa (A. f. kingi). Las dos poblaciones fueron descritas como dos subespecies o especies distintas con base en diferencias de tamaño y plumaje. Evaluamos la variación genética en muestras de sangre de 15 individuos de la población moderna de Nihoa utilizando alrededor de 3000 pares de bases (pb) de ADN mitocondrial y 14 loci de microsatelites. Obtuvimos también hasta 1028 pb de secuencia de ADNmt de ADN fragmentado de especímenes de museo de tres individuos colectados en Nihoa en 1923 y cinco individuos colectados en Laysan en 1902 y 1911 (muestras antiguas). La variación genética en ambos tipos de marcadores fue extremadamente baja en la población moderna de Nihoa (diversidad nucleotídica [π]  =  0.00005 para secuencias de ADNmt; la heterocigocidad observada fue de 7.2% para los loci de microsatelites). De modo contrastante, encontramos tres haplotipos de ADNmt en cinco individuos de Laysan (π  =  0.0023), indicando una variación genética substancialmente mayor. Los taxones de Nihoa y de Laysan difieren en 1.7% de divergencia sin corrección de secuencia de ADNmt, una magnitud que apoyaría la designación a nivel de subespecie, y quizás a nivel de especie, con relación a otros pares de especies estrechamente relacionados en el genero Acrocephalus. Sin embargo, en vista de la fuerte similitud ecológica que existe entre los dos taxones, y de la necesidad de que existan poblaciones adicionales para prevenir la extinción debido a efectos estocásticos y catástrofes, creemos que estas diferencias genéticas no deben disuadir una posible translocación de individuos de Nihoa a Laysan. The Millerbirds (Acrocephalus familiaris) of the Northwestern Hawaiian Islands (Fig. 1) include one subspecies from Laysan Island (A. f. familiaris) and another from Nihoa Island (A. f. kingi). The taxonomic status of the Millerbirds is unclear, with some authors favoring designation at the level of separate species (Wetmore 1924, Olson 1996). The nominate subspecies of Millerbird on Laysan went extinct before 1923 due to devegetation of the island by introduced rabbits. Also endemic to Laysan were two other landbirds, the Laysan Honeycreeper (Himatione sanguinea freethii) and the Laysan Rail (Porzana palmeri), three plant species (Christophersen and Caum 1931), and a dozen or more arthropod species (Butler and Usinger 1963). The Nihoa Millerbird, which was discovered in 1923 (Wetmore 1924), is listed as endangered (U.S. Fish and Wildlife Service 1984). Its population size ranges between 31 and 731 birds, with an average of 381 individuals over the past 30 years (Morin et al. 1997). Nihoa Island, less than 175 acres, is the entire remaining range for the Millerbird, and proposals have been made (Morin et al. 1997, Conant and Morin 2001) to increase the species' effective population size and decrease its probability of extinction by translocating individuals from Nihoa to Laysan or other islands. In this light, analyses of genetic variability of the Nihoa Millerbird and a genetically based taxonomic evaluation of the two subspecies would be valuable. The levels of genetic variability would reflect the historical effective population sizes of each population, while a comparative analysis would determine how genetically similar birds on Laysan were to the taxon on Nihoa. Figure 1 Open in new tabDownload slide Map of the South Pacific showing the five islands—Laysan, Nihoa, Pitcairn, Henderson, and Kiritimati—and two archipelagoes—Marquesas and Cook Islands—on which the Acrocephalus taxa included in analyses occur. Locations of occurrence are highlighted with boldface type and asterisks. See Table 1 for list of specimens collected from each locality. Figure 1 Open in new tabDownload slide Map of the South Pacific showing the five islands—Laysan, Nihoa, Pitcairn, Henderson, and Kiritimati—and two archipelagoes—Marquesas and Cook Islands—on which the Acrocephalus taxa included in analyses occur. Locations of occurrence are highlighted with boldface type and asterisks. See Table 1 for list of specimens collected from each locality. Table 1 Acrocephalus samples used for genetic analysis. Open in new tab Table 1 Acrocephalus samples used for genetic analysis. Open in new tab High genetic similarity between the populations would help to justify translocating Nihoa birds to Laysan Island, a measure that could be of immense importance to the survival of the species (Conant and Morin 2001). However, genetic similarity may not be required if the taxa are considered ecological replacements, and this criterion is considered valuable by conservation managers. Both taxa have been described as generalist insectivores, gleaning insects (both native and introduced species) from virtually any portion of their shrub and grassland habitats (Ely and Clapp 1973, Morin et al. 1997). Both islands have diverse and abundant arthropod fauna. The Nihoa Millerbird takes its food opportunistically, and there is no reason to suspect it is different from the Laysan Millerbird in this respect. We know that Nihoa Millerbirds nest in shrubs (Morin et al. 1997), of which there are several species currently on Laysan, and that Laysan Millerbirds mostly nested in clumps of the bunchgrass (Eragrostis variabilis), which occurs on both islands (Lamoureux 1963, Conant 1985). Laysan's plant communities have recovered almost completely from the devastation caused by introduced rabbits in the early part of the 20th century (Lamoureux 1963, Ely and Clapp 1973, Morin et al. 1997, Morin and Conant 2007). The size of Laysan, and the availability of habitat, arthropod food, and nesting sites that are similar to those on Nihoa suggest that Laysan is a suitable site to which the Nihoa Millerbird could be translocated (Morin and Conant 2007). Introduction of the Nihoa Millerbird to Laysan would restore an insectivorous passerine to that ecosystem; however, managers feel the most important reason to consider this translocation is to assure the continued survival of the Nihoa Millerbird by creating a second population of this bird as a buffer against extinction. A single hurricane or fire, or the accidental introduction of rats, could drive the species to extinction in an extremely short period of time. Methods Samples Blood samples from 15 Nihoa Millerbirds were collected by SC in July of 1992 (Table 1). Toe pad samples from three Nihoa Millerbird (collected in 1923) and six Laysan Millerbird specimens (collected in 1902 and 1911; Table 1) were obtained from the U.S. National Museum. We used five related Pacific Acrocephalus taxa for comparison of genetic divergence levels and as outgroups to root phylogenetic trees: Pitcairn Island Reed-Warbler (A. vaughani), Henderson Island Reed-Warbler (A. taiti), Bokikokiko, found on Kiritimati (A. aequinoctialis), Tuamotu Reed-Warbler (A. atyphus), and Cook Islands Reed-Warbler (A. kerearako). Dna Protocols and Primers “Modern” DNA was isolated from the 15 blood samples of Nihoa Millerbird using Qiagen (Chatsworth, California) DNeasy kits following the manufacturer's recommended protocol. “Ancient” DNA was isolated from toe pads of museum specimens using a phenol-chloroform, centrifugal dialysis method detailed by Slikas et al. (2000). We amplified mitochondrial DNA (mtDNA) sequences from the genomic DNA samples using standard polymerase chain reaction (PCR) methods (Slikas et al. 2000). Regions of four different mtDNA genes were amplified: control region; ATP synthase, subunits 6 and 8 (ATP6/8); cytochrome b (cytb); and NADH dehydrogenase, subunit 2 (ND2), using primers in Table 2. Primer pairs that amplify smaller fragments were used to amplify sequences from the ancient DNA isolated from museum specimens (Table 2). We were unable to obtain sequences of all possible gene regions from these samples and were generally limited to products of small size because of the degraded and damaged nature of DNA from older specimens. Amplified products were cleaned of unincorporated nucleotides and primers using Qiagen QIAquick columns and sequenced in both directions on either an ABI 377 automated DNA sequencer (Applied Biosystems, Foster City, California) or an ABI 3100 automated DNA capillary sequencer. Sequences were edited for computer miscalled bases and aligned using Sequencher version 4.1 (Gene Codes Corporation, Ann Arbor, Michigan). Table 2 Mitochondrial DNA (mtDNA) PCR primers used to assess sequence divergence in Acrocephalus species, separated by their use for modern and ancient samples, when these differed. Open in new tab Table 2 Mitochondrial DNA (mtDNA) PCR primers used to assess sequence divergence in Acrocephalus species, separated by their use for modern and ancient samples, when these differed. Open in new tab We amplified 14 microsatellite loci for the 15 modern Nihoa samples. These loci are polymorphic in other species of Acrocephalus (Richardson et al. 2000; Table 3). Amplifications were carried out in 10 µl volumes following the methods of Richardson et al. (2000), with some exceptions regarding annealing temperature and MgCl2 concentration (Table 3). Amplifications were also attempted from the nine ancient DNA samples, but very few amplified. Thus, we restrict our microsatellite analyses in this paper to the modern samples. Table 3 Microsatellite loci used to assess variation in Nihoa Millerbirds (Acrocephalus familiaris kingi). Variability (k is number of alleles, Ho is observed heterozygosity) in the Seychelles Warbler (A. sechellensis; Richardson et al. 2000) and Nihoa Millerbird (this study), and PCR conditions (annealing temperature and MgCl2 concentration) are included. Dash indicates that no value was available. Open in new tab Table 3 Microsatellite loci used to assess variation in Nihoa Millerbirds (Acrocephalus familiaris kingi). Variability (k is number of alleles, Ho is observed heterozygosity) in the Seychelles Warbler (A. sechellensis; Richardson et al. 2000) and Nihoa Millerbird (this study), and PCR conditions (annealing temperature and MgCl2 concentration) are included. Dash indicates that no value was available. Open in new tab Phylogenetic and Statistical Analyses Aligned sequences were compared for divergence levels and subjected to phylogenetic analyses with other Acrocephalus outgroups. We constructed a phylogeny using sequences from the two Millerbird taxa along with five other Pacific Island Acrocephalus species used as outgroups, also to compare the relative divergence levels within two pairs of sister species (Henderson Island Reed-Warbler and Pitcairn Island Reed-Warbler, and Cook Islands Reed-Warbler and Tuamotu Reed-Warbler). We selected these two pairs of sister species for this comparison because they have the lowest mtDNA sequence divergence between Pacific Acrocephalus taxa that are currently designated as full species (RCF, unpubl. data), and thus make a conservative comparison. The program Modeltest (Posada and Crandall 1998) with Akaike's information criterion (AIC) was used to determine an appropriate model of DNA sequence evolution. We conducted exhaustive searches in PAUP* (Swofford 2001) under both maximum parsimony and maximum likelihood criteria to select trees, and used bootstrapping (1000 repetitions) to determine support for nodes. Both uncorrected and maximum likelihood–corrected genetic distance matrices were also calculated in PAUP*. For microsatellites, we calculated expected and observed heterozygosity and allele frequencies, and tested for Hardy-Weinberg equilibrium and linkage disequilibrium using the programs Genepop on the Web (Raymond and Rousset 1995) and Arlequin (Schneider et al. 2000). Results Genetic Variation Long mtDNA sequences, totaling up to 3090 base pairs (bp; average of 2624 bp per individual), of four gene regions were obtained from the 15 Nihoa Millerbird blood samples (i.e., from modern A. f. kingi): ATP6/8 (769 bp; Genbank accession number EU119959); control region (960 bp; EU119967); ND2 (808 bp; EU119962); and Cytb (860 bp; EU119965). Only a single base substitution was detected among the 15 Nihoa individuals (a T-C transition in the 5′ end of the control region of Nihoa Millerbird, band number 1600–19324), indicating extremely low mtDNA sequence variation in the modern population on Nihoa (nucleotide diversity [π]  =  0.00005). It is unlikely that each of these four independently amplified gene regions was the result of a nuclear transposition of mtDNA (Sorenson and Fleischer 1996). In addition to the sequences from blood samples, we were able to amplify and sequence shorter mtDNA segments from the fragmented and damaged DNA isolated from museum specimens. We obtained a combined total of 327–344 bp of protein coding sequence (ATP6/8 and ND2) from the three Nihoa Millerbird specimens collected in 1923. These were identical in sequence to corresponding gene regions obtained from the blood samples, suggesting that mtDNA sequence variation was not appreciably higher in 1923 than it is now. We obtained between 353 and 1028 bp of mtDNA sequence from five Laysan Millerbird museum specimens, including four collected in 1902 and one collected in 1911. These ancient sequences included segments from ATP6/8 (196–318 bp; EU119960 and EU119961), ND2 (70–158 bp; EU119963 and EU119964), and the control region (318–561 bp; EU119966). For specimen USNM 301124, we obtained 1028 bp of sequence (317 of ATP6/8, 149 of ND2, and 561 of control region), and this sequence was used for comparison to modern Nihoa sequences (see below). From the combined protein coding sequences for the five individuals (255–354 bp) we identified two variable sites (both transitional changes) and three different haplotypes, and calculated π  =  0.0023 (95% CI  =  0.0009–0.0037). The same sequence region was invariant for the 18 Nihoa Millerbird samples. Microsatellite variation was very low in the 15 modern Nihoa Millerbird samples, with only four of the 14 loci variable (Ase11, Ase48, Ase57, and Ase44). The first three loci had only two alleles, while the fourth (Ase44) had three, and the mean number of alleles per locus across the 14 loci was 1.4 ± 0.6 SD. Observed heterozygosity averaged 7.1%, expected heterozygosity was 8.4%, and there were no significant deviations from Hardy-Weinberg expectations for the four heterozygous loci either by locus (P  =  0.10, 1.00, 0.23, and 1.00) or overall (P  =  0.27). There was no evidence of linkage disequilibrium among the four variable loci (all P > 0.10). Comparison of the Taxa The transitional model of sequence evolution (TIM, Posada and Crandall 1998) was selected as the best model, with the proportion of invariant sites I  =  0.78. Uncorrected mtDNA sequence divergence between the Laysan and Nihoa Millerbirds was 1.7% for the 1028 bp of overlapping sequence, while maximum likelihood corrected divergence was 1.9%. Our larger mtDNA sequence dataset includes nearly all Acrocephalus taxa (RCF, unpubl. data), and in all trees, the millerbirds were relatively close sister taxa and were isolated in a long-branched clade from all other Acrocephalus species. Maximum parsimony and maximum likelihood trees were identical (Fig. 2). The uncorrected (Duncorr) and model-corrected (Dcorr) sequence divergences between the two other sister pairs of Pacific Acrocephalus species (Henderson Island Reed Warbler and Pitcairn Island Reed Warbler: Duncorr  =  1.9%, Dcorr  =  2.1%; Cook Islands Reed Warbler and Tuamotu Reed Warbler: Duncorr  =  1.5%, Dcorr  =  1.6%) were very similar to those calculated between Nihoa and Laysan Millerbirds. Figure 2 Open in new tabDownload slide Phylogram of Laysan (Acrocephalus familiaris familiaris) and Nihoa Millerbirds (A. f. kingi) and five additional Acrocephalus species (Table 1), based on up to 1028 base pairs (bp) of mitochondrial DNA (mtDNA) sequence. A single tree was obtained from an exhaustive search under a maximum likelihood criterion. Proportions of trees containing a node from a bootstrap (1000 repetitions) are shown at appropriate nodes. Maximum parsimony reconstruction produced an identical topology. The Nihoa Millerbird in the tree represents 17 individuals with identical sequences; one other bird differed by one base but was not included in the analysis. Only the single Laysan Millerbird (specimen number USNM301124) with 1028 bp of mtDNA sequence was included. Figure 2 Open in new tabDownload slide Phylogram of Laysan (Acrocephalus familiaris familiaris) and Nihoa Millerbirds (A. f. kingi) and five additional Acrocephalus species (Table 1), based on up to 1028 base pairs (bp) of mitochondrial DNA (mtDNA) sequence. A single tree was obtained from an exhaustive search under a maximum likelihood criterion. Proportions of trees containing a node from a bootstrap (1000 repetitions) are shown at appropriate nodes. Maximum parsimony reconstruction produced an identical topology. The Nihoa Millerbird in the tree represents 17 individuals with identical sequences; one other bird differed by one base but was not included in the analysis. Only the single Laysan Millerbird (specimen number USNM301124) with 1028 bp of mtDNA sequence was included. Discussion Genetic Variability Genetic variation in Nihoa Millerbirds is extremely low. We found only a single haplotype among 17 of 18 birds (including three old museum specimens) sequenced for up to 3090 bp of mtDNA sequence, and only one variable site that was found to differ in only a single individual. Most other species of Hawaiian songbirds thus far assessed (Tarr and Fleischer 1993, Jarvi et al. 2004, Reding 2007; but see data for ‘I‘iwi [Vestiaria coccinea] in Jarvi et al. 2004, Foster et al. 2007) have considerably higher levels of mtDNA variation. In addition, in the modern sample of 15 Nihoa Millerbirds, most microsatellite loci (10 of 14) were fixed for a single allele. In contrast, only five of 13 of these same loci were fixed in populations of the Seychelles Warbler (Acrocephalus sechellensis), and only four of the 14 were fixed in the Bokikokiko, a related taxon that occurs only on Christmas Island (JB, unpubl. data). Average observed microsatellite heterozygosity is also very low relative to other species of songbirds (e.g., 7.1% versus 69% ± 16% SE, range: 37%–91%; Neff and Gross 2001), including island-inhabiting songbirds (Tarr et al. 1998, Richardson et al. 2000, Markert et al. 2004). The low genetic variation in this endemic island taxon makes sense given the recent history of its population on Nihoa. When discovered on Nihoa in 1923, the total population was estimated at approximately 100 birds. Censuses taken in the past 30 years have yielded an average population estimate of 381 with a range from 31 to as high as 731 (Morin et al. 1997). If we assume an effective population size (Ne) of 10%–50% of the census size (Nunney and Elam 1994, Frankham 1995), then we can roughly estimate a range of Ne from 38 to 190 individuals. In 50 generations (perhaps 100–150 years) at these population sizes, the Nihoa Millerbird would lose from 26% (Ne  =  190) to 76% (Ne  =  38) of its starting genetic variation. It is unknown what the historical population size of the Nihoa Millerbird was but, given the small size of Nihoa, no evidence for existence of the taxon on other islands (James and Olson 1991), and significant divergence from the Laysan taxon (our data), it probably has not been much larger than current populations. The Laysan Millerbird appears to have had greater mtDNA variability than the Nihoa Millerbird. This may reflect the higher population size estimates for the historical Laysan population (∼1500 birds; Morin et al. 1997) compared to the one on Nihoa. Certainly, this low heterozygosity supports the expectation of Conant and Morin (2001) that the population on Nihoa has been inbred for a long period of time. However, there is no evidence for current inbreeding depression in Nihoa Millerbirds (Conant and Morin 2001), perhaps because it was ameliorated by past purging of deleterious recessive alleles and adaptation to inbreeding (but see Leberg and Firmin [2007] for discussion of this issue). Laysan Finches (Telespiza cantans) have low genetic variation, and their introduction to Pearl and Hermes Reef reduced their genetic diversity even further (Tarr et al. 1998), but this species has also survived its “double-bottleneck” with no evidence of inbreeding effects. Taxonomy Avian taxonomists have considered the Laysan and Nihoa Millerbirds as sister species (Wetmore 1924, Olson 1996, Munro 1960) or subspecies (Vanderbilt and Meyer de Schauensee 1941, AOU 1983). The former authors felt that morphological differences in size and coloration and existence on widely separated islands justified species level classification. Our results support the contention of these authors that the two are closely related sister taxa. However, the level of divergence between them appears to be sufficiently high (1.7%) to support their designation as different subspecies, and possibly even different species. This is especially true because their mtDNA sequence divergence level is comparable to that found between other closely related Acrocephalus species pairs. Based on molecular clock estimates for protein coding loci in songbirds (Fleischer et al. 1998, Warren et al. 2003, Arbogast et al. 2006), the divergences we found for the ND2 and ATP6/8 genes (1.8% and 1.1%, respectively) correspond very roughly from one hundred thousand to several hundred thousand years of isolation between the forms, at least for their maternally inherited mtDNA. The Hawaiian Millerbird taxon itself is also a unique lineage within the Pacific Acrocephalus, at least 3% divergent in mtDNA sequence from any other extant Acrocephalus species (RCF et al., unpubl. data). Conservation Recommendations Serious consideration of establishing additional populations of Nihoa Millerbirds via translocation began in early 2006. In the past, the desirability of introducing this taxon to Laysan Island was questioned (Conant 1988). However, we feel that the extreme vulnerability caused by the entire species currently existing on a single small island (Conant and Morin 2001), its phylogenetic uniqueness relative to other Acrocephalus species, and the ecological similarities between the Nihoa and Laysan taxa (Morin et al. 1997) and the two islands provide sufficient justification to carry out this important translocation, regardless of the minor genetic divergence we found between the forms. In addition, VORTEX modeling of the populations with a translocation to Laysan resulted in an extinction probability of zero, while without translocation, under all scenarios, Nihoa Millerbirds went extinct (Conant and Morin 2001). Thus, we support plans to conduct experimental translocations of Nihoa Millerbirds to Laysan, ideally with preliminary assessment of ecological impacts and recruitment likelihood prior to full implementation. 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TI - Genetic Variability and Taxonomic Status of the Nihoa and Laysan MillerbirdsVariabilidad Genética Y Estatus Taxonómico De Acrocephalus FamiliaresShort Communications
JF - Condor: Ornithological Applications
DO - 10.1093/condor/109.4.954
DA - 2007-11-01
UR - https://www.deepdyve.com/lp/oxford-university-press/genetic-variability-and-taxonomic-status-of-the-nihoa-and-laysan-f2sMAgFcdt
SP - 954
VL - 109
IS - 4
DP - DeepDyve
ER -