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Phenotypic convergence of traits in similar environments can provide insights into the evolutionary processes shaping trait evolution. Among squamate reptiles, horn-like cephalic appendages have evolved under various selective pressures, including selection for defence, crypsis or sexual selection. Yet, among snakes, particularly vipers, the functional and evolutionary significance of horns are unknown. We used a comparative phylogenetic approach with habitat and diet data on 263 viper taxa to shed light on the selective pressures underlying horn evolution in vipers. We detected significant correlations with habitat but not diet. The relative positions of horns are ecologically divergent in that supranasal horns are positively correlated with terrestrial forest habitats while supraocular horns are negatively correlated with terrestrial forest habitats and are instead associated with arboreal or sparsely vegetated habitats. Multiple independent origins of supranasal or supraocular horns in similar habitats provide evidence of adaptive convergence. Comparisons with other snake lineages suggest that cephalic appendages may have evolved under selection for crypsis in ambush foraging snakes.

Traits shared among distantly related lineages are indicators of common evolutionary constraints, at the ecological, physiological, or molecular level. Here, we show that the vertebral stripe, a cryptic color pattern, has evolved hundreds of times in the evolutionary history of anurans (frogs and toads) and is favored in terrestrial habitats. Using a genome-wide association study, we demonstrate that variation near the Agouti signaling protein gene (ASIP) is responsible for the different vertebral stripe phenotypes in the African grass frog Ptychadena robeensis. RNAseq and real-time quantitative PCR revealed that differential expression of the gene and an adjacent long non-coding RNA is linked to patterning in this species. Surprisingly, and although the stripe phenotypes are shared with closely related species, we found that the P. robeensis alleles are private to the species and unlikely to evolve under long-term balancing selection, thus indicating that the vertebral stripe phenotypes result from parallel evolution within the group. Our findings demonstrate that this cryptic color pattern evolved rapidly and recurrently in terrestrial anurans, and therefore constitutes an ideal system to study repeated evolution.

Falcons are diverse birds of cultural and economic importance. They have undergone major lineage-specific chromosomal rearrangements, resulting in greatly-reduced chromosome counts relative to other birds. Here, we use 10X Genomics linked reads to provide new high-contiguity genomes for two gyrfalcons, a saker falcon, a lanner falcon, three subspecies of peregrine falcons, and the common kestrel. Assisted by a transcriptome sequenced from 22 gyrfalcon tissues, we annotate these genomes for a variety of genomic features, estimate historical demography, and then investigate genomic equilibrium in the context of falcon-specific chromosomal rearrangements. We find that falcon genomes are not in AT-GC equilibrium with a bias in mutations towards higher AT content; this bias is predominantly driven by—but not dependent on—hypermutability of CpG sites. Small indels and large structural variants were also biased towards insertions rather than deletions. Patterns of disequilibrium were linked to chromosomal rearrangements: falcons have lost GC content in regions that have fused to larger chromosomes from microchromosomes and gained GC content in regions of macrochromosomes that have translocated to microchromosomes. Inserted bases have accumulated on regions ancestrally belonging to microchromosomes, consistent with insertion-biased gene conversion. We also find an excess of interspersed repeats on regions of microchromosomes that have fused to macrochromosomes. Our results reveal that falcon genomes are in a state of flux. They further suggest that many of the key differences between microchromosomes and macrochromosomes are driven by differences in chromosome size, and indicate a clear role for recombination and biased-gene-conversion in determining genomic equilibrium.SignificanceFalcons are a particularly diverse and widespread genus of birds of particular cultural and economic importance. Falcons have also undergone recent large-scale chromosomal rearrangements to arrive at atypically low chromosome counts relative to other birds. We produced eight new high-quality falcon genomes to support general research on falcons, and we analyze these genomes to assess how chromosome loss has influenced specific aspects of genomic architecture.

SummaryTraits shared among distantly related lineages are indicators of common evolutionary constraints, at the ecological, physiological or molecular level. The vertebral stripe is a color pattern that is widespread across the anuran phylogeny. Despite its prevalence in the order, surprisingly little is known about the genetic basis and evolutionary dynamic of this color pattern. Here we combine histology, genome- and transcriptome-wide analyses with order-scale phylogenetic comparative analyses to investigate this common phenotype. We show that the vertebral stripe has evolved hundreds of times in the evolutionary history of anurans and is selected for in terrestrial habitats. Using the Ethiopian Ptychadena radiation as a model system, we demonstrate that variation at the ASIP gene is responsible for the different vertebral stripe phenotypes. Alleles associated to these phenotypes are younger than the split between closely related Ptychadena species, thus indicating that the vertebral stripe results from parallel evolution within the group. Our findings demonstrate that this widespread color pattern evolves rapidly and recurrently in terrestrial anurans, and therefore constitute an ideal system to study repeated evolution.

Here, we review the diversity, evolutionary history, and genomics of falcons in the context of their conservation and interactions with humans, and provide a perspective on how new genomic approaches may be applied to expand our knowledge of these topics. For millennia, humans and falcons (genus Falco) have developed unique relationships through falconry, religious rituals, conservation efforts, and human lifestyle transitions. From an evolutionary perspective, falcons remain an enigma. Having experienced several recent radiations, they have reached an unparalleled and almost global distribution, with an intrageneric species richness that is roughly an order of magnitude higher than typical within their family (Falconidae) and across other birds (Phylum: Aves). This diversity has evolved in the context of unusual genomic architecture that includes unique chromosomal rearrangements, relatively low chromosome counts, extremely low microdeletion rates, and high levels of nuclear mitochondrial DNA segments (NUMTs). These genomic peculiarities combine with high levels of ecological and organismal diversity and a legacy of human interactions to make falcons obvious candidates for evolutionary studies, providing unique research opportunities in common topics, including chromosomal evolution, the mechanics of speciation, local adaptation, domestication, and urban adaptation., Here, we review the ecology, evolutionary history, and genomics of falcons in the context of their interactions with humans, and provide perspective on how new genomic approaches may be applied to the study of these topics with implications for several fields of study, including chromosomal evolution, the mechanics of speciation, population structure, domestication, and urban adaptation.

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Gaining a better understanding on how selection and neutral processes affect genomic diversity is essential to gain better insights into the mechanisms driving adaptation and speciation. However, the evolutionary processes affecting variation at a genomic scale have not been investigated in most vertebrate lineages. Here, we present the first population genomics survey using whole genome resequencing in the green anole (Anolis carolinensis). Anoles have been intensively studied to understand mechanisms underlying adaptation and speciation. The green anole in particular is an important model to study genome evolution. We quantified how demography, recombination, and selection have led to the current genetic diversity of the green anole by using whole-genome resequencing of five genetic clusters covering the entire species range. The differentiation of green anole’s populations is consistent with a northward expansion from South Florida followed by genetic isolation and subsequent gene flow among adjacent genetic clusters. Dispersal out-of-Florida was accompanied by a drastic population bottleneck followed by a rapid population expansion. This event was accompanied by male-biased dispersal and/or selective sweeps on the X chromosome. We show that the interaction between linked selection and recombination is the main contributor to the genomic landscape of differentiation in the anole genome.

A new species of Phrynobatrachus is described from the unexplored and isolated Bibita Mountain, southwestern Ethiopia, based on morphological characters and sequences of the mitochondrial rRNA16s. The new species can be distinguished from all its congeners by a small size (SVL = 16.8 ± 0.1 mm for males, 20.3 ± 0.9 mm for females), a slender body with long legs and elongated fingers and toes, a golden coloration, a completely hidden tympanum, and a marked canthus rostralis. The phylogenetic hypothesis based on 16s sequences places the new species as sister to the species group that includes P.natalensis, although it is morphologically more similar to other dwarf Phrynobatrachus species, such as the Ethiopian P.minutus.

Made available in DSpace on 2021-06-25T11:53:54Z (GMT). No. of bitstreams: 0 Previous issue date: 2021-03-01 Deutsche Forschungsgemeinschaft Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) MfN Taxonomy Fund NYUAD NYUAD Research Institute Climate has a large impact on diversity and evolution of the world's biota. The Eocene-Oligocene transition from tropical climate to cooler, drier environments was accompanied by global species turnover. A large number of Old World lacertid lizard lineages have diversified after the Eocene-Oligocene boundary. One of the most speciose reptile genera in the arid Palearctic, Acanthodactylus, contains two sub-Saharan species with unresolved phylogenetic relationship and unknown climatic preferences. We here aim to understand how and when adaptation to arid conditions occurred in Acanthodactylus and when tropical habitats where entered. Using whole mitogenomes from fresh and archival DNA and published sequences we recovered a well-supported Acanthodactylus phylogeny and underpinned the timing of diversification with environmental niche analyses of the sub-Saharan species A. guineensis and A. boueti in comparison to all arid Acanthodactylus. We found that A. guineensis represents an old lineage that splits from a basal node in the Western clade, and A. boueti is a derived lineage and probably not its sister. Their long branches characterize them-and especially A. guineensis-as lineages that may have persisted for a long time without further diversification or have undergone multiple extinctions. Environmental niche models verified the occurrence of A. guineensis and A. boueti in hot humid environments different from the other 42 arid Acanthodactylus species. While A. guineensis probably remained in tropical habitat from periods prior to the Eocene-Oligocene boundary, A. boueti entered tropical environments independently at a later period. Our results provide an important baseline for studying adaptation and the transition from humid to arid environments in Lacertidae. New York Univ Abu Dhabi, Abu Dhabi, Saadiyat Island, U Arab Emirates Univ Estadual Paulista, Dept Biodiversidade, Inst Biociencias, BR-13506900 Rio Claro, SP, Brazil Univ Vet Med Hannover, Inst Zool, Bunteweg 17, D-30559 Hannover, Germany Univ Antilles, Sorbonne Univ, Inst Systemat Evolut Biodivers ISYEB, Museum Natl Hist Nat,CNRS,Ecole Prat Hautes Etud, CP 30,57 Rue Cuvier, F-75005 Paris, France Leibniz Inst Evolut & Biodivers Sci, Museum Nat Kunde, Invalidenstr 43, D-10115 Berlin, Germany IRD, UMR MIVEGEC, Lab Paludol & Zool Med, BP 1386, Dakar, Senegal Tech Univ Carolo Wilhelmina Braunschweig, Zool Inst, Mendelssohnstr 4, D-38106 Braunschweig, Germany Univ Estadual Paulista, Dept Biodiversidade, Inst Biociencias, BR-13506900 Rio Claro, SP, Brazil Deutsche Forschungsgemeinschaft: VE 247/11-1/MU 1760/9-1 FAPESP: 2017/26162-8 NYUAD: AD180 NYUAD Research Institute: G1205A

Taxon-specific characteristics and extrinsic climatic and geological forces may both shape population differentiation and speciation. In geographically and taxonomically focused investigations, differentiation may occur synchronously as species respond to the same external conditions. Conversely, when evolution is investigated in taxa with largely varying traits, population differentiation and speciation is complex and shaped by interactions of Earth’s template and species-specific traits. As such, it is important to characterize evolutionary histories broadly across the tree of life, especially in geographic regions that are exceptionally diverse and under pressures from human activities such as in biodiversity hotspots. Here, using whole-genome sequencing data, we characterize genomic variation in populations of six Ethiopian Highlands forest bird species separated by a lowland biogeographic barrier, the Great Rift Valley (GRV). In all six species, populations on either side of the GRV exhibited significant but varying levels of genetic differentiation. Species with lower dispersal ability generally had higher levels of population differentiation. Divergence dating indicated asynchronous population differentiation histories, with at least three distinct diversification periods. We found that demographic histories—estimated for each individual—varied by both species and population but were consistent between individuals of the same species and sampling region. We found that genomic diversity varied by half an order of magnitude across species, and that this variation could largely be explained by the harmonic mean of effective population size over the past 200,000 years. Overall, we found that even in highly dispersive species like birds, the GRV acts as a substantial biogeographic barrier.

Frogs of the genus Ptychadena that inhabit the Ethiopian highlands serve as a model system to understand biogeography, diversification, and adaptations to high elevations. Despite recent studies focusing on the systematics of this group, the taxonomy of the Ptychadena neumanni species complex remains only partially resolved, owing largely to the morphological resemblance of its members. Here, the taxonomy of this historically problematic group of frogs is revised by integrating morphological and molecular analyses on both century-old type specimens and more recently collected material. Based on these multiple lines of evidence, the P. neumanni species complex is shown to be more speciose than previously thought and four new species are described. With the aim of clarifying and stabilizing the taxonomy of the group, six species are also re-described and morphological and acoustic identification keys are provided. This study also establishes species distribution maps and reveals important differences in range size between the members of the P. neumanni complex, calling for adapted conservation measures across the Ethiopian highlands.

Transposable elements (TE) constitute one of the most variable genomic features among vertebrates, impacting genome size, structure, and composition. Despite their important role in shaping genomic diversity, they have mostly been studied in mammals, which display one of the least diverse genomes in terms of TE diversity. Recent new resources in reptilian genomics have opened a broader perspective about TE evolution in amniotes. We discuss these recent results by showing that TE diversity is high in reptiles, particularly in squamates, with strong heterogeneity in the number of TE classes retained in each lineage, even at short evolutionary scales. More research is needed to uncover the exact mechanisms that regulate TE proliferation in reptiles and to what extent these selfish elements can play a role in local adaptation or in the emergence of barriers to gene flow.

The small and conserved genomes of birds are likely a result of flight-related metabolic constraints. Recombination-driven deletions and minimal transposable element (TE) expansions have led to continually shrinking genomes during evolution of many lineages of volant birds. Despite constraints of genome size in birds, we identified multiple waves of amplification of TEs in Piciformes (woodpeckers, honeyguides, toucans, and barbets). Relative to other bird species’ genomic TE abundance (

Variation in LINE composition is one of the major determinants for the substantial size and structural differences among vertebrate genomes. In particular, the larger genomes of mammals are characterized by hundreds of thousands of copies from a single LINE clade, L1, whereas nonmammalian vertebrates possess a much greater diversity of LINEs, yet with orders of magnitude less in copy number. It has been proposed that such variation in copy number among vertebrates is due to differential effect of LINE insertions on host fitness. To investigate LINE selection, we deployed a framework of demographic modeling, coalescent simulations, and probabilistic inference against population-level whole-genome data sets for four model species: one population each of threespine stickleback, green anole, and house mouse, as well as three human populations. Specifically, we inferred a null demographic background utilizing SNP data, which was then exploited to simulate a putative null distribution of summary statistics that was compared with LINE data. Subsequently, we applied the inferred null demographic model with an additional exponential size change parameter, coupled with model selection, to test for neutrality as well as estimate the strength of either negative or positive selection. We found a robust signal for purifying selection in anole and mouse, but a lack of clear evidence for selection in stickleback and human. Overall, we demonstrated LINE insertion dynamics that are not in accordance to a mammalian versus nonmammalian dichotomy, and instead the degree of existing LINE activity together with host-specific demographic history may be the main determinants of LINE abundance.

LINE-1 (L1) retrotransposons constitute the dominant category of transposons in mammalian genomes. L1 elements are active in the vast majority of mammals, and only a few cases of L1 extinction have been documented. The only possible case of extinction in primates was suggested for South American spider monkeys. However, these previous studies were based on a single species. We revisited this question with a larger phylogenetic sample, covering all 4 genera of Atelidae and 3 species of spider monkeys. We used an enrichment method to clone recently inserted L1 elements and performed an evolutionary analysis of the sequences. We were able to identify young L1 elements in all taxa, suggesting that L1 is probably still active in all Atelidae examined. However, we also detected considerable variations in the proportion of recent elements indicating that the rate of L1 amplification varies among Atelidae by a 3-fold factor. The extent of L1 amplification in Atelidae remains overall lower than in other New World monkeys. Multiple factors can affect the amplification of L1, such as the demography of the host and the control of transposition. These factors are discussed in the context of host life history.

Transposable elements (TEs) play an important role in shaping genomic organization and structure, and may cause dramatic changes in phenotypes. Despite the genetic load they may impose on their host and their importance in microevolutionary processes such as adaptation and speciation, the number of population genetics studies focused on TEs has been rather limited so far compared to single nucleotide polymorphisms (SNPs). Here, we review the current knowledge about the dynamics of transposable elements at recent evolutionary time scales, and discuss the mechanisms that condition their abundance and frequency. We first discuss non-adaptive mechanisms such as purifying selection and the variable rates of transposition and elimination, and then focus on positive and balancing selection, to finally conclude on the potential role of TEs in causing genomic incompatibilities and eventually speciation. We also suggest possible ways to better model TEs dynamics in a population genomics context by incorporating recent advances in TEs into the rich information provided by SNPs about the demography, selection, and intrinsic properties of genomes.

New world coralsnakes of the genus Micrurus are a diverse radiation of highly venomous and brightly colored snakes that range from North Carolina to Argentina. Species in this group have played central roles in developing and testing hypotheses about the evolution of mimicry and aposematism. Despite their diversity and prominence as model systems, surprisingly little is known about species boundaries and phylogenetic relationships within Micrurus, which has substantially hindered meaningful analyses of their evolutionary history. Here we use mitochondrial genes together with thousands of nuclear genomic loci obtained via ddRADseq to study the phylogenetic relationships and population genomics of a subclade of the genus Micrurus: The M. diastema species complex. Our results indicate that prior species and species-group inferences based on morphology and color pattern have grossly misguided taxonomy, and that the M. diastema complex is not monophyletic. Based on our analyses of molecular data, we infer the phylogenetic relationships among species and populations, and provide a revised taxonomy for the group. Two non-sister species-complexes with similar color patterns are recognized, the M. distans and the M. diastema complexes, the first being basal to the monadal Micrurus and the second encompassing most North American monadal taxa. We examined all 13 species, and their respective subspecies, for a total of 24 recognized taxa in the M. diastema species complex. Our analyses suggest a reduction to 10 species, with no subspecific designations warranted, to be a more likely estimate of species diversity, namely, M. apiatus, M. browni, M. diastema, M. distans, M. ephippifer, M. fulvius, M. michoacanensis, M. oliveri, M. tener, and one undescribed species.

Evolutionary biologists have long used behavioral, ecological, and genetic data from contact zones between closely related species to study various phases of the speciation continuum. North America has several concentrations of avian contact zones, where multiple pairs of sister lineages meet, with or without hybridization. In a southern California contact zone, 2 species of woodpeckers, Nuttall’s Woodpecker (Dryobates nuttallii) and the Ladder-backed Woodpecker (D. scalaris), occasionally hybridize. We sampled these 2 species in a transect across this contact zone and included samples of their closest relative, the Downy Woodpecker (D. pubescens), to obtain large single nucleotide polymorphism panels using restriction-site associated DNA sequencing (RAD-seq). Furthermore, we used whole-genome resequencing data for 2 individuals per species to identify whether patterns of diversity inferred from RAD-seq were representative of whole-genome diversity. We found that these 3 woodpecker species are genomically distinct. Although low levels of gene flow occur between D. nuttallii and D. scalaris across the contact zone, there was no evidence for widespread genomic introgression between these 2 species. Overall patterns of genomic diversity from the RAD-seq and wholegenome datasets appear to be related to distributional range size and, by extension, are likely related to effective population sizes for each species.

Infections with viral pathogens impose considerable selective pressure on host defensive genes. Those genes at the forefront, responsible for identifying and binding exogenous molecular viral components, will carry the hallmarks of this struggle. Oligoadenylate synthetase (OAS) enzymes play a major role in the innate defense against a large number of viruses by acting as sensors of viral infections. Following their up-regulation by the interferon pathway, OASs bind viral dsRNA and then signal ribonuclease L (RNase L) to degrade RNA, shutting down viral and host protein synthesis. We have investigated the evolution of OAS1 in twenty-two Old World monkey species. We identified a total of 35 codons with the earmarks of positive selection and we performed a comprehensive analysis of their functional significance using in silico modeling of the OAS1 protein. Subdividing OAS1 into functional domains revealed intense purifying selection in the active domain but significant positive directional selection in the RNA-binding domain (RBD), the region where OAS1 binds viral dsRNA. The modeling analysis revealed a concentration of rapidly evolving residues in one region of the RBD suggestive of the sub-functionalization of different regions of the RBD. This analysis also identified several positively selected residues circumscribing the entry to the active site suggesting adaptive evasion of viral antagonism and/or selection for production of oligoadenylate of different length.

The abundance and diversity of the LINE-1 (L1) retrotransposon differ greatly among vertebrates. Mammalian genomes contain hundreds of thousands L1s that have accumulated since the origin of mammals. A single group of very similar elements is active at a time in mammals, thus a single lineage of active families has evolved in this group. In contrast, non-mammalian genomes (fish, amphibians, reptiles) harbor a large diversity of concurrently transposing families, which are all represented by very small number of recently inserted copies. Why the pattern of diversity and abundance of L1 is so different among vertebrates remains unknown. To address this issue, we performed a detailed analysis of the evolution of active L1 in 14 mammals and in 3 non-mammalian vertebrate model species. We examined the evolution of base composition and codon bias, the general structure, and the evolution of the different domains of L1 (5′UTR, ORF1, ORF2, 3′UTR). L1s differ substantially in length, base composition, and structure among vertebrates. The most variation is found in the 5′UTR, which is longer in amniotes, and in the ORF1, which tend to evolve faster in mammals. The highly divergent L1 families of lizard, frog, and fish share species-specific features suggesting that they are subjected to the same functional constraints imposed by their host. The relative conservation of the 5′UTR and ORF1 in non-mammalian vertebrates suggests that the repression of transposition by the host does not act in a sequence-specific manner and did not result in an arms race, as is observed in mammals.

The green anole (Anolis carolinensis) is a lizard widespread throughout the southeastern United States and is a model organism for the study of reproductive behavior, physiology, neural biology, and genomics. Previous phylogeographic studies of A. carolinensis using mitochondrial DNA and small numbers of nuclear loci identified conflicting and poorly supported relationships among geographically structured clades; these inconsistencies preclude confident use of A. carolinensis evolutionary history in association with morphological, physiological, or reproductive biology studies among sampling localities and necessitate increased effort to resolve evolutionary relationships among natural populations. Here, we used anchored hybrid enrichment of hundreds of genetic markers across the genome of A. carolinensis and identified five strongly supported phylogeographic groups. Using multiple analyses, we produced a fully resolved species tree, investigated relative support for each lineage across all gene trees, and identified mito‐nuclear discordance when comparing our results to previous studies. We found fixed differences in only one clade—southern Florida restricted to the Everglades region—while most polymorphisms were shared between lineages. The southern Florida group likely diverged from other populations during the Pliocene, with all other diversification during the Pleistocene. Multiple lines of support, including phylogenetic relationships, a latitudinal gradient in genetic diversity, and relatively more stable long‐term population sizes in southern phylogeographic groups, indicate that diversification in A. carolinensis occurred northward from southern Florida.

What makes a species able to colonize novel environments? This question is key to understand the dynamics of adaptive radiations and ecological niche shifts, but the mechanisms that underlie expansion into novel habitats remain poorly understood at a genomic scale. Lizards from the genusAnolisare typically tropical and the green anole(Anolis carolinensis)constitutes an exception since it expanded into temperate North America from subtropical Florida. Thus, we used the green anole as a model to investigate signatures of selection associated with colonization of a new environment, namely temperate North America. To this end, we analyzed 29 whole genome sequences, representing the entire genetic diversity of the species. We used a combination of recent methods to quantify both positive and balancing selection in northern populations, including FSToutlier methods, machine learning and ancestral recombination graphs. We naively scanned for genes of interest and assessed the overlap between multiple tests. Strikingly, we identified many genes involved in behavior, suggesting that the recent successful colonization of northern environments may have been linked to behavioral shifts as well as physiological adaptation. These results were robust to recombination, gene length and clustering. Using a candidate genes strategy, we determined that genes involved in response to cold or behavior displayed more frequently signals of selection, while controlling for local recombination rate and gene length. In addition, we found signatures of balancing selection at immune genes in all investigated genetic groups, but also at genes involved in neuronal and anatomical development in Florida.

Gaining a better understanding on how selection and neutral processes affect genomic diversity is essential to gain better insights into the mechanisms driving adaptation and speciation. However, the evolutionary processes affecting variation at a genomic scale have not been investigated in most vertebrate lineages. Previous studies have been limited to a small number of model species, mostly mammals, and no studies have investigated genomic variation in non avian reptiles. Here we present the first population genomics survey using whole genome re sequencing in the green anole (Anolis carolinensis). This species has emerged as a model for the study of genomic evolution in squamates. We quantified how demography, recombination and selection have led to the current genetic diversity of the green anole by using whole-genome resequencing of five genetic clusters covering the entire species range. The differentiation of green anole’s populations is consistent with a northward expansion from South Florida followed by genetic isolation and subsequent gene flow among adjacent genetic clusters. Dispersal out-of-Florida was accompanied by a drastic population bottleneck followed by a rapid population expansion. This event was accompanied by male-biased dispersal and/or selective sweeps on the X chromosome. We show that the combined effect of background selection and recombination rates is the main contributor to the genomic landscape of differentiation in the anole genome. We further demonstrate that recombination rates are positively correlated with GC content at third codon position (GC3) and confirm the importance of biased gene conversion in shaping genome wide patterns of diversity in reptiles.

The oligoadenylate synthetase 1 (OAS1) enzyme acts as an innate sensor of viral infection and plays a major role in the defense against a wide diversity of viruses. Polymorphisms at OAS1 have been shown to correlate with differential susceptibility to several infections of great public health significance, including hepatitis C virus, SARS coronavirus, and West Nile virus. Population genetics analyses in hominoids have revealed interesting evolutionary patterns. In Central African chimpanzee, OAS1 has evolved under long-term balancing selection, resulting in the persistence of polymorphisms since the origin of hominoids, whereas human populations have acquired and retained OAS1 alleles from Neanderthal and Denisovan origin. We decided to further investigate the evolution of OAS1 in primates by characterizing intra-specific variation in four species commonly used as models in infectious disease research: the rhesus macaque, the cynomolgus macaque, the olive baboon, and the Guinea baboon. In baboons, OAS1 harbors a very low level of variation. In contrast, OAS1 in macaques exhibits a level of polymorphism far greater than the genomic average, which is consistent with the action of balancing selection. The region of the enzyme that directly interacts with viral RNA, the RNA-binding domain, contains a number of polymorphisms likely to affect the RNA-binding affinity of OAS1. This strongly suggests that pathogen-driven balancing selection acting on the RNA-binding domain of OAS1 is maintaining variation at this locus. Interestingly, we found that a number of polymorphisms involved in RNA-binding were shared between macaques and chimpanzees. This represents an unusual case of convergent polymorphism.

The frog genus Leptopelis is composed of ~50 species that occur across sub-Saharan Africa. The majority of these frogs are typically arboreal; however, a few species have evolved a fossorial lifestyle. Most species inhabit lowland forests, but a few species have adapted to high elevations. Five species of Leptopelis occupy the Ethiopian highlands and provide a good opportunity to study the evolutionary transition from an arboreal to a fossorial lifestyle, as well as the diversification in this biodiversity hot spot. We sequenced 14 nuclear and three mitochondrial genes, and generated thousands of SNPs from ddRAD sequencing to study the evolutionary relationships of Ethiopian Leptopelis. The five species of highland Leptopelis form a monophyletic group, which diversified during the late Miocene and Pliocene. We found strong population structure in the fossorial species L. gramineus, with levels of genetic differentiation between populations similar to those found between arboreal species. This could indicate that L. gramineus is a complex of cryptic species. We propose that after the original colonization of the Ethiopian highlands by the ancestor of the L. gramineus group, episodes of vicariance fragmented the ancestral populations of this group. We also report the re-evolution of arboreality in L. susanae, which evolved from a fossorial ancestor, a rare ecological switch in frogs that had previously been reported only once.

Chloride intracellular channel proteins (CLICs) are multi-functional proteins that are expressed in various cell types and differ in their subcellular location. Two CLIC homologs, EXL-1 (excretory canal abnormal like-1) and EXC-4 (excretory canal abnormal- 4), are encoded in the Caenorhabditis elegans genome, providing an excellent model to study the functional diversification of CLIC proteins. EXC-4 functions in excretory canal formation during normal animal development. However, to date, the physiological function of EXL-1 remains largely unknown. In this study, we demonstrate that EXL-1 responds specifically to heat stress and translocates from the cytoplasm to the nucleus in intestinal cells and body wall muscle cells under heat shock. In contrast, we do not observe EXC-4 nuclear translocation under heat shock. Full protein sequence analysis shows that EXL-1 bears a non-classic nuclear localization signal (NLS) that EXC-4 is lacking. All mammalian CLIC members have a nuclear localization signal, with the exception of CLIC3. Our phylogenetic analysis of the CLIC gene families across various animal species demonstrates that the duplication of CLICs in protostomes and deuterostomes occurred independently and that the NLS was subsequently lost in amniotes and nematodes, suggesting convergent evolution. We also observe that EXL-1 nuclear translocation occurs in a timely ordered manner in the intestine, from posterior to anterior regions. Finally, we find that exl-1 loss of function mutants are more susceptible to heat stress than wild-type animals, demonstrating functional relevance of the nuclear translocation. This research provides the first link between CLICs and environmental heat stress. We propose that C. elegans CLICs evolved to achieve different physiological functions through subcellular localization change and spatial separation in response to external or internal signals.

Vertebrate genomes differ considerably in size and structure. Among the features that show the most variation is the abundance of Long Interspersed Nuclear Elements (LINEs). Mammalian genomes contain 100,000s LINEs that belong to a single clade, L1, and in most species a single family is usually active at a time. In contrast, non-mammalian vertebrates (fish, amphibians and reptiles) contain multiple active families, belonging to several clades, but each of them is represented by a small number of recently inserted copies. It is unclear why vertebrate genomes harbor such drastic differences in LINE composition. To address this issue, we conducted whole genome resequencing to investigate the population genomics of LINEs across 13 genomes of the lizard Anolis carolinensis sampled from two geographically and genetically distinct populations in the Eastern Florida and the Gulf Atlantic regions of the United States. We used the Mobile Element Locator Tool to identify and genotype polymorphic insertions from five major clades of LINEs (CR1, L1, L2, RTE and R4) and the 41 subfamilies that constitute them. Across these groups we found large variation in the frequency of polymorphic insertions and the observed length distributions of these insertions, suggesting these groups vary in their activity and how frequently they successfully generate full-length, potentially active copies. Though we found an abundance of polymorphic insertions (over 45,000) most of these were observed at low frequencies and typically appeared as singletons. Site frequency spectra for most LINEs showed a significant shift toward low frequency alleles compared to the spectra observed for total genomic single nucleotide polymorphisms. Using Tajima’s D, FST and the mean number of pairwise differences in LINE insertion polymorphisms, we found evidence that negative selection is acting on LINE families in a length-dependent manner, its effects being stronger in the larger Eastern Florida population. Our results suggest that a large effective population size and negative selection limit the expansion of polymorphic LINE insertions across these populations and that the probability of LINE polymorphisms reaching fixation is extremely low.

The genus Papio (the baboons) is one of the most widespread and ecologically successful primate genera. Baboons are found across sub-Saharan Africa, only avoiding the tropical humid forests of Central Africa, and in the southern portion of the Arabian Peninsula. Historically, six distinct forms of baboons have been recognized based on morphology (Frost et al. 2003; Jolly 1993): the chacma baboon (P. ursinus) found in the Southern part of the African continent, the yellow baboon (P. cynocephalus) from Eastern Africa, the olive baboon (P. anubis) which distribution extends from western Kenya and south Ethiopia to Guinea and Southern Mali, the Guinea baboon (P. papio) which is limited to Senegal and western Guinea, the hamadryas baboon (P. hamadryas) which inhabits semi-desert habitats in Ethiopia, Eritrea and the Arabian peninsula and the Kinda baboon (P. kindae) from Zambia. Depending on the authors, these forms have been considered either sub-species of Papio hamadryas or separate species, but there is currently no consensus on the taxonomic status of the different baboon morphotypes (Frost et al. 2003; Jolly 1993). Although these six forms are morphologically and geographically distinct, they do hybridize in nature showing little reproductive isolation (Alberts and Altmann 2001; Bergman et al. 2008; Jolly 1993; Jolly et al. 2011; Tung et al. 2008). Mitochondrial analyses suggest that baboons diversified during the last 2 million years and that their differentiation could have been driven by glacial and inter-glacial cycles during the late Pliocene and Pleistocene (Newman et al. 2004; Zinner et al. 2009). Because the geography and time scale of the diversification of baboons mirrors the diversification of the genus Homo, it has been proposed that baboons constitute a useful model to understand the evolution of the human lineage over the last 2 million years (Jolly 2001). In addition, the past and current hybridization between baboon morphotypes could help elucidate the genetic exchanges that have occurred between ancestral human populations and Neandertals (Green et al. 2010; Prufer et al. 2014; Sankararaman et al. 2014; Sankararaman et al. 2012) or Denisovans (Reich et al. 2010). Finally, the transition from savanna-dwelling baboons to the multi-level social structure of the hamadryas baboon constitute a useful model to understand the evolution of hominin social behavior (Swedell and Plummer 2012). The evolutionary relationships between the different baboon forms have long been a subject of controversy. Based on morphological similarity it has been proposed that the olive and chacma baboons are sister taxa (Ellerman et al. 1953; Kingdon 1997). Other authors have suggested that Guinea and hamadryas baboons are sister-taxa due to their phenotypic and behavioral similarity and that the yellow baboon branches with the chacma and olive baboons (Hill 1967). Based on socio-ecological arguments, it was proposed that the hamadryas baboon is sister to all other baboons (Buettner-Janusch 1966; Thorington and Groves 1970) whereas biochemical analyses suggested that it was the Guinea baboon that was the sister to all other forms (Williams-Blangero et al. 1990). More recently, a north/south model was proposed (Jolly 1993) with the yellow and chacma baboons as sister taxa and a northern monophyletic group composed of the olive, hamadryas and Guinea baboons. In the past decade, several groups have attempted to resolve the evolutionary relationships among baboons using mitochondrial DNA sequences (Newman et al. 2004; Sithaldeen et al. 2009; Wildman et al. 2004; Zinner et al. 2009; Zinner et al. 2013). All these studies support the existence of two clades (figure 1): a southern clade consisting of the chacma baboon, Kinda baboon and yellow baboons from Zambia, Malawi and southern Tanzania and a northern clade consisting of the hamadryas baboon, Guinea baboon, olive baboon and yellow baboons from Kenya and northern Tanzania. Depending on the study, the split between the northern and southern mitochondrial lineages occurred between 1.79 and 2.09 million years (my) ago. Within the northern clade, there is a clear break dated around 1.34 – 1.89 my between western baboons (Guinea baboon and olive baboons from Nigeria, Cameroon and Ivory Coast) and eastern baboons (hamadryas, olive baboons from Kenya, Eritrea and Ethiopia, and yellow baboons from Kenya and Tanzania). In the southern clade (which might be paraphyletic based on complete mitochondrial genome analyses; (Zinner et al. 2013)), there is a distinct south/north split around 1.80 my between south chacma (South Africa and coastal Namibia) and a group composed of Kinda, northern chacma (Zimbabwe, south Zambia, Mozambique and eastern Namibia) and southern yellow baboons. Figure 1 Phylogeny of mitochondrial sequences. We used a representative subset of the sequences used by Zinner et al. (2009) and we named the clades following the nomenclature proposed by these authors. The samples used in the present study are indicated with ... The different clades and sub-clades recovered by analysis of the mitochondrial genome have clearly defined geographic distributions, possibly reflecting ancient fragmentation and speciation events in the late Pliocene and Pleistocene (Zinner et al. 2011; Zinner et al. 2009). However, the discordance between mitochondrial lineages and the distribution of morphotypes suggests that introgressive hybridization has occurred frequently (Keller et al. 2010; Newman et al. 2004; Wildman et al. 2004; Zinner et al. 2011; Zinner et al. 2009). For instance, southern and northern yellow baboons carry two highly divergent mitochondrial lineages while western and eastern olive baboons carry mitochondrion that diverged approximately 1.4 to 1.9 my (Zinner et al. 2011; Zinner et al. 2009). In contrast, northern yellow, eastern olive and hamadryas baboons share a 0.6 my old mitochondrial lineage, although they have maintained their morphological distinctiveness (Zinner et al. 2011; Zinner et al. 2009). This pattern is best explained by extensive and asymmetric gene flow. The proposed model, called “nuclear swamping”, posits that hybridization followed by repeated asymmetric backcrossing between hybrid females and males of one of the parental morphotypes will result in individuals with the mitochondrion of one form and the nuclear genome of another form. For instance, when olive baboons expanded their distribution into Ethiopian hamadryas territory (Wildman et al. 2004), hybrid females mated preferentially with olive males while the hybrid males had a lower reproductive success (Phillips-Conroy and Jolly 2004; Wildman et al. 2004). Subsequent and numerous generations of backcrossing resulted in baboons that are morphologically olive-like, but carry a hamadryas mitochondrion. The extensive discordance between mitochondrial lineages and morphology indicates that the evolution of baboons has been extremely complex and that mitochondrial analyses are of limited use to resolve the evolutionary relationships among baboons as well as the origin of the modern morphotypes. To decipher the evolutionary relationships among baboons we decided to perform an analysis using neutral nuclear polymorphisms. We analyzed 12 non-coding autosomal segments, one X-linked region and 18 polymorphic transposable element insertions in a sample of 45 baboons representing 5 of the 6 recognized morphotypes.

Vertebrate genomes differ considerably in size and structure. Among the features that show the most variation is the abundance of Long Interspersed Nuclear Elements (LINEs). Mammalian genomes contain 100,000s LINEs that belong to a single clade, L1, and in most species a single family is usually active at a time. In contrast, non-mammalian vertebrates (fish, amphibians and reptiles) contain multiple active families, belonging to several clades, but each of them is represented by a small number of recently inserted copies. It is unclear why vertebrate genomes harbor such drastic differences in LINE composition. To address this issue, we conducted whole genome resequencing to investigate the population genomics of LINEs across 13 genomes of the lizard Anolis carolinensis sampled from two geographically and genetically distinct populations in the Eastern Florida and the Gulf Atlantic regions of the United States. We used the Mobile Element Locator Tool to identify and genotype polymorphic insertions from five major clades of LINEs (CR1, L1, L2, RTE and R4) and the 41 subfamilies that constitute them. Across these groups we found large variation in the frequency of polymorphic insertions and the observed length distributions of these insertions, suggesting these groups vary in their activity and how frequently they successfully generate full-length, potentially active copies. Though we found an abundance of polymorphic insertions (over 45,000) most of these were observed at low frequencies and typically appeared as singletons. Site frequency spectra for most LINEs showed a significant shift toward low frequency alleles compared to the spectra observed for total genomic single nucleotide polymorphisms. Using Tajima’s D, FST and the mean number of pairwise differences in LINE insertion polymorphisms, we found evidence that negative selection is acting on LINE families in a length-dependent manner, its effects being stronger in the larger Eastern Florida population. Our results suggest that a large effective population size and negative selection limit the expansion of polymorphic LINE insertions across these populations and that the probability of LINE polymorphisms reaching fixation is extremely low.

The evolution of the amniotic egg was one of the great evolutionary innovations in the history of life, freeing vertebrates from an obligatory connection to water and thus permitting the conquest of terrestrial environments. Among amniotes, genome sequences are available for mammals and birds, but not for non-avian reptiles. Here we report the genome sequence of the North American green anole lizard, Anolis carolinensis. We find that A. carolinensis microchromosomes are highly syntenic with chicken microchromosomes, yet do not exhibit the high GC and low repeat content that are characteristic of avian microchromosomes. Also, A. carolinensis mobile elements are very young and diverse—more so than in any other sequenced amniote genome. The GC content of this lizard genome is also unusual in its homogeneity, unlike the regionally variable GC content found in mammals and birds. We describe and assign sequence to the previously unknown A. carolinensis X chromosome. Comparative gene analysis shows that amniote egg proteins have evolved significantly more rapidly than other proteins. An anole phylogeny resolves basal branches to illuminate the history of their repeated adaptive radiations., National Science Foundation (U.S.) (NSF grant DEB-0920892), National Science Foundation (U.S.) (NSF grant DEB-0844624), National Human Genome Research Institute (U.S.)

The diversity and abundance of non-long terminal repeat (LTR) retrotransposons (nLTR-RT) differ drastically among vertebrate genomes. At one extreme, the genome of placental mammals is littered with hundreds of thousands of copies resulting from the activity of a single clade of nLTR-RT, the L1 clade. In contrast, fish genomes contain a much more diverse repertoire of nLTR-RT, represented by numerous active clades and families. Yet, the number of nLTR-RT copies in teleostean fish is two orders of magnitude smaller than in mammals. The vast majority of insertions appear to be very recent, suggesting that nLTR-RT do not accumulate in fish genomes. This pattern had previously been explained by a high rate of turnover, in which the insertion of new elements is offset by the selective loss of deleterious inserts. The turnover model was proposed because of the similarity between fish and Drosophila genomes with regard to their nLTR-RT profile. However, it is unclear if this model applies to fish. In fact, a previous study performed on the puffer fish suggested that transposable element insertions behave as neutral alleles. Here we examined the dynamics of amplification of nLTR-RT in the three-spine stickleback (Gasterosteus aculeatus). In this species, the vast majority of nLTR-RT insertions are relatively young, as suggested by their low level of divergence. Contrary to expectations, a majority of these insertions are fixed in lake and oceanic populations; thus, nLTR-RT do indeed accumulate in the genome of their fish host. This is not to say that nLTR-RTs are fully neutral, as the lack of fixed long elements in this genome suggests a deleterious effect related to their length. This analysis does not support the turnover model and strongly suggests that a much higher rate of DNA loss in fish than in mammals is responsible for the relatively small number of nLTR-RT copies and for the scarcity of ancient elements in fish genomes. We further demonstrate that nLTR-RT decay in fish occurs mostly through large deletions and not by the accumulation of small deletions.

DNA transposons have considerably affected the size and structure of eukaryotic genomes and have been an important source of evolutionary novelties. In vertebrates, DNA transposons are discontinuously distributed due to the frequent extinction and recolonization of these genomes by active elements. We performed a detailed analysis of the DNA transposons in the genome of the lizard Anolis carolinensis, the first non-avian reptile to have its genome sequenced. Elements belonging to six of the previously recognized superfamilies of elements (hAT, Tc1/Mariner, Helitron, PIF/Harbinger, Polinton/Maverick, and Chapaev) were identified. However, only four (hAT, Tc1/Mariner, Helitron, and Chapaev) of these superfamilies have successfully amplified in the anole genome, producing 67 distinct families. The majority (57/67) are nonautonomous and demonstrate an extraordinary diversity of structure, resulting from frequent interelement recombination and incorporation of extraneous DNA sequences. The age distribution of transposon families differs among superfamilies and reveals different dynamics of amplification. Chapaev is the only superfamily to be extinct and is represented only by old copies. The hAT, Tc1/Mariner, and Helitron superfamilies show different pattern of amplification, yet they are predominantly represented by young families, whereas divergent families are exceedingly rare. Although it is likely that some elements, in particular long ones, are subjected to purifying selection and do not reach fixation, the majority of families are neutral and accumulate in the anole genome in large numbers. We propose that the scarcity of old copies in the anole genome results from the rapid decay of elements, caused by a high rate of DNA loss.

In animals, the mode of transmission of transposable elements is generally vertical. However, recent studies have suggested that lateral transfer has occurred repeatedly in several distantly related tetrapod lineages, including mammals. Using transposons extracted from the genome of the lizard Anolis carolinensis as probes, we identified four novel families of hAT transposons that share extremely high similarity with elements in other genomes including several mammalian lineages (primates, chiropters, marsupials), one amphibian and one flatworm, the planarian Schmidtea mediterranea. The discontinuous phylogenetic distribution of these hAT families, coupled with very low synonymous divergence between species, strongly suggests that these elements were laterally transferred to these different species. This indicates that the horizontal transfer of DNA transposons in vertebrates might be more common than previously thought. Yet, it appears that the transfer of DNA transposons did not occur randomly as the same genomes have been invaded independently by different, unrelated transposon families whereas others seem to be immune to lateral transfer. This suggests that some organisms might be intrinsically more vulnerable to DNA transposon lateral transfer, possibly because of a weakened defense against transposons or because they have developed mechanisms to tolerate their impact.

The genome of the lizard Anolis carolinensis (the green anole) is the first nonavian reptilian genome sequenced. It offers a unique opportunity to comparatively examine the evolution of amniote genomes. We analyzed the abundance and diversity of non-LTR (long terminal repeat) retrotransposons in the anole using the Genome Parsing Suite. We found that the anole genome contains an extraordinary diversity of elements. We identified 46 families of elements representing five clades (L1, L2, CR1, RTE, and R4). Within most families, elements are very similar to each other suggesting that they have been inserted recently. The rarity of old elements suggests a high rate of turnover, the insertion of new elements being offset by the loss of element-containing loci. Consequently, non-LTR retrotransposons accumulate in the anole at a low rate and are found in low copy number. This pattern of diversity shows some striking similarity with the genome of teleostean fish but contrasts greatly with the low diversity and high copy number of mammalian L1 elements, suggesting a fundamental difference in the way mammals and nonmammalian vertebrates interact with their genomic parasites. The scarcity of divergent elements in anoles suggests that insertions have a deleterious effect and are eliminated by natural selection. We propose that the low abundance of non-LTR retrotransposons in the anole is related directly or indirectly to a higher rate of ectopic recombination in the anole relative to mammals.

LINE-1 (L1) retrotransposons constitute the most successful family of retroelements in mammals and account for as much as 20% of mammalian DNA. L1 elements can be found in all genomic regions but they are far more abundant in AT-rich, gene-poor, and low-recombining regions of the genome. In addition, the sex chromosomes and some genes seem disproportionately enriched in L1 elements. Insertion bias and selective processes can both account for this biased distribution of L1 elements. L1 elements do not appear to insert randomly in the genome and this insertion bias can at least partially explain the genomic distribution of L1. The contrasted distribution of L1 and Alu elements suggests that postinsertional processes play a major role in shaping L1 distribution. The most likely mechanism is the loss of recently integrated L1 elements that are deleterious (negative selection) either because of disruption of gene function or their ability to mediate ectopic recombination. By comparison, the retention of L1 elements because of some positive effect is limited to a small fraction of the genome. Understanding the respective importance of insertion bias and selection will require a better knowledge of insertion mechanisms and the dynamics of L1 inserts in populations.

Background/Aims: The L1 retrotransposable element family is the most successful self-replicating genomic parasite of the human genome. L1 elements drive replication of Alu elements, and both have had far-reaching impacts on the human genome. We use L1 and Alu insertion polymorphisms to analyze human population structure. Methods: We genotyped 75 recent, polymorphic L1 insertions in 317 individuals from 21 populations in sub-Saharan Africa, East Asia, Europe and the Indian subcontinent. This is the first sample of L1 loci large enough to support detailed population genetic inference. We analyzed these data in parallel with a set of 100 polymorphic Alu insertion loci previously genotyped in the same individuals. Results and Conclusion: The data sets yield congruent results that support the recent African origin model of human ancestry. A genetic clustering algorithm detects clusters of individuals corresponding to continental regions. The number of loci sampled is critical: with fewer than 50 typical loci, structure cannot be reliably discerned in these populations. The inclusion of geographically intermediate populations (from India) reduces the distinctness of clustering. Our results indicate that human genetic variation is neither perfectly correlated with geographic distance (purely clinal) nor independent of distance (purely clustered), but a combination of both: stepped clinal.