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 Transposable elements (TEs) are DNA sequences that are able to move and replicate throughout the genome. They can be highly deleterious when inserted in genetic regions Electronic supplementary material The online version of this article (https ://doi.org/10.1007/s0023 9-018-9847-7) contains but they also have been a great source of genomic innova- supplementary material, which is available to authorized users. tions (Richardson et al. 2015). For example, TEs play an important role in telomere maintenance (Farkash and Prak Marco Ricci, Valentina Peona as well as Cristian Taccioli, Alessio 2006), rewiring of transcriptional networks (Kunarso et al. Boattini have contributed equally to this study. 2010), regulation of gene expression (Chuong et al. 2016), The original version of this article was revised. Given name and ectopic recombination, and chromosomal rearrangements Surname of all authors are corrected. (Fedoroff 2012). Furthermore, TEs have been key contribu- tors to evolution (Biemont 2010; Oliver et al. 2013; Kapusta * Marco Ricci et al. 2017) and led the insurgences of the V(D)J system email@example.com of acquired immunity (Kapitonov and Jurka 2005; Koonin * Etienne Guichard and Krupovic 2014) and mammalian placenta (Lynch et al. firstname.lastname@example.org 2011). Given their huge impact on shaping genomes, TEs Department of Biological, Geological and Environmental are also thought to influence differentiation (Huff et al. 2016) Sciences, University of Bologna, Bologna, Italy and speciation as proposed by the Epi-Transposon (Zeh et al. Department of Ecology and Genetics, University of Uppsala, 2009), CArrier SubPopulation (Jurka et al. 2011), and TE- Uppsala, Sweden Thrust (Oliver and Greene 2012) hypotheses. Department of Animal Medicine, Health and Production, University of Padova, Padova, Italy Vol.:(0123456789) 1 3 304 Journal of Molecular Evolution (2018) 86:303–310 Phyletic gradualism (PG) (Charlesworth et al. 1982) and For instance, the well-characterized mammalian phylogeny punctuated equilibria (PE) (Eldredge and Gould 1972) are (Meredith et al. 2011) shows that the order Monotremata is the most important evolutionary theories for explaining spe- the most ancient and the poorest in living species (Fig. 1a). ciation dynamics. According to PG, species continuously Accordingly, the platypus genome, belonging to this taxon, accumulate mutations that would eventually lead to differ - should harbor the lowest number of recently mobilized TEs, entiation and speciation (McPeek and Brown 2007). Instead, which was actually demonstrated by Jurka et al. (2011). 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. 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 (2018) 86:303–310 305 as well as a reliable phylogeny (Meredith et al. 2011) and Methods” for details). We finally tested the hypothesis that abundant fossil records (Paleobiology Database 2018). TE activity is related with speciation patterns by estimating the association between NF, DI, and RS (Fig. 2) with Spear- Testing Phyletic Gradualism for Speciation man correlation and linear regression models (Table S5A- and Extinction S6A). Notably, all the parameters showed significant corre- lation with RS in the whole Mammalia class. In particular, In order to establish if the speciation rates varied or remained linear models (Table S6A) showed positive regression coef- constant among the mammalian families, we have tested the ficients and significant P values for all parameters except prevalence of phyletic gradualism as a model of speciation. 5%DI. When extinct species are included in the RS calcula- The main assumption of the PG theory is that genomes accu- tion (Fig. S3), we obtained similar results. In fact, all the mulate mutations and clades accumulate species constantly parameters show a significantly positive association with RS in time; therefore, older clades should be richer in species (TableS5B–S6B), with the exception of the linear regression than younger ones. Older clades should also have accumu- model including 5%DI. lated more extinction events than younger ones. Correlation Since other factors may influence speciation processes, tests and linear regressions between clade age and species we tested the association between RS and two important richness on all the 152 mammalian families (Table S1) were life history traits, i.e., body mass and generation time (see found to be statistically non-significant (P value 0.82) (Fig. Materials and Methods and Table S7). S1). Correlation tests between the number of extinct spe- The results of the Spearman correlation test suggest that cies recorded for each clade (Table S2) and its age resulted high body mass is related to low RS (and vice versa, P value in a non-significant association of those variables (P value 0.021) and short generation time is related to high RS (and 0.95) (Table S3). Furthermore, the extinction rate of a clade vice versa, P value 0.008) (Table S8). (calculated as extinct species/total species) does not show Having ascertained that there is a potential relationship significant correlation with the clade’s age (P value 0.81) between life history traits and the rates of speciation, we (Table S3). A linear regression model associating the rate tested if these non-genomic traits also show a correlation of extinction and the clade age is, again, non-significant (P with TE activity. However, tests showed no correlation value 0.87) (Fig. S2, Table S3). between these factors (Table S9–S10), with the only excep- Thus, the PG model does not seem to describe mamma- tion of generation time, shows a significant correlation with lian evolution accurately, confirming previously reported 5%DI. This association likely reflects the possible influence 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 Density of Insertion (DI) and might have been transmitted from one generation to the other. In order to evaluate TE activity in mammalian genomes, we However, this effect seems to be only visible in a consid - took into account the data produced by the study of Jurka erable amount of time and in a larger dataset of TE inser- et al. (2011) (Table S4) that provide the number of inser- tions (5%DI). We conclude that, while other parameters tions and the number of TE families (NF) diverging less may impact TE dynamics, speciation rates in mammals are than 1% and less than 5% (1NF, 5%NF) from their consen- strongly and unambiguously related to TE activity, espe- sus sequences. The consensus sequence for a transposable cially recent TE bursts (1%DI). Based on these results, it element is the best approximation of the active element that is tempting to speculate that the repertoire and activity of gave rise to the different insertions in a genome. The diver - TEs in a given genome might contribute to its capability to gence from consensus, on a large scale, is a proxy for the diversify. insertions’ age (Jurka et al. 2011). Therefore, we considered insertions diverging less than 1% as more recent, while those Relative Rate of Speciation (RRS) diverging less than 5% as older. We designed a parameter called density of insertion (DI), Under a non-gradualistic model of speciation and differen- which is the ratio between the number of TE insertions in tiation, RS, or the number of species alone, cannot identify a genome and its size, to summarize the level of TE activ- and relatively locate finer adaptive radiation events within ity in a genome. We calculated the DI at both divergence single taxonomical groups. In order to identify these events, thresholds (1DI and 5%DI). we designed a new parameter called Relative rate of specia- As for the rates of speciation (RS), we calculated them tion (RRS) (Fig. 1c). RRS is a conditional parameter that as the ratio between the number of extant species and the compares a pair of taxa at the same hierarchical level (e.g., crown age (CA) of the taxon of interest (see “Materials and two families within the same order). Briefly, if one taxon of 1 3 306 Journal of Molecular Evolution (2018) 86:303–310 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) a given pair at the same time shows (1) a higher number of expect that genomes with higher TE activity (“hot”) should species and (2) a lower age compared to its paired taxon, correspond to RRS(+) taxa, while RRS(−) taxa should have then its RRS is positive (+) and putatively experienced a lower TE activity (“cold” genomes). (relatively) recent speciation burst. Consequently, the other taxon has a negative RRS(−) and is experiencing a more RRS and DI Between Mammalian Families static phase (Fig. 1c). If only one of the two conditions is met, there is no evidence of adaptive radiation/stasis for At the lowest taxonomical level hereby considered (families neither of the two taxa (RRS = 0) (see Materials and Meth- within orders), we compared 15 mammalian species (encom- ods and Supplementary Text 1). RRS can be applied at any passing six orders) arranged in 16 pairs (Table S11A). For taxonomical level on any monophyletic clade. In order to each genome, we calculated the four parameters described minimize the impact of external factors (such as differen- above (1DI, 5%DI, 1NF, 5%NF; Table S10). We tested the tial generation time and genomic mutation rate of species association between putative “hot”/“cold” genomes (defined belonging to distantly related taxa), we applied the RRS to via RRS) and TE activity (DI and NF) with the paired Wil- mammalian families that belong to the same order and to coxon signed-rank test. All tests, excluding 5%DI, were sig- mammalian superorders belonging to the same subclass. nificant (Table S12). The parameter with the highest confi- Given the genomic impact of transposable elements, we dence is 1%DI (Fig. 3a, Table S12). Using 1%DI, 14 out of 1 3 Journal of Molecular Evolution (2018) 86:303–310 307 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) 16 pairs matched the RRS results (Table S13, Supplemen- Overall, our RRS results suggest that, in mammals, tary Text 2). Furthermore, 11 pairs showed a difference in the recent TE activity is associated with recent adaptive DI of at least one order of magnitude, up to almost 180-fold radiation. Therefore, we can conclude that the activity of higher (Macaca mulatta vs. Tarsius syrichta). TEs does not vary randomly within the mammalian phy- RRS was estimated also considering the sum of the logeny: on the contrary, the relative level of TE activity extant and extinct species for each taxon. By doing this, between two taxa is highly related to their relative abil- the number of possible comparisons increases from 16 ity to differentiate and speciate. In addition, 1%DI seems to 20 (Table S11B). We tested the new list of paired spe- to be a more sensible parameter than NF for measuring cies using the most descriptive among our four genomic recent TE 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, 1 3 308 Journal of Molecular Evolution (2018) 86:303–310 E and L showed RRS(+), thus putatively they are “hot” Additionally, the measured TE parameters seem to be mostly taxa, while A and X showed RRS(−), thus putatively they unrelated to life history traits, such as body mass and gen- are “cold” taxa (Fig. 1a, Table S14). After averaging their eration time, suggesting that TE activity can autonomously respective DIs, we merged the putatively “hot” superorders affect differentiation processes. Therefore, TEs might play (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 predicted by phyletic gradualism, which therefore does not of insertional bursts and silencing (Muñoz-Lopez et al. seem to be the best model to explain evolutionary patterns 2011), which is consistent with the molecular processes in the considered class. that should occur as stated by the PE theory. Accordingly, Despite being influenced by a wide variety of biologi- recent studies show that young LINE-1 elements are mostly cal processes and life history traits, speciation revealed a repressed via methylation while old TEs are regulated by strong association with the activity of TEs. In particular, our the KRAB/KAP1 system (Castro-Diaz et al. 2015). Less- analysis of TE content of the considered genomes showed strongly silenced elements can produce bursts of insertions, that a high differentiation rate in a taxon is strongly related potentially generating many new variants in a short time and to an increased molecular activity of the TEs (Feiner 2016). leading to a “hot” state of the host genome, which is highly 1 3 Journal of Molecular Evolution (2018) 86:303–310 309 capable of responding to environmental stresses and selec- RRS1(−), RRS2(+) ∶ NS1 < NS2 Λ CA1 > CA2. tive pressures. While silencing mechanisms progressively If one of these conditions is false, there is no evidence inhibit TE activity (inducing a state of “cold” genome), of adaptive radiation events between the considered taxa their lack of contribution to molecular differentiation might therefore RRS = 0. RRS was applied on couples of families lead to a relatively static phase that is consistent with vari- belonging to the same order (Table S11, Supplementary Text able-rate speciation patterns. Species harboring these static 2) and to the four superorders of Eutheria (Table S14, Sup- genomes could, in evolutionary time frames, be less likely plementary Text 3). RRS determination was also repeated to adapt to environmental changes, thus being more likely including extinct species in NS. to become extinct. Both factors (i.e., TE activity/inactiv- All Spearman correlation tests and linear regres- ity influencing speciation or extinction respectively) could sion models were performed in R (cor.test with account for species variability and phylogenetic relation- method="spearman” and lm functions, respectively). ships observed in present-day mammals. We tested the correlation between putative “hot”/“cold” Whether TE mobilization and accumulation of new inser- genomes and RRS(+/−) using the Wilcoxon Signed-Rank tions is the cause or the effect of adaptive radiation/specia- Test for both families and superorders (wilcox.test func- tion remains open for debate. However, the results presented tion). All statistical analyses and graphs were performed/ in this study and the intrinsic characteristics of the mobilome produced with the R software. activity suggest that TEs might have played an important 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. Compliance with Ethical Standards Materials and Methods Conflict of interest The authors declared that they have no conflict of The numbers of species for all 152 mammalian families 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 mmons.or g/licenses/b y/4.0/), which permits unrestricted use, distribu- from Paleobiology Database (https://paleo biodb .or g). Their 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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Published: May 31, 2018
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