Nicolas Perrin

• University of Lausanne

Sex chromosomes constantly exist in a dynamic state of evolution: rapid turnover and change of heterogametic sex during homomorphic state, and often stepping out to a heteromorphic state followed by chromosomal decaying. However, the forces driving these different trajectories of sex chromosome evolution are still unclear. The Japanese frog Glandir...

Reproductive isolation is instrumental to the formation of new species (speciation), but it remains largely enigmatic how many incompatibilities are required to prevent hybridization and where they lie across the genome. By studying patterns of admixture in amphibian hybrid zones, we found that reproductive isolation is initiated by numerous small-...

Until recently, the field of sex chromosome evolution has been dominated by the canonical unidirectional scenario, first developed by Muller in 1918. This model postulates that sex chromosomes emerge from autosomes by acquiring a sex-determining locus. Recombination reduction then expands outwards from this locus, to maintain its linkage with sexua...

We report the discovery of a population of the exotic North African Water Frog Pelophylax saharicus around the Etang de Berre, on the Mediterranean coast of France, about 25 km north-west of Marseille. The animals had been originally identified as P. perezi or P. kl. grafi by a combination of acoustic and morphological characters and their true ide...

Sex-antagonistic (SA) genes are widely considered to be crucial players in the evolution of sex chromosomes, being instrumental in the arrest of recombination and degeneration of Y chromosomes, as well as important drivers of sex-chromosome turnovers. To test such claims, one needs to focus on systems at the early stages of differentiation, ideally...

Hybridogenesis is a reproductive tool for sexual parasitism. Hybridogenetic hybrids use gametes from their sexual host for their own reproduction, but sexual species gain no benefit from such matings as their genome is later eliminated. Here, we examine the presence of sexual parasitism in water frogs through crossing experiments and genome-wide da...

Sex chromosomes are classically predicted to stop recombining in the heterogametic sex, thereby enforcing linkage between sex-determining (SD) and sex-antagonistic (SA) genes. With the same rationale, a pre-existing sex asymmetry in recombination is expected to affect the evolution of heterogamety, e. g. a low rate of male recombination might favor...

Sex chromosomes of eutherian mammals are highly different in size and gene content, and share only a small region of homology (pseudoautosomal region, PAR). They are thought to have evolved through an addition-attrition cycle involving the addition of autosomal segments to sex chromosomes and their subsequent differentiation. The events that drive...

The growing interest in the lability of sex determination in non-model vertebrates such as amphibians and fishes has revealed high rates of sex chromosome turnovers among closely related species of the same clade. Can such lineages hybridize and admix with different sex-determining systems, or could the changes have precipitated their speciation? W...

Sex chromosomes of eutherian mammals are highly different in size and gene content, and share only a small region of homology (pseudoautosomal region, PAR). They are thought to have evolved through an addition-attrition cycle involving the addition of autosomal segments to sex chromosomes and their subsequent differentiation. The events that drive...

Because it is indicative of reproductive isolation, the amount of genetic introgression across secondary contact zones is increasingly considered in species delimitation. However, patterns of admixture at range margins can be skewed by the regional dynamics of hybrid zones. In this context, we posit an important role for phylogeographic history: hy...

Molecular ecologists often rely on phylogenetic evidence for assessing the species-level systematics of newly-discovered lineages. Alternatively, the extent of introgression at phylogeographic transitions can provide a more direct test to assign candidate taxa into subspecies or species categories. Here we compared phylogenetic versus hybrid zone a...

Subdivided Pleistocene glacial refugia, best known as “refugia within refugia”, provided opportunities for diverging populations to evolve into incipient species and/or to hybridize and merge following range shifts tracking the climatic fluctuations, potentially promoting extensive cytonuclear discordances and “ghost” mtDNA lineages. Here we tested...

The canonical model of sex‐chromosome evolution assigns a key role to sexually antagonistic (SA) genes on the arrest of recombination and ensuing degeneration of Y chromosomes. This assumption cannot be tested in organisms with highly differentiated sex chromosomes, such as mammals or birds, owing to the lack of polymorphism. Fixation of SA alleles...

Sex chromosomes in vertebrates range from highly heteromorphic (as in most birds and mammals) to strictly homomorphic (as in many fishes, amphibians, and non‐avian reptiles). Reasons for these contrasted evolutionary trajectories remain unclear, but species such as common frogs with polymorphism in the extent of sex‐chromosome differentiation may p...

Cryptic phylogeographic diversifications are unique models to examine the role of phylogenetic divergence on the evolution of reproductive isolation, without extrinsic factors such as ecology. Yet, to date very few comparative studies were attempted within such radiations. Here, we characterize a new speciation continuum in a group of widespread Eu...

The canonical model of sex-chromosome evolution assigns a key role to sexually antagonistic (SA) genes on the arrest of recombination and ensuing degeneration of Y chromosomes. This assumption cannot be tested in organisms with highly differentiated sex chromosomes, such as mammals or birds, owing to the lack of polymorphism. Fixation of SA alleles...

Deleterious mutations accumulating on non-recombining Y chromosomes can drive XY to XY turnovers, as they allow to replace the old mutation-loaded Y by a new mutation-free one. The same process is thought to prevent XY to ZW turnovers, because the latter requires fixation of the ancestral Y, assuming dominance of the emergent feminizing mutation. U...

Comparative molecular studies emphasized a new biogeographic paradigm for the terrestrial fauna of North Africa, one of the last uncharted ecoregions of the Western Palearctic: two independent east-west divisions across the Maghreb. Through a comprehensive phylogeography, we assessed how this model suits the genetic diversification documented for t...

Alloparapatric species meeting in secondary contact zones are evolutionary witnesses to how reproductive isolation progresses over time and space. Western Palearctic tree frogs (Hyla) are phenotypically similar and all the species pairs tested can hybridize and eventually admix at range margins. All except one. The early-diverged Hyla meridionalis...

X and Y chromosomes can diverge when rearrangements block recombination between them. Here we present the first genomic view of a reciprocal translocation that causes two physically unconnected pairs of chromosomes to be coinherited as sex chromosomes. In a population of the common frog (Rana temporaria), both pairs of X and Y chromosomes show exte...

Deleterious mutations accumulating on non-recombining Y chromosomes can drive XY to XY turnovers, but are thought to prevent XY to ZW turnovers, because the latter require fixation of the ancestral Y. Using individual-based simulations, we explored whether and how a dominant W allele can spread in a young XY system that gradually accumulates delete...

The canonical model of sex-chromosome evolution predicts that, as recombination is suppressed along sex chromosomes, gametologs will progressively differentiate, eventually becoming heteromorphic. However, there are numerous examples of homomorphic sex chromosomes across the tree of life. This homomorphy has been suggested to result from frequent s...

Background: The patterns of gene expression on highly differentiated sex chromosomes differ drastically from those on autosomes, due to sex-specific patterns of selection and inheritance. As a result, X chromosomes are often enriched in female-biased genes (feminization) and Z chromosomes in male-biased genes (masculinization). However, it is not...

Sex-biased genes are central to the study of sexual selection, sexual antagonism, and sex chromosome evolution. We describe a comprehensive de novo assembled transcriptome in the common frog Rana temporaria based on five developmental stages and three adult tissues from both sexes, obtained from a population with karyotypically homomorphic but gene...

The recent advances of new genomic technologies has enabled to identify and characterize sex chromosomes in an increasing number of non‐model species, revealing that many plants and animals undergo frequent sex chromosome turnovers. What evolutionary forces drive these turnovers remains poorly understood, but it was recently proposed that drift mig...

Background: Debated aspects in speciation research concern the amount of gene flow between incipient species under secondary contact and the modes by which post-zygotic isolation accumulates. Secondary contact zones of allopatric lineages, involving varying levels of divergence, provide natural settings for comparative studies, for which the Aegean...

Dobzhansky‐Muller (DM) incompatibilities involving sex chromosomes have been proposed to account for Haldane's rule (lowered fitness among hybrid offspring of the heterogametic sex) as well as Darwin's corollary (asymmetric fitness costs with respect to the direction of the cross). We performed simulation studies of a hybrid zone to investigate the...

Suppl. Info of Open Access Paper "Profound genetic divergence and asymmetric parental genome contributions as hallmarks of hybrid speciation in polyploid toads".

The evolutionary causes and consequences of allopolyploidization, an exceptional pathway to instant hybrid speciation, are poorly investigated in animals. In particular, when and why hybrid polyploids versus diploids are produced, and constraints on sources of paternal and maternal ancestors, remain underexplored. Using the Palearctic green toad ra...

According to the canonical model of sex-chromosome evolution, the degeneration of Y or W chromosomes (as observed in mammals and birds respectively) results from an arrest of recombination in the heterogametic sex, driven by the fixation of sexually antagonistic mutations. However, sex chromosomes have remained homomorphic in many lineages of fishe...

The canonical model of sex-chromosome evolution predicts that sex-antagonistic (SA) genes play an instrumental role in the arrest of XY recombination and ensuing Y-chromosome degeneration. Although this model might account for the highly differentiated sex chromosomes of birds and mammals, it does not fit the situation of many lineages of fish, amp...

Sex-determination mechanisms vary both within and among populations of common frogs, opening opportunities to investigate the molecular pathways and ultimate causes shaping their evolution. We investigated the association between sex-chromosome differentiation (as assayed from microsatellites) and polymorphism at the candidate sex-determining gene...

Human introductions of exotic amphibians can have catastrophic effects on native species. However, they usually remain unnoticed without genetic tools when species are difficult to distinguish morphologically. In Western Europe, pool frogs (Pelophylax sp.) make a worrisome case: recent genetic data showed the presence of Italian (Pelophylax bergeri...

Artificial stocking practices are widely used by resource managers worldwide, in order to sustain fish populations exploited by both recreational and commercial activities, but their benefits are controversial. Former practices involved exotic strains, although current programs rather consider artificial breeding of local fishes (supportive breedin...

Background In contrast to the Western Palearctic and Nearctic biogeographic regions, the phylogeography of Eastern-Palearctic terrestrial vertebrates has received relatively little attention. In East Asia, tectonic events, along with Pleistocene climatic conditions, likely affected species distribution and diversity, especially through their impact...

We demonstrate a genotyping-by-sequencing approach to identify homomorphic sex chromosomes and their homolog in a distantly related reference genome, based on non-invasive sampling of wild-caught individuals, in the moor frog Rana arvalis. Double-digest RADseq libraries were generated using buccal swabs from 30 males and 21 females from the same po...

Oestrogenic hormones are a major environmental threat to aquatic wildlife. Here we report on chronic toxic effects of larval exposure to the naturally excreted oestrogen 17β-estradiol (E2), in the European tree frog (Hyla arborea), by means of an experimental setting and long-term monitoring. Larval survival was significantly lower in treated tanks...

Sex-determining factors are usually assumed to be either genetic or environmental. The present paper aims at drawing attention to the potential contribution of developmental noise, an important but often-neglected component of phenotypic variance. Mutual inhibitions between male and female pathways make sex a bistable equilibrium, such that random...

Genetic pollution through introgressive hybridization of local species by exotic relatives is a major, yet neglected aspect of biological invasions, particularly in amphibians where human introductions are frequent. In Western Switzerland, crested newts make an interesting case: the Italian species Triturus carnifex was introduced at least a centur...

Appendix S1. Text S1. Seven scaffolds from the draft genome of Rana temporaria, containing, respectively, the five Dmrt1 exons, Kank1 intron 1, and Dmrt3 intron 1. Text S2. Transcript sequences of R. temporaria Dmrt1 in five froglets. Text S3. Concatenated sequences of three Dmrt1 polymorphic sites for 26 individuals from Ammarnäs and Tvedöra.

Appendix S2 Table S1. Primer pairs and PCR conditions for amplifying Dmrt1 transcript and individual exons. Table S2. Primers pairs and PCR conditions for genotyping. Table S3. Between‐sex F ST values in Ammarnäs and Tvedöra.

Hotspots of intraspecific genetic diversity, which are of primary importance for the conservation of species, have been associated to glacial refugia, i.e. areas where species survived the Quaternary climatic oscillations. However, the proximate mechanisms generating these hotspots remain an open issue. Hotspots may reflect the long-term persistenc...

Patterns of sex-chromosome differentiation and gonadal development have been shown to vary among populations of Rana temporaria along a latitudinal transect in Sweden. Frogs from the northern-boreal population of Ammarnäs displayed well-differentiated X and Y haplotypes, early gonadal differentiation, and a perfect match between phenotypic and geno...

The patterns of sex determination and sex differentiation have been shown to differ among geographic populations of common frogs. Notably, the association between phenotypic sex and linkage group 2 (LG2) has been found to be perfect in a northern Swedish population, but weak and variable among families in a southern one. By analyzing these populati...

Reproductive isolation is crucial for the process of speciation to progress. Sex chromosomes have been assigned a key role in driving reproductive isolation but empirical evidence from natural population processes has been restricted to organisms with degenerated sex chromosomes such as mammals and birds. Here we report restricted introgression at...

Identifying homology between sex chromosomes of different species is essential to understanding the evolution of sex determination. Here, we show that the identity of a homomorphic sex chromosome pair can be established using a linkage map, without information on offspring sex. By comparing sex-specific maps of the European tree frog Hyla arborea,...

Empirical studies on the relative roles of occasional XY recombination versus sex-chromosome turnover in preventing sex-chromosome differentiation may shed light on the evolutionary forces acting on sex-determination systems. Signatures of XY recombination are difficult to distinguish from those of homologous transitions (i.e., transitions in sex-d...

Sex-chromosome differentiation in Rana temporaria varies strikingly among populations or families: whereas some males display well-differentiated Y haplotypes at microsatellite markers on linkage group 2 (LG2), others are genetically undistinguishable from females. We analyzed with RADseq markers one family from a Swiss lowland population with no d...

Background: Hybridization between incipient species is expected to become progressively limited as their genetic divergence increases and reproductive isolation proceeds. Amphibian radiations and their secondary contact zones are useful models to infer the timeframes of speciation, but empirical data from natural systems remains extremely scarce. H...

Hybridization by introduced taxa is a major threat to native species. Characterizing human introductions is thus one of the missions of conservation geneticists. Here we survey a declining population of the regionally endangered European tree frog (Hyla arborea) in the Grangettes natural reserve (Rhone valley, Western Switzerland), where previous e...

Contrasting with birds and mammals, poikilothermic vertebrates often have homomorphic sex chromosomes, possibly resulting from high rates of sex-chromosome turnovers and/or occasional X-Y recombination. Strong support for the latter mechanism was provided by four species of European tree frogs, which inherited from a common ancestor (~ 5 Mya) the s...

Sex-chromosome differentiation was recently shown to vary among common frog populations in Fennoscandia, suggesting a trend of increased differentiation with latitude. By rearing families from two contrasted populations (respectively, from northern and southern Sweden), we show this disparity to stem from differences in sex-determination mechanisms...

The genetic diversity of populations, which contributes greatly to their adaptive potential, is negatively affected by anthropogenic habitat fragmentation and destruction. However, continental-scale losses of genetic diversity also resulted from the population expansions that followed the end of the last glaciation, an element that is rarely consid...

Western Palearctic tree frogs (Hyla arborea group) represent a strong potential for evolutionary and conservation genetic research, so far underexploited due to limited molecular resources. New microsatellite markers have recently been developed for Hyla arborea, with high cross-species utility across the entire circum-Mediterranean radiation. Here...

Complex adaptive polymorphisms are common in nature, but what mechanisms maintain the underlying favorable allelic combinations [1-4]? The convergent evolution of polymorphic social organization in two independent ant species provides a great opportunity to investigate how genomes evolved under parallel selection. Here, we demonstrate that a large,...

Polyploidization, which is expected to trigger major genomic reorganizations, occurs much less commonly in animals than in plants, possibly because of constraints imposed by sex-determination systems. We investigated the origins and consequences of allopolyploidization in Palearctic green toads (Bufo viridis subgroup) from Central Asia, with three...

Occasional XY recombination is a proposed explanation for the sex-chromosome homomorphy in European tree frogs. Numerous laboratory crosses, however, failed to detect any event of male recombination, and a detailed survey of NW-European Hyla arborea populations identified male-specific alleles at sex-linked loci, pointing to the absence of XY recom...

The water-frog L–E system, widespread in Western Europe, comprises the pool frog Pelophylax lessonae and the hybridogenetic edible frog P. esculentus, which originated from hybridization between pool frogs and marsh frogs (P. ridibundus). In P. esculentus, the lessonae (L) genome is eliminated during meiosis and has to be gained anew each generatio...

Distribution of Pelophylax species among the five sampling sites. Color legend to pie charts: dark blue RR ridibundus, pale blue neo-ridibundus (3_EN_13), dark green ancient R′L esculentus, pale green neo R′L esculentus, red LL lessonae

A simple way to quickly optimize microsatellites in non-model organisms is to re-use loci available in closely related taxa; however, this approach can be limited by the stochastic and low cross-amplification success experienced in some groups (e.g. amphibians). An efficient alternative is to develop loci from transcriptome sequences. Transcriptomi...

Sexual reproduction is an ancient feature of life on earth, and the familiar X and Y chromosomes in humans and other model species have led to the impression that sex determination mechanisms are old and conserved. In fact, males and females are determined by diverse mechanisms that evolve rapidly in many taxa. Yet this diversity in primary sex-det...

The vast majority of eukaryotic organisms reproduce sexually, yet the nature of the sexual system and the mechanism of sex determination often vary remarkably, even among closely related species. Some species of animals and plants change sex across their lifespan, some contain hermaphrodites as well as males and females, some determine sex with hig...

In sharp contrast with birds and mammals, sex-determination systems in ectothermic vertebrates are often highly dynamic and sometimes multifactorial. Both environmental and genetic effects have been documented in common frogs (Rana temporaria). One genetic linkage group, mapping to the largest pair of chromosomes and harboring the candidate sex-det...

Sexual reproduction is a fundamental aspect of life. It is defined by the occurrence of meiosis and the fusion of two gametes of different sexes or mating types. Genetic mechanisms for the determination and differentiation of the two sexes are diverse and evolutionary labile. This book synthesizes the contemporary literature on patterns and process...

Sexual reproduction is a fundamental aspect of life. It is defined by the occurrence of meiosis and the fusion of two gametes of different sexes or mating types. Genetic mechanisms for the determination and differentiation of the two sexes are diverse and evolutionary labile. This book synthesizes the contemporary literature on patterns and process...

This chapter first describes the overall structure of sex-determination cascades and the function of the main upstream and downstream actors (Section 3.1). Given the fundamental bipotentiality of genomes, the mechanisms of sex determination must insure proper development towards one or the other sex, and not towards intermediate phenotypes of reduc...

Sexual reproduction is a fundamental aspect of life. It is defined by the occurrence of meiosis and the fusion of two gametes of different sexes or mating types. Genetic mechanisms for the determination and differentiation of the two sexes are diverse and evolutionary labile. This book synthesizes the contemporary literature on patterns and process...

Sexual reproduction is a fundamental aspect of life. It is defined by the occurrence of meiosis and the fusion of two gametes of different sexes or mating types. Genetic mechanisms for the determination and differentiation of the two sexes are diverse and evolutionary labile. This book synthesizes the contemporary literature on patterns and process...

Sexual reproduction is a fundamental aspect of life. It is defined by the occurrence of meiosis and the fusion of two gametes of different sexes or mating types. Genetic mechanisms for the determination and differentiation of the two sexes are diverse and evolutionary labile. This book synthesizes the contemporary literature on patterns and process...

Sexual reproduction is a fundamental aspect of life. It is defined by the occurrence of meiosis and the fusion of two gametes of different sexes or mating types. Genetic mechanisms for the determination and differentiation of the two sexes are diverse and evolutionary labile. This book synthesizes the contemporary literature on patterns and process...

Sexual reproduction is a fundamental aspect of life. It is defined by the occurrence of meiosis and the fusion of two gametes of different sexes or mating types. Genetic mechanisms for the determination and differentiation of the two sexes are diverse and evolutionary labile. This book synthesizes the contemporary literature on patterns and process...

In contrast with mammals and birds, most poikilothermic vertebrates feature structurally undifferentiated sex chromosomes, which may result either from frequent turnovers, or from occasional events of XY recombination. The latter mechanism was recently suggested to be responsible for sex-chromosome homomorphy in European tree frogs (Hyla arborea)....

The marsh frog (Pelophylax ridibundus) has been introduced in many areas in Central and Western Europe as a result of commercial trade with Eastern Europe, and is rapidly replacing the native pool frog (P. lessonae). A large number of Pelophylax species are distributed in Eastern Europe and the strong phenotypic similarity between these species is...