Transposable Elements Activity is Positively Related to Rate of Speciation in Mammals

Transposable Elements Activity is Positively Related to Rate of Speciation in Mammals Transposable elements (TEs) play an essential role in shaping eukaryotic genomes and generating variability. Speciation and TE activity bursts could be strongly related in mammals, in which simple gradualistic models of differentiation do not account for the currently observed species variability. In order to test this hypothesis, we designed two parameters: the Density of insertion (DI) and the Relative rate of speciation (RRS). DI is the ratio between the number of TE insertions in a genome and its size, whereas the RRS is a conditional parameter designed to identify potential speciation bursts. Thus, by analyzing TE insertions in mammals, we defined the genomes as “hot” (high DI) and “cold” (low DI). Then, comparing TE activity among 29 taxonomical families of the whole Mammalia class, 16 intra-order pairs of mammalian species, and four superorders of Eutheria, we showed that taxa with high rates of speciation are associated with “hot” genomes, whereas taxa with low ones are associated with “cold” genomes. These results suggest a remarkable correlation between TE activity and speciation, also being consistent with patterns describing variable rates of differentiation and accounting for the different time frames of the speciation bursts. Keywords Speciation · Rate of speciation · Transposable elements · Cold genome · Relative rate of speciation · Mammals evolution Introduction but they also have been a great source of genomic innova- tions (Richardson et al. 2015). For example, TEs play an Transposable elements (TEs) are DNA sequences that are important role in telomere maintenance (Farkash and Prak able to move and replicate throughout the genome. They 2006), rewiring of transcriptional networks (Kunarso et al. can be highly deleterious when inserted in genetic regions 2010), regulation of gene expression (Chuong et al. 2016), ectopic recombination, and chromosomal rearrangements (Fedoroff 2012). Furthermore, TEs have been key contribu- Electronic supplementary material The online version of this tors to evolution (Biemont 2010; Oliver et al. 2013; Kapusta article (https ://doi.org/10.1007/s0023 9-018-9847-7) contains et  al. 2017) and led the insurgences of the V(D)J system supplementary material, which is available to authorized users. of acquired immunity (Kapitonov and Jurka 2005; Koonin Ricci Marco, Peona Valentina as well as Taccioli Cristian, Boattini and Krupovic 2014) and mammalian placenta (Lynch et al. Alessio have contributed equally to this study. 2011). Given their huge impact on shaping genomes, TEs are also thought to influence differentiation (Huff et al. 2016) * Ricci Marco and speciation as proposed by the Epi-Transposon (Zeh et al. marco.ricci19@unibo.it 2009), CArrier SubPopulation (Jurka et al. 2011), and TE- * Guichard Etienne Thrust (Oliver and Greene 2012) hypotheses. etienne.guichard2@unibo.it Phyletic gradualism (PG) (Charlesworth et al. 1982) and Department of Biological, Geological and Environmental punctuated equilibria (PE) (Eldredge and Gould 1972) are Sciences, University of Bologna, Bologna, Italy the most important evolutionary theories for explaining spe- Department of Ecology and Genetics, University of Uppsala, ciation dynamics. According to PG, species continuously Uppsala, Sweden accumulate mutations that would eventually lead to differ - Department of Animal Medicine, Health and Production, entiation and speciation (McPeek and Brown 2007). Instead, University of Padova, Padova, Italy Vol.:(0123456789) 1 3 Journal of Molecular Evolution the PE theory suggests that rapid bursts of differentiation This specific case led to the hypothesis that Mammals with and speciation are alternated to “static” phases in which higher rates of speciation should show higher TE activity organisms do not significantly change (Eldredge and Gould (“hot” genomes). Conversely, taxa with low rates of specia- 1972). Authors as Mattila and Bokma (2008) suggest that tion should exhibit a lower TE activity (“cold” genomes; the PE theory should be taken into account for a more com- Fig. 1b, c). plete and accurate explanation of mammalian evolutionary In this study, we assess and test the association between dynamics. If TEs widely influenced speciation, as suggested speciation and TE activity in mammals, by taking into by the previously reported hypotheses, it should be possible account both extant and extinct species. In fact, mammals to find an association between the profiles of TE activity have particularly detailed TEs annotation (Jurka et al. 2011) within genomes and patterns of speciation of organisms. as well as a reliable phylogeny (Meredith et al. 2011) and For instance, the well-characterized mammalian phylogeny abundant fossil records (Paleobiology Database 2018). (Meredith et al. 2011) shows that the order Monotremata is the most ancient and the poorest in living species (Fig. 1a). Accordingly, the platypus genome, belonging to this taxon, should harbor the lowest number of recently mobilized TEs, which was actually demonstrated by Jurka et  al. (2011). Fig. 1 a Tree of mammals. Species abundance and phylogenetic rela- Exemplified use of the relative rate of speciation (RRS) within the tionships of the main mammalian clades. Putatively “hot” superorders order Primates. I Galagidae, when compared to Cercopithecidae, of Eutheria (RRS(+)) are shown in red; putatively“cold” superorders are older and poorer in species, thus Galagidae: RRS(−), Cerco- (RRS(−)) are shown in blue. Animal icons made by Freepik from pithecidae: RRS(+). II Galagidae, when compared to Tarsiidae, are http://www.flati con.com b Modelization of the Cold Genome hypoth- younger and richer in species, thus Galagidae: RRS(+) and Tarsii- esis. “Hot” genomes contain a fraction of active, recently mobilized dae: RRS(−). III Cercopithecidae when compared to Tarsiidae, are TEs (diverging less than 1% from their consensus sequence). “Inter- younger and richer in species, thus Cercopithecidae: RRS(+) and mediate” genomes contain a fraction of less recently mobilized TEs Tarsiidae: RRS(−). (Color code: RRS(+): red; RRS(−): blue). (Color (diverging less than 5% from their consensus sequence). “Cold” figure online) genomes show ancient insertions with very low or absent activity. c 1 3 Journal of Molecular Evolution correlation and linear regression models (Table S5A-S6A). Testing Phyletic Gradualism for Speciation and Extinction Notably, all the parameters showed significant correlation with RS in the whole Mammalia class. In particular, lin- In order to establish if the speciation rates varied or remained ear models (Table S6A) showed positive regression coef- ficients and significant P values for all parameters except constant among the mammalian families, we have tested the prevalence of phyletic gradualism as a model of speciation. 5%DI. When extinct species are included in the RS calcula- tion (Fig. S3), we obtained similar results. In fact, all the The main assumption of the PG theory is that genomes accu- mulate mutations and clades accumulate species constantly parameters show a significantly positive association with RS (TableS5B–S6B), with the exception of the linear regression in time; therefore, older clades should be richer in species than younger ones. Older clades should also have accumu- model including 5%DI. Since other factors may influence speciation processes, lated more extinction events than younger ones. Correlation tests and linear regressions between clade age and species we tested the association between RS and two important life history traits, i.e., body mass and generation time (see richness on all the 152 mammalian families (Table S1) were found to be statistically non-significant (P value 0.82) (Fig. Materials and Methods and Table S7). The results of the Spearman correlation test suggest that S1). Correlation tests between the number of extinct spe- cies recorded for each clade (Table S2) and its age resulted high body mass is related to low RS (and vice versa, P value 0.021) and short generation time is related to high RS (and in a non-significant association of those variables (P value 0.95) (Table S3). Furthermore, the extinction rate of a clade vice versa, P value 0.008) (Table S8). Having ascertained that there is a potential relationship (calculated as extinct species/total species) does not show significant correlation with the clade’s age (P value 0.81) between life history traits and the rates of speciation, we tested if these non-genomic traits also show a correlation (Table S3). A linear regression model associating the rate of extinction and the clade age is, again, non-significant (P with TE activity. However, tests showed no correlation between these factors (Table S9–S10), with the only excep- value 0.87) (Fig. S2, Table S3). Thus, the PG model does not seem to describe mamma- tion of generation time, shows a significant correlation with 5%DI. This association likely reflects the possible influence lian evolution accurately, confirming previously reported results (Mattila and Bokma 2008). of meiosis frequency in the rate of TE accumulation in the long term. In fact, a higher number of generations imply Rate of Speciation (RS), Life History Traits, that more TE insertion events are likely to have occurred and might have been transmitted from one generation to the and Density of Insertion (DI) other. However, this effect seems to be only visible in a consid - In order to evaluate TE activity in mammalian genomes, we took into account the data produced by the study of Jurka erable amount of time and in a larger dataset of TE inser- tions (5%DI). We conclude that, while other parameters et al. (2011) (Table S4) that provide the number of inser- tions and the number of TE families (NF) diverging less may impact TE dynamics, speciation rates in mammals are strongly and unambiguously related to TE activity, espe- than 1% and less than 5% (1NF, 5%NF) from their consen- sus sequences. The consensus sequence for a transposable cially recent TE bursts (1%DI). Based on these results, it is tempting to speculate that the repertoire and activity of element is the best approximation of the active element that gave rise to the different insertions in a genome. The diver - TEs in a given genome might contribute to its capability to diversify. gence from consensus, on a large scale, is a proxy for the insertions’ age (Jurka et al. 2011). Therefore, we considered Relative Rate of Speciation (RRS) insertions diverging less than 1% as more recent, while those diverging less than 5% as older. Under a non-gradualistic model of speciation and differen- We designed a parameter called density of insertion (DI), which is the ratio between the number of TE insertions in tiation, RS, or the number of species alone, cannot identify and relatively locate finer adaptive radiation events within a genome and its size, to summarize the level of TE activ- ity in a genome. We calculated the DI at both divergence single taxonomical groups. In order to identify these events, we designed a new parameter called Relative rate of specia- thresholds (1DI and 5%DI). As for the rates of speciation (RS), we calculated them as tion (RRS) (Fig. 1c). RRS is a conditional parameter that compares a pair of taxa at the same hierarchical level (e.g., the ratio between the number of extant species and the crown age (CA) of the taxon of interest (see “Materials and Meth- two families within the same order). Briefly, if one taxon of a given pair at the same time shows (1) a higher number of ods” for details). We finally tested the hypothesis that TE activity is related with speciation patterns by estimating the species and (2) a lower age compared to its paired taxon, then its RRS is positive (+) and putatively experienced a association between NF, DI, and RS (Fig. 2) with Spearman 1 3 Journal of Molecular Evolution Fig. 2 Relationship between the rate of speciation (RS) and TEs activity estimated according to the four considered param- eters (1DI, 5DI, 1NF, 5%NF) in the 29 mammalian families of Eutheria. The families are arranged in the increasing order of RS (see also Table S11) (relatively) recent speciation burst. Consequently, the other RRS and DI Between Mammalian Families taxon has a negative RRS(−) and is experiencing a more static phase (Fig. 1c). If only one of the two conditions is At the lowest taxonomical level hereby considered (families met, there is no evidence of adaptive radiation/stasis for within orders), we compared 15 mammalian species (encom- neither of the two taxa (RRS = 0) (see Materials and Meth- passing six orders) arranged in 16 pairs (Table S11A). For ods and Supplementary Text 1). RRS can be applied at any each genome, we calculated the four parameters described taxonomical level on any monophyletic clade. In order to above (1DI, 5%DI, 1NF, 5%NF; Table S10). We tested the minimize the impact of external factors (such as differen- association between putative “hot”/“cold” genomes (defined tial generation time and genomic mutation rate of species via RRS) and TE activity (DI and NF) with the paired Wil- belonging to distantly related taxa), we applied the RRS to coxon signed-rank test. All tests, excluding 5%DI, were sig- mammalian families that belong to the same order and to nificant (Table S12). The parameter with the highest confi- mammalian superorders belonging to the same subclass. dence is 1%DI (Fig. 3a, Table S12). Using 1%DI, 14 out of Given the genomic impact of transposable elements, we 16 pairs matched the RRS results (Table S13, Supplemen- expect that genomes with higher TE activity (“hot”) should tary Text 2). Furthermore, 11 pairs showed a difference in correspond to RRS(+) taxa, while RRS(−) taxa should have DI of at least one order of magnitude, up to almost 180-fold lower TE activity (“cold” genomes). higher (Macaca mulatta vs. Tarsius syrichta). 1 3 Journal of Molecular Evolution Fig. 3 a 1%DI values in the 16 pairs of mammalian species which exhibit evidence of adaptive radiation/stasis. Blue bars: RRS(−) (putative “cold” genomes); red bars: RRS(+) (putative “hot” genomes). I Carnivora, II Cetartiodactyla, III Chiroptera, IV Primates, V Rodentia. b Comparison of the 1DI and 5%DI in the 4 superorders of Eutheria. Blue bars: RRS(−) (putative “cold” genomes); red bars: RRS(+) (putative “hot” genomes). P value < 0.05. (Color figure online) RRS was estimated also considering the sum of the on the contrary, the relative level of TE activity between extant and extinct species for each taxon. By doing this, two taxa is highly related to their relative ability to dif- the number of possible comparisons increases from 16 ferentiate and speciate. In addition, 1%DI seems to be a to 20 (Table S11B). We tested the new list of paired spe- more sensible parameter than NF for measuring recent TE cies using the most descriptive among our four genomic activity (Supplementary Text 2). parameters, i.e., 1%DI (Fig. S3). The Wilcoxon Signed- −5 Rank test was highly significant (P value 6×10 ), with RRS and DI Between Placentalia Superorders 18 out of 20 pairs following the expected trend. Thus, the inclusion of extinct species not only confirmed, but Next, we tested such association at a higher taxonomic also enhanced the robustness of the association between level considering the Placentalia superorders of Afrotheria TE activity and adaptive radiation events using RRS as a (A), Euarchontoglires (E), Laurasiatheria (L), and Xenar- comparative strategy for speciation. thra (X) (Fig. 3b, Table S14). According to RRS results, Overall, our RRS results suggest that, in mammals, the E and L showed RRS(+), thus putatively they are “hot” recent TE activity is associated with recent adaptive radi- taxa, while A and X showed RRS(−), thus putatively they ation. Therefore, we can conclude that the activity of TEs are “cold” taxa (Fig. 1a, Table S14). After averaging their does not vary randomly within the mammalian phylogeny: respective DIs, we merged the putatively “hot” superorders 1 3 Journal of Molecular Evolution (E and L, 22 species) and the putatively “cold” superorders a major role in contributing to the genomic plasticity neces- (A and X, 5 species) and tested their association with DI sary for species differentiation. as above (Supplementary Text 3). For both 1DI and 5%DI, Then, we designed a new parameter, the Relative Rate of “cold” superorders show an averaged DI more than three- Speciation (RRS), as a tool to identify finer adaptive radia- fold lower than “hot” superorders. tion events that occurred within orders of the mammalian Differently from what is observed at the lower taxonomi- class. That way, we further strengthened the positive asso- cal level, 5%DI yields a significant difference between the ciation between TEs and recent bursts of speciation. In fact, two groups, while the 1%DI shows a non-significant asso- taxa that experienced a recent radiation (RRS(+)) were con- ciation (Fig. 3b, Table S15). This discrepancy between the sidered as “hot genomes” and showed a strong association lower and higher taxonomical levels may be interpreted with high TE activity, whereas taxa that are less likely to from an evolutionary point of view. In fact, 5%DI, which have experienced recent bursts of differentiation (RRS(−), represents older accumulation of TE insertions, is the worst “cold genomes”) generally show lower TE activity. In addi- predictor of TE activity among the four considered param- tion, we showed that TE insertions and their approximate eters (1DI, 5%DI, 1NF, 5%NF) when studying recent specia- occurrence times are consistent with clade differentiation tion (Fig. 3a, Table S12). On the contrary, it is the best one estimates: older TE bursts are associated to older adaptive when considering older macroevolutionary events, such as radiation events (origin of mammalian superorders), whereas the differentiation of the four Eutheria superorders (Fig.  3b, novel TE bursts correlate to newer evolutionary phenomena Table S15). Hence, the divergence of the elements from their (origin of mammalian families). consensus does reflect, on average, their age (Jurka et al. A number of recent studies suggests that TEs seem to 2011), and related adaptive radiation events. be important for adaptive radiation (Carmi et  al. 2011; Belyayev 2014; Elbarbary et al. 2016; Huff et al. 2016). TEs, which probably reach fixation during speciation events by Discussion and Conclusions genetic drift (Jurka et al. 2011), have been associated with a variety of relevant biological innovations (Richardson et al. With this study, we explored the relationship between TEs 2015). TEs also have been shown to have a wide variety of activity and speciation patterns in the mammalian lineage, functional/regulatory effects on the loci in which they insert highlighting their impact in the evolution of this phylum and (Goodier and Kazazian 2008; Cordaux and Batzer 2009), in particular their possible association with bursts of specia- potentially generating new functional variants. Therefore, tion. Of course, we cannot exclude that taxonomical errors, we could speculate that TE activity influences speciation such as the presence of cryptic species Bickford et al. (2007) patterns in mammals. However, since differential molecu- or inappropriate descriptions of new taxa (Komarek and lar evolution rates are positively correlated with punctuated Beutel 2006; Zachos 2018), could propagate into our conclu- patterns of speciation (Pagel et al. 2006), the observed TE sions. However, compared to other clades, the mammalian insertion patterns may be interpreted as the outcome of the taxonomy is undeniably quite well studied, and, additionally, same processes that affect the rate of speciation at a popula- the families here considered encompass a varied number of tion level. TE activity would then follow speciation events, documented species (minimum: 7, maximum: 690, mean: and not the contrary, closely reflecting adaptive radiation 129 spp). We believe that these facts should minimize the (and promising to be ideal markers for phylogenetic analy- probability of introducing biases in our analyses. ses, as they are virtually homoplasy-free). We started our study by showing that neither speciation In conclusion, we hypothesize that TE activity is modu- nor extinction rates in mammals do follow a regular trend as lated in evolutionary time frames, producing alternations of predicted by phyletic gradualism, which therefore does not insertional bursts and silencing (Muñoz-Lopez et al. 2011), seem to be the best model to explain evolutionary patterns which is consistent with the molecular processes that should in the considered class. occur as stated by the PE theory. Accordingly, recent stud- Despite being influenced by a wide variety of biologi- ies show that young LINE-1 elements are mostly repressed cal processes and life history traits, speciation revealed a via methylation while old TEs are regulated by the KRAB/ strong association with the activity of TEs. In particular, our KAP1 system (Castro-Diaz et  al. 2015). Less-strongly analysis of TE content of the considered genomes showed silenced elements can produce bursts of insertions, poten- that a high differentiation rate in a taxon is strongly related tially generating many new variants in a short time and lead- to an increased molecular activity of the TEs (Feiner 2016). ing to a “hot” state of the host genome, which is highly capa- Additionally, the measured TE parameters seem to be mostly ble of responding to environmental stresses and selective unrelated to life history traits, such as body mass and gen- pressures. While silencing mechanisms progressively inhibit eration time, suggesting that TE activity can autonomously TE activity (inducing a state of “cold” genome), their lack affect differentiation processes. Therefore, TEs might play of contribution to molecular differentiation might lead to a 1 3 Journal of Molecular Evolution relatively static phase that is consistent with variable-rate therefore RRS = 0. RRS was applied on couples of families speciation patterns. Species harboring these static genomes belonging to the same order (Table S11, Supplementary Text could, in evolutionary time frames, be less likely to adapt to 2) and to the four superorders of Eutheria (Table S14, Sup- environmental changes, thus being more likely to become plementary Text 3). RRS determination was also repeated extinct. Both factors (i.e., TE activity/inactivity influencing including extinct species in NS. speciation or extinction respectively) could account for spe- All Spearman correlation tests and linear regres- cies variability and phylogenetic relationships observed in sion models were performed in R (cor.test with present-day mammals. method="spearman” and lm functions, respectively). Whether TE mobilization and accumulation of new inser- We tested the correlation between putative “hot”/“cold” tions is the cause or the effect of adaptive radiation/specia- genomes and RRS(+/−) using the Wilcoxon Signed-Rank tion remains open for debate. However, the results presented Test for both families and superorders (wilcox.test func- in this study and the intrinsic characteristics of the mobilome tion). All statistical analyses and graphs were performed/ activity suggest that TEs might have played an important produced with the R software. role in the molecular differentiation of mammals and can Acknowledgements The authors would like to acknowledge and thank continue to influence the evolution of their genomes. Piero Angela, the greatest Italian scientific journalist and popularizer, for his inspirational contribution in the cultural advancement of our country. Materials and Methods Compliance with Ethical Standards The numbers of species for all 152 mammalian families Conflict of interest The authors declared that they have no conflict of interest. listed in the last mammalian phylogeny (Meredith et  al. 2011) were retrieved from Catalogue of Life (http://www. Open Access This article is distributed under the terms of the Crea- catalogueo flif e.com ), whereas the number of extinct species tive Commons Attribution 4.0 International License (http://creat iveco from Paleobiology Database (https://paleo biodb .or g). Their mmons.or g/licenses/b y/4.0/), which permits unrestricted use, distribu- tion, and reproduction in any medium, provided you give appropriate crown ages (CA) were estimated from the timed phyloge- credit to the original author(s) and the source, provide a link to the netic tree (Meredith et al. 2011). 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Transposable Elements Activity is Positively Related to Rate of Speciation in Mammals

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Abstract

Transposable elements (TEs) play an essential role in shaping eukaryotic genomes and generating variability. Speciation and TE activity bursts could be strongly related in mammals, in which simple gradualistic models of differentiation do not account for the currently observed species variability. In order to test this hypothesis, we designed two parameters: the Density of insertion (DI) and the Relative rate of speciation (RRS). DI is the ratio between the number of TE insertions in a genome and its size, whereas the RRS is a conditional parameter designed to identify potential speciation bursts. Thus, by analyzing TE insertions in mammals, we defined the genomes as “hot” (high DI) and “cold” (low DI). Then, comparing TE activity among 29 taxonomical families of the whole Mammalia class, 16 intra-order pairs of mammalian species, and four superorders of Eutheria, we showed that taxa with high rates of speciation are associated with “hot” genomes, whereas taxa with low ones are associated with “cold” genomes. These results suggest a remarkable correlation between TE activity and speciation, also being consistent with patterns describing variable rates of differentiation and accounting for the different time frames of the speciation bursts. Keywords Speciation · Rate of speciation · Transposable elements · Cold genome · Relative rate of speciation · Mammals evolution Introduction but they also have been a great source of genomic innova- tions (Richardson et al. 2015). For example, TEs play an Transposable elements (TEs) are DNA sequences that are important role in telomere maintenance (Farkash and Prak able to move and replicate throughout the genome. They 2006), rewiring of transcriptional networks (Kunarso et al. can be highly deleterious when inserted in genetic regions 2010), regulation of gene expression (Chuong et al. 2016), ectopic recombination, and chromosomal rearrangements (Fedoroff 2012). Furthermore, TEs have been key contribu- Electronic supplementary material The online version of this tors to evolution (Biemont 2010; Oliver et al. 2013; Kapusta article (https ://doi.org/10.1007/s0023 9-018-9847-7) contains et  al. 2017) and led the insurgences of the V(D)J system supplementary material, which is available to authorized users. of acquired immunity (Kapitonov and Jurka 2005; Koonin Ricci Marco, Peona Valentina as well as Taccioli Cristian, Boattini and Krupovic 2014) and mammalian placenta (Lynch et al. Alessio have contributed equally to this study. 2011). Given their huge impact on shaping genomes, TEs are also thought to influence differentiation (Huff et al. 2016) * Ricci Marco and speciation as proposed by the Epi-Transposon (Zeh et al. marco.ricci19@unibo.it 2009), CArrier SubPopulation (Jurka et al. 2011), and TE- * Guichard Etienne Thrust (Oliver and Greene 2012) hypotheses. etienne.guichard2@unibo.it Phyletic gradualism (PG) (Charlesworth et al. 1982) and Department of Biological, Geological and Environmental punctuated equilibria (PE) (Eldredge and Gould 1972) are Sciences, University of Bologna, Bologna, Italy the most important evolutionary theories for explaining spe- Department of Ecology and Genetics, University of Uppsala, ciation dynamics. According to PG, species continuously Uppsala, Sweden accumulate mutations that would eventually lead to differ - Department of Animal Medicine, Health and Production, entiation and speciation (McPeek and Brown 2007). Instead, University of Padova, Padova, Italy Vol.:(0123456789) 1 3 Journal of Molecular Evolution the PE theory suggests that rapid bursts of differentiation This specific case led to the hypothesis that Mammals with and speciation are alternated to “static” phases in which higher rates of speciation should show higher TE activity organisms do not significantly change (Eldredge and Gould (“hot” genomes). Conversely, taxa with low rates of specia- 1972). Authors as Mattila and Bokma (2008) suggest that tion should exhibit a lower TE activity (“cold” genomes; the PE theory should be taken into account for a more com- Fig. 1b, c). plete and accurate explanation of mammalian evolutionary In this study, we assess and test the association between dynamics. If TEs widely influenced speciation, as suggested speciation and TE activity in mammals, by taking into by the previously reported hypotheses, it should be possible account both extant and extinct species. In fact, mammals to find an association between the profiles of TE activity have particularly detailed TEs annotation (Jurka et al. 2011) within genomes and patterns of speciation of organisms. as well as a reliable phylogeny (Meredith et al. 2011) and For instance, the well-characterized mammalian phylogeny abundant fossil records (Paleobiology Database 2018). (Meredith et al. 2011) shows that the order Monotremata is the most ancient and the poorest in living species (Fig. 1a). Accordingly, the platypus genome, belonging to this taxon, should harbor the lowest number of recently mobilized TEs, which was actually demonstrated by Jurka et  al. (2011). Fig. 1 a Tree of mammals. Species abundance and phylogenetic rela- Exemplified use of the relative rate of speciation (RRS) within the tionships of the main mammalian clades. Putatively “hot” superorders order Primates. I Galagidae, when compared to Cercopithecidae, of Eutheria (RRS(+)) are shown in red; putatively“cold” superorders are older and poorer in species, thus Galagidae: RRS(−), Cerco- (RRS(−)) are shown in blue. Animal icons made by Freepik from pithecidae: RRS(+). II Galagidae, when compared to Tarsiidae, are http://www.flati con.com b Modelization of the Cold Genome hypoth- younger and richer in species, thus Galagidae: RRS(+) and Tarsii- esis. “Hot” genomes contain a fraction of active, recently mobilized dae: RRS(−). III Cercopithecidae when compared to Tarsiidae, are TEs (diverging less than 1% from their consensus sequence). “Inter- younger and richer in species, thus Cercopithecidae: RRS(+) and mediate” genomes contain a fraction of less recently mobilized TEs Tarsiidae: RRS(−). (Color code: RRS(+): red; RRS(−): blue). (Color (diverging less than 5% from their consensus sequence). “Cold” figure online) genomes show ancient insertions with very low or absent activity. c 1 3 Journal of Molecular Evolution correlation and linear regression models (Table S5A-S6A). Testing Phyletic Gradualism for Speciation and Extinction Notably, all the parameters showed significant correlation with RS in the whole Mammalia class. In particular, lin- In order to establish if the speciation rates varied or remained ear models (Table S6A) showed positive regression coef- ficients and significant P values for all parameters except constant among the mammalian families, we have tested the prevalence of phyletic gradualism as a model of speciation. 5%DI. When extinct species are included in the RS calcula- tion (Fig. S3), we obtained similar results. In fact, all the The main assumption of the PG theory is that genomes accu- mulate mutations and clades accumulate species constantly parameters show a significantly positive association with RS (TableS5B–S6B), with the exception of the linear regression in time; therefore, older clades should be richer in species than younger ones. Older clades should also have accumu- model including 5%DI. Since other factors may influence speciation processes, lated more extinction events than younger ones. Correlation tests and linear regressions between clade age and species we tested the association between RS and two important life history traits, i.e., body mass and generation time (see richness on all the 152 mammalian families (Table S1) were found to be statistically non-significant (P value 0.82) (Fig. Materials and Methods and Table S7). The results of the Spearman correlation test suggest that S1). Correlation tests between the number of extinct spe- cies recorded for each clade (Table S2) and its age resulted high body mass is related to low RS (and vice versa, P value 0.021) and short generation time is related to high RS (and in a non-significant association of those variables (P value 0.95) (Table S3). Furthermore, the extinction rate of a clade vice versa, P value 0.008) (Table S8). Having ascertained that there is a potential relationship (calculated as extinct species/total species) does not show significant correlation with the clade’s age (P value 0.81) between life history traits and the rates of speciation, we tested if these non-genomic traits also show a correlation (Table S3). A linear regression model associating the rate of extinction and the clade age is, again, non-significant (P with TE activity. However, tests showed no correlation between these factors (Table S9–S10), with the only excep- value 0.87) (Fig. S2, Table S3). Thus, the PG model does not seem to describe mamma- tion of generation time, shows a significant correlation with 5%DI. This association likely reflects the possible influence lian evolution accurately, confirming previously reported results (Mattila and Bokma 2008). of meiosis frequency in the rate of TE accumulation in the long term. In fact, a higher number of generations imply Rate of Speciation (RS), Life History Traits, that more TE insertion events are likely to have occurred and might have been transmitted from one generation to the and Density of Insertion (DI) other. However, this effect seems to be only visible in a consid - In order to evaluate TE activity in mammalian genomes, we took into account the data produced by the study of Jurka erable amount of time and in a larger dataset of TE inser- tions (5%DI). We conclude that, while other parameters et al. (2011) (Table S4) that provide the number of inser- tions and the number of TE families (NF) diverging less may impact TE dynamics, speciation rates in mammals are strongly and unambiguously related to TE activity, espe- than 1% and less than 5% (1NF, 5%NF) from their consen- sus sequences. The consensus sequence for a transposable cially recent TE bursts (1%DI). Based on these results, it is tempting to speculate that the repertoire and activity of element is the best approximation of the active element that gave rise to the different insertions in a genome. The diver - TEs in a given genome might contribute to its capability to diversify. gence from consensus, on a large scale, is a proxy for the insertions’ age (Jurka et al. 2011). Therefore, we considered Relative Rate of Speciation (RRS) insertions diverging less than 1% as more recent, while those diverging less than 5% as older. Under a non-gradualistic model of speciation and differen- We designed a parameter called density of insertion (DI), which is the ratio between the number of TE insertions in tiation, RS, or the number of species alone, cannot identify and relatively locate finer adaptive radiation events within a genome and its size, to summarize the level of TE activ- ity in a genome. We calculated the DI at both divergence single taxonomical groups. In order to identify these events, we designed a new parameter called Relative rate of specia- thresholds (1DI and 5%DI). As for the rates of speciation (RS), we calculated them as tion (RRS) (Fig. 1c). RRS is a conditional parameter that compares a pair of taxa at the same hierarchical level (e.g., the ratio between the number of extant species and the crown age (CA) of the taxon of interest (see “Materials and Meth- two families within the same order). Briefly, if one taxon of a given pair at the same time shows (1) a higher number of ods” for details). We finally tested the hypothesis that TE activity is related with speciation patterns by estimating the species and (2) a lower age compared to its paired taxon, then its RRS is positive (+) and putatively experienced a association between NF, DI, and RS (Fig. 2) with Spearman 1 3 Journal of Molecular Evolution Fig. 2 Relationship between the rate of speciation (RS) and TEs activity estimated according to the four considered param- eters (1DI, 5DI, 1NF, 5%NF) in the 29 mammalian families of Eutheria. The families are arranged in the increasing order of RS (see also Table S11) (relatively) recent speciation burst. Consequently, the other RRS and DI Between Mammalian Families taxon has a negative RRS(−) and is experiencing a more static phase (Fig. 1c). If only one of the two conditions is At the lowest taxonomical level hereby considered (families met, there is no evidence of adaptive radiation/stasis for within orders), we compared 15 mammalian species (encom- neither of the two taxa (RRS = 0) (see Materials and Meth- passing six orders) arranged in 16 pairs (Table S11A). For ods and Supplementary Text 1). RRS can be applied at any each genome, we calculated the four parameters described taxonomical level on any monophyletic clade. In order to above (1DI, 5%DI, 1NF, 5%NF; Table S10). We tested the minimize the impact of external factors (such as differen- association between putative “hot”/“cold” genomes (defined tial generation time and genomic mutation rate of species via RRS) and TE activity (DI and NF) with the paired Wil- belonging to distantly related taxa), we applied the RRS to coxon signed-rank test. All tests, excluding 5%DI, were sig- mammalian families that belong to the same order and to nificant (Table S12). The parameter with the highest confi- mammalian superorders belonging to the same subclass. dence is 1%DI (Fig. 3a, Table S12). Using 1%DI, 14 out of Given the genomic impact of transposable elements, we 16 pairs matched the RRS results (Table S13, Supplemen- expect that genomes with higher TE activity (“hot”) should tary Text 2). Furthermore, 11 pairs showed a difference in correspond to RRS(+) taxa, while RRS(−) taxa should have DI of at least one order of magnitude, up to almost 180-fold lower TE activity (“cold” genomes). higher (Macaca mulatta vs. Tarsius syrichta). 1 3 Journal of Molecular Evolution Fig. 3 a 1%DI values in the 16 pairs of mammalian species which exhibit evidence of adaptive radiation/stasis. Blue bars: RRS(−) (putative “cold” genomes); red bars: RRS(+) (putative “hot” genomes). I Carnivora, II Cetartiodactyla, III Chiroptera, IV Primates, V Rodentia. b Comparison of the 1DI and 5%DI in the 4 superorders of Eutheria. Blue bars: RRS(−) (putative “cold” genomes); red bars: RRS(+) (putative “hot” genomes). P value < 0.05. (Color figure online) RRS was estimated also considering the sum of the on the contrary, the relative level of TE activity between extant and extinct species for each taxon. By doing this, two taxa is highly related to their relative ability to dif- the number of possible comparisons increases from 16 ferentiate and speciate. In addition, 1%DI seems to be a to 20 (Table S11B). We tested the new list of paired spe- more sensible parameter than NF for measuring recent TE cies using the most descriptive among our four genomic activity (Supplementary Text 2). parameters, i.e., 1%DI (Fig. S3). The Wilcoxon Signed- −5 Rank test was highly significant (P value 6×10 ), with RRS and DI Between Placentalia Superorders 18 out of 20 pairs following the expected trend. Thus, the inclusion of extinct species not only confirmed, but Next, we tested such association at a higher taxonomic also enhanced the robustness of the association between level considering the Placentalia superorders of Afrotheria TE activity and adaptive radiation events using RRS as a (A), Euarchontoglires (E), Laurasiatheria (L), and Xenar- comparative strategy for speciation. thra (X) (Fig. 3b, Table S14). According to RRS results, Overall, our RRS results suggest that, in mammals, the E and L showed RRS(+), thus putatively they are “hot” recent TE activity is associated with recent adaptive radi- taxa, while A and X showed RRS(−), thus putatively they ation. Therefore, we can conclude that the activity of TEs are “cold” taxa (Fig. 1a, Table S14). After averaging their does not vary randomly within the mammalian phylogeny: respective DIs, we merged the putatively “hot” superorders 1 3 Journal of Molecular Evolution (E and L, 22 species) and the putatively “cold” superorders a major role in contributing to the genomic plasticity neces- (A and X, 5 species) and tested their association with DI sary for species differentiation. as above (Supplementary Text 3). For both 1DI and 5%DI, Then, we designed a new parameter, the Relative Rate of “cold” superorders show an averaged DI more than three- Speciation (RRS), as a tool to identify finer adaptive radia- fold lower than “hot” superorders. tion events that occurred within orders of the mammalian Differently from what is observed at the lower taxonomi- class. That way, we further strengthened the positive asso- cal level, 5%DI yields a significant difference between the ciation between TEs and recent bursts of speciation. In fact, two groups, while the 1%DI shows a non-significant asso- taxa that experienced a recent radiation (RRS(+)) were con- ciation (Fig. 3b, Table S15). This discrepancy between the sidered as “hot genomes” and showed a strong association lower and higher taxonomical levels may be interpreted with high TE activity, whereas taxa that are less likely to from an evolutionary point of view. In fact, 5%DI, which have experienced recent bursts of differentiation (RRS(−), represents older accumulation of TE insertions, is the worst “cold genomes”) generally show lower TE activity. In addi- predictor of TE activity among the four considered param- tion, we showed that TE insertions and their approximate eters (1DI, 5%DI, 1NF, 5%NF) when studying recent specia- occurrence times are consistent with clade differentiation tion (Fig. 3a, Table S12). On the contrary, it is the best one estimates: older TE bursts are associated to older adaptive when considering older macroevolutionary events, such as radiation events (origin of mammalian superorders), whereas the differentiation of the four Eutheria superorders (Fig.  3b, novel TE bursts correlate to newer evolutionary phenomena Table S15). Hence, the divergence of the elements from their (origin of mammalian families). consensus does reflect, on average, their age (Jurka et al. A number of recent studies suggests that TEs seem to 2011), and related adaptive radiation events. be important for adaptive radiation (Carmi et  al. 2011; Belyayev 2014; Elbarbary et al. 2016; Huff et al. 2016). TEs, which probably reach fixation during speciation events by Discussion and Conclusions genetic drift (Jurka et al. 2011), have been associated with a variety of relevant biological innovations (Richardson et al. With this study, we explored the relationship between TEs 2015). TEs also have been shown to have a wide variety of activity and speciation patterns in the mammalian lineage, functional/regulatory effects on the loci in which they insert highlighting their impact in the evolution of this phylum and (Goodier and Kazazian 2008; Cordaux and Batzer 2009), in particular their possible association with bursts of specia- potentially generating new functional variants. Therefore, tion. Of course, we cannot exclude that taxonomical errors, we could speculate that TE activity influences speciation such as the presence of cryptic species Bickford et al. (2007) patterns in mammals. However, since differential molecu- or inappropriate descriptions of new taxa (Komarek and lar evolution rates are positively correlated with punctuated Beutel 2006; Zachos 2018), could propagate into our conclu- patterns of speciation (Pagel et al. 2006), the observed TE sions. However, compared to other clades, the mammalian insertion patterns may be interpreted as the outcome of the taxonomy is undeniably quite well studied, and, additionally, same processes that affect the rate of speciation at a popula- the families here considered encompass a varied number of tion level. TE activity would then follow speciation events, documented species (minimum: 7, maximum: 690, mean: and not the contrary, closely reflecting adaptive radiation 129 spp). We believe that these facts should minimize the (and promising to be ideal markers for phylogenetic analy- probability of introducing biases in our analyses. ses, as they are virtually homoplasy-free). We started our study by showing that neither speciation In conclusion, we hypothesize that TE activity is modu- nor extinction rates in mammals do follow a regular trend as lated in evolutionary time frames, producing alternations of predicted by phyletic gradualism, which therefore does not insertional bursts and silencing (Muñoz-Lopez et al. 2011), seem to be the best model to explain evolutionary patterns which is consistent with the molecular processes that should in the considered class. occur as stated by the PE theory. Accordingly, recent stud- Despite being influenced by a wide variety of biologi- ies show that young LINE-1 elements are mostly repressed cal processes and life history traits, speciation revealed a via methylation while old TEs are regulated by the KRAB/ strong association with the activity of TEs. In particular, our KAP1 system (Castro-Diaz et  al. 2015). Less-strongly analysis of TE content of the considered genomes showed silenced elements can produce bursts of insertions, poten- that a high differentiation rate in a taxon is strongly related tially generating many new variants in a short time and lead- to an increased molecular activity of the TEs (Feiner 2016). ing to a “hot” state of the host genome, which is highly capa- Additionally, the measured TE parameters seem to be mostly ble of responding to environmental stresses and selective unrelated to life history traits, such as body mass and gen- pressures. While silencing mechanisms progressively inhibit eration time, suggesting that TE activity can autonomously TE activity (inducing a state of “cold” genome), their lack affect differentiation processes. Therefore, TEs might play of contribution to molecular differentiation might lead to a 1 3 Journal of Molecular Evolution relatively static phase that is consistent with variable-rate therefore RRS = 0. RRS was applied on couples of families speciation patterns. Species harboring these static genomes belonging to the same order (Table S11, Supplementary Text could, in evolutionary time frames, be less likely to adapt to 2) and to the four superorders of Eutheria (Table S14, Sup- environmental changes, thus being more likely to become plementary Text 3). RRS determination was also repeated extinct. Both factors (i.e., TE activity/inactivity influencing including extinct species in NS. speciation or extinction respectively) could account for spe- All Spearman correlation tests and linear regres- cies variability and phylogenetic relationships observed in sion models were performed in R (cor.test with present-day mammals. method="spearman” and lm functions, respectively). Whether TE mobilization and accumulation of new inser- We tested the correlation between putative “hot”/“cold” tions is the cause or the effect of adaptive radiation/specia- genomes and RRS(+/−) using the Wilcoxon Signed-Rank tion remains open for debate. However, the results presented Test for both families and superorders (wilcox.test func- in this study and the intrinsic characteristics of the mobilome tion). All statistical analyses and graphs were performed/ activity suggest that TEs might have played an important produced with the R software. role in the molecular differentiation of mammals and can Acknowledgements The authors would like to acknowledge and thank continue to influence the evolution of their genomes. Piero Angela, the greatest Italian scientific journalist and popularizer, for his inspirational contribution in the cultural advancement of our country. Materials and Methods Compliance with Ethical Standards The numbers of species for all 152 mammalian families Conflict of interest The authors declared that they have no conflict of interest. listed in the last mammalian phylogeny (Meredith et  al. 2011) were retrieved from Catalogue of Life (http://www. Open Access This article is distributed under the terms of the Crea- catalogueo flif e.com ), whereas the number of extinct species tive Commons Attribution 4.0 International License (http://creat iveco from Paleobiology Database (https://paleo biodb .or g). Their mmons.or g/licenses/b y/4.0/), which permits unrestricted use, distribu- tion, and reproduction in any medium, provided you give appropriate crown ages (CA) were estimated from the timed phyloge- credit to the original author(s) and the source, provide a link to the netic tree (Meredith et al. 2011). Data about body mass and Creative Commons license, and indicate if changes were made. generation time have been retrieved from Animal Diversity Web (https://anima ldiv ersity .or g). For each species, the gen- eration time has been calculated as the sum of gestation time and the time from birth to the sexual maturity measured in References months (namely, the time passed from a meiosis to the next). The body mass has been calculated as the median between Belyayev A (2014) Bursts of transposable elements as an evolution- the average body mass of males and females of each species ary driving force. J Evol Biol 27:2573–2584 measured in kg. Data about TE families and TE insertions in Bickford D, Lohman DJ, Sodhi NS et al (2006) Cryptic species as a window on diversity and conservation. Trends Ecol Evol. https the genomes of the considered species were retrieved from ://doi.org/10.1016/j.tree.2006.11.004 Jurka et al. 2011. 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Journal of Molecular EvolutionSpringer Journals

Published: May 31, 2018

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