Repeated loss of function at HD mating-type genes and of recombination suppression without mating-type locus linkage in anther-smut fungi.

A wide diversity of mating systems occur in nature, with frequent evolutionary transitions in mating-compatibility mechanisms. Basidiomycete fungi typically have two mating-type loci controlling mating compatibility, HD and PR, usually residing on different chromosomes. In Microbotryum anther-smut fungi, there have been repeated events of linkage between the two mating-type loci through chromosome fusions, leading to large non-recombining regions. By generating high-quality genome assemblies, we found that two sister Microbotryum species parasitizing Dianthus plants, M. superbum and M. shykoffianum, as well as the distantly related M. scorzonarae, have their HD and PR mating-type loci on different chromosomes, but with the PR mating-type chromosome fused with part of the ancestral HD chromosome. Furthermore, progressive extensions of recombination suppression have generated evolutionary strata. In all three species, rearrangements suggest the existence of a transient stage of HD-PR linkage by whole chromosome fusion, and, unexpectedly, the HD genes lost their function. In M. superbum, multiple natural diploid strains were homozygous, and the disrupted HD2 gene was hardly expressed. Mating tests confirmed that a single genetic factor controlled mating compatibility (i.e. PR) and that haploid strains with identical HD alleles could mate and produce infectious hyphae. The HD genes have therefore lost their function in the control of mating compatibility in these Microbotryum species. While the loss of function of PR genes in mating compatibility has been reported in a few basidiomycete fungi, these are the first documented cases for the loss of mating-type determination by HD genes in heterothallic fungi. The control of mating compatibility by a single genetic factor is beneficial under selfing and can thus be achieved repeatedly, through evolutionary convergence in distant lineages, involving different genomic or similar pathways.

Allele surfing causes maladaptation in a Pacific salmon of conservation concern.

How various factors, including demography, recombination or genome duplication, may impact the efficacy of natural selection and the burden of deleterious mutations, is a central question in evolutionary biology and genetics. In this study, we show that key evolutionary processes, including variations in i) effective population size (Ne) ii) recombination rates and iii) chromosome inheritance, have influenced the genetic load and efficacy of selection in Coho salmon (Oncorhynchus kisutch), a widely distributed salmonid species on the west coast of North America. Using whole genome resequencing data from 14 populations at different migratory distances from their southern glacial refugium, we found evidence supporting gene surfing, wherein reduced Ne at the postglacial recolonization front, leads to a decrease in the efficacy of selection and a surf of deleterious alleles in the northernmost populations. Furthermore, our results indicate that recombination rates play a prime role in shaping the load along the genome. Additionally, we identified variation in polyploidy as a contributing factor to within-genome variation of the load. Overall, our results align remarkably well with expectations under the nearly neutral theory of molecular evolution. We discuss the fundamental and applied implications of these findings for evolutionary and conservation genomics.

Subtle Introgression Footprints at the End of the Speciation Continuum in a Clade of Heliconius Butterflies.

Quantifying gene flow between lineages at different stages of the speciation continuum is central to understanding speciation. Heliconius butterflies have undergone an adaptive radiation in wing color patterns driven partly by natural selection for local mimicry. Color patterns are also known to be used as assortative mating cues. Therefore, wing pattern divergence is considered to play a role in speciation. A corollary is that mimicry between closely related species may be associated with hybridization and interfere with reproductive isolation. Here, we take a multifaceted approach to explore speciation history, species boundaries, and traits involved in species differentiation between the two closely related species, Heliconius hecale and Heliconius ismenius. We focus on geographic regions where the two species mimic each other and contrast this with geographic regions where they do not mimic each other. To examine population history and patterns of gene flow, we tested and compared a four-population model accounting for linked selection. This model suggests that the two species have remained isolated for a large part of their history, yet with a small amount of gene exchange. Accordingly, signatures of genomic introgression were small except at a major wing pattern allele and chemosensing genes and stronger in the mimetic populations compared with nonmimetic populations. Behavioral assays confirm that visual confusion exists but that short-range cues determine strong sexual isolation. Tests for chemical differentiation between species identified major differences in putative pheromones which likely mediate mate choice and the maintenance of species differences.

Population-size history inferences from the coho salmon (Oncorhynchus kisutch) genome.

Coho salmon (Oncorhynchus kisutch) are a culturally and economically important species that return from multiyear ocean migrations to spawn in rivers that flow to the Northern Pacific Ocean. Southern stocks of coho salmon in Canada and the United States have significantly declined over the past quarter century, and unfortunately, conservation efforts have not reversed this trend. To assist in stock management and conservation efforts, we generated a chromosome-level genome assembly. We also resequenced the genomes of 83 coho salmon across the North American range to identify nucleotide variants and understand the demographic histories of these salmon by modeling effective population size from genome-wide data. From demographic history modeling, we observed reductions in effective population sizes between 3,750 and 8,000 years ago for several northern sampling sites, which may correspond to bottleneck events during recolonization after glacial retreat.

Long-distance migration is a major factor driving local adaptation at continental scale in Coho salmon.

Inferring the genomic basis of local adaptation is a long-standing goal of evolutionary biology. Beyond its fundamental evolutionary implications, such knowledge can guide conservation decisions for populations of conservation and management concern. Here, we investigated the genomic basis of local adaptation in the Coho salmon (Oncorhynchus kisutch) across its entire North American range. We hypothesized that extensive spatial variation in environmental conditions and the species' homing behaviour may promote the establishment of local adaptation. We genotyped 7829 individuals representing 217 sampling locations at more than 100,000 high-quality RADseq loci to investigate how recombination might affect the detection of loci putatively under selection and took advantage of the precise description of the demographic history of the species from our previous work to draw accurate population genomic inferences about local adaptation. The results indicated that genetic differentiation scans and genetic-environment association analyses were both significantly affected by variation in recombination rate as low recombination regions displayed an increased number of outliers. By taking these confounding factors into consideration, we revealed that migration distance was the primary selective factor driving local adaptation and partial parallel divergence among distant populations. Moreover, we identified several candidate single nucleotide polymorphisms associated with long-distance migration and altitude including a gene known to be involved in adaptation to altitude in other species. The evolutionary implications of our findings are discussed along with conservation applications.

Re-evaluating Coho salmon (Oncorhynchus kisutch) conservation units in Canada using genomic data.

Conservation units (CUs) are important tools for supporting the implementation of standardized management practices for exploited species. Following the adoption of the Wild Salmon Policy in Canada, CUs were defined for Pacific salmon based on characteristics related to ecotype, life history and genetic variation using microsatellite markers as indirect measures of local adaptation. Genomic data sets have the potential to improve the definition of CUs by reducing variance around estimates of population genetic parameters, thereby increasing the power to detect more subtle patterns of population genetic structure and by providing an opportunity to incorporate adaptive information more directly with the identification of variants putatively under selection. We used one of the largest genomic data sets recently published for a nonmodel species, comprising 5662 individual Coho salmon (Oncorhynchus kisutch) from 149 sampling locations and a total of 24,542 high-quality SNPs obtained using genotyping-by-sequencing and mapped to the Coho salmon reference genome to (1) evaluate the current delineation of CUs for Coho in Canada and (2) compare patterns of population structure observed using neutral and outlier loci from genotype-environment association analyses to determine whether separate CUs that capture adaptive diversity are needed. Our results reflected CU boundaries on the whole, with the majority of sampling locations managed in the same CU clustering together within genetic groups. However, additional groups that are not currently represented by CUs were also uncovered. We observed considerable overlap in the genetic clusters identified using neutral or candidate loci, indicating a general congruence in patterns of genetic variation driven by local adaptation and gene flow in this species. Consequently, we suggest that the current CU boundaries for Coho salmon are largely well-suited for meeting the Canadian Wild Salmon Policy's objective of defining biologically distinct groups, but we highlight specific areas where CU boundaries may be refined.

Landscape genomics of the American lobster (Homarus americanus).

In marine species experiencing intense fishing pressures, knowledge of genetic structure and local adaptation represent a critical information to assist sustainable management. In this study, we performed a landscape genomics analysis in the American lobster to investigate the issues pertaining to the consequences of making use of putative adaptive loci to reliably infer population structure and thus more rigorously delineating biological management units in marine exploited species. Toward this end, we genotyped 14,893 single nucleotide polymorphism (SNPs) in 4190 lobsters sampled across 96 sampling sites distributed along 1000 km in the northwest Atlantic in both Canada and the USA. As typical for most marine species, we observed a weak, albeit highly significant genetic structure. We also found that adaptive genetic variation allows detecting fine-scale population structure not resolved by neutral genetic variation alone. Using the recent genome assembly of the American lobster, we were able to map and annotate several SNPs located in functional genes potentially implicated in adaptive processes such as thermal stress response, salinity tolerance and growth metabolism pathways. Taken together, our study indicates that weak population structure in high gene flow systems can be resolved at various spatial scales, and that putatively adaptive genetic variation can substantially enhance the delineation of biological management units of marine exploited species.

Population genetics reveals divergent lineages and ongoing hybridization in a declining migratory fish species complex.

Deciphering the effects of historical and recent demographic processes responsible for the spatial patterns of genetic diversity and structure is a key objective in evolutionary and conservation biology. Using population genetic analyses, we investigated the demographic history, the contemporary genetic diversity and structure, and the occurrence of hybridization and introgression of two species of anadromous fish with contrasting life history strategies and which have undergone recent demographic declines, the allis shad (Alosa alosa) and the twaite shad (Alosa fallax). We genotyped 706 individuals from 20 rivers and 5 sites at sea in Southern Europe at thirteen microsatellite markers. Genetic structure between populations was lower for the nearly semelparous species A. alosa, which disperses greater distances compared to the iteroparous species, A. fallax. Individuals caught at sea were assigned at the river level for A. fallax and at the region level for A. alosa. Using an approximate Bayesian computation framework, we inferred that the most likely long term historical divergence scenario between both species and lineages involved historical separation followed by secondary contact accompanied by strong population size decline. Accordingly, we found evidence for contemporary hybridization and bidirectional introgression due to gene flow between both species and lineages. Moreover, our results support the existence of at least one distinct species in the Mediterrannean sea: A. agone in Golfe du Lion area, and another divergent lineage in Corsica. Overall, our results shed light on the interplay between historical and recent demographic processes and life history strategies in shaping population genetic diversity and structure of closely related species. The recent demographic decline of these species' populations and their hybridization should be carefully considered while implementing conservation programs.

Individual-based eco-evolutionary models for understanding adaptation in changing seas.

As climate change threatens species' persistence, predicting the potential for species to adapt to rapidly changing environments is imperative for the development of effective conservation strategies. Eco-evolutionary individual-based models (IBMs) can be useful tools for achieving this objective. We performed a literature review to identify studies that apply these tools in marine systems. Our survey suggested that this is an emerging area of research fuelled in part by developments in modelling frameworks that allow simulation of increasingly complex ecological, genetic and demographic processes. The studies we identified illustrate the promise of this approach and advance our understanding of the capacity for adaptation to outpace climate change. These studies also identify limitations of current models and opportunities for further development. We discuss three main topics that emerged across studies: (i) effects of genetic architecture and non-genetic responses on adaptive potential; (ii) capacity for gene flow to facilitate rapid adaptation; and (iii) impacts of multiple stressors on persistence. Finally, we demonstrate the approach using simple simulations and provide a framework for users to explore eco-evolutionary IBMs as tools for understanding adaptation in changing seas.

Population genomics and history of speciation reveal fishery management gaps in two related redfish species (Sebastes mentella and Sebastes fasciatus).

Understanding the processes shaping population structure and reproductive isolation of marine organisms can improve their management and conservation. Using genomic markers combined with estimation of individual ancestries, assignment tests, spatial ecology, and demographic modeling, we (i) characterized the contemporary population structure, (ii) assessed the influence of space, fishing depth, and sampling years on contemporary distribution, and (iii) reconstructed the speciation history of two cryptic redfish species, Sebastes mentella and S. fasciatus. We genotyped 860 individuals in the Northwest Atlantic Ocean using 24,603 filtered single nucleotide polymorphisms (SNPs). Our results confirmed the clear genetic distinctiveness of the two species and identified three ecotypes within S. mentella and five populations in S. fasciatus. Multivariate analyses highlighted the influence of spatial distribution and depth on the overall genomic variation, while demographic modeling revealed that secondary contact models best explained inter- and intragenomic divergence. These species, ecotypes, and populations can be considered as a rare and wide continuum of genomic divergence in the marine environment. This acquired knowledge pertaining to the evolutionary processes driving population divergence and reproductive isolation will help optimizing the assessment of demographic units and possibly to refine fishery management units.

Correction: Demographic history shaped geographical patterns of deleterious mutation load in a broadly distributed Pacific Salmon.

[This corrects the article DOI: 10.1371/journal.pgen.1008348.].

Riverscape genetics in brook lamprey: genetic diversity is less influenced by river fragmentation than by gene flow with the anadromous ecotype.

Understanding the effect of human-induced landscape fragmentation on gene flow and evolutionary potential of wild populations has become a major concern. Here, we investigated the effect of riverscape fragmentation on patterns of genetic diversity in the freshwater resident European brook lamprey (Lampetra planeri) that has a low ability to pass obstacles to migration. We tested the hypotheses of (i) asymmetric gene flow following water current and (ii) an effect of gene flow with the closely related anadromous river lamprey (L. fluviatilis) ecotype on L. planeri genetic diversity. We genotyped 2472 individuals, including 225 L. fluviatilis, sampled from 81 sites upstream and downstream barriers to migration, in 29 western European rivers. Linear modelling revealed a strong positive relationship between genetic diversity and the distance from the river source, consistent with expected patterns of decreased gene flow into upstream populations. However, the presence of anthropogenic barriers had a moderate effect on spatial genetic structure. Accordingly, we found evidence for downstream-directed gene flow, supporting the hypothesis that barriers do not limit dispersal mediated by water flow. Downstream L. planeri populations in sympatry with L. fluviatilis displayed consistently higher genetic diversity. We conclude that genetic drift and slight downstream gene flow drive the genetic make-up of upstream L. planeri populations whereas gene flow between ecotypes maintains higher levels of genetic diversity in L. planeri populations sympatric with L. fluviatilis. We discuss the implications of these results for the design of conservation strategies of lamprey, and other freshwater organisms with several ecotypes, in fragmented dendritic river networks.

Introduction to Population Genomics Methods.

High-throughput sequencing technologies have provided an unprecedented opportunity to study the different evolutionary forces that have shaped present-day patterns of genetic diversity, with important implications for many directions in plant biology research. To manage such massive quantities of sequencing data, biologists, however, need new additional skills in informatics and statistics. In this chapter, our objective is to introduce population genomics methods to beginners following a learning-by-doing strategy in order to help the reader to analyze the sequencing data by themselves. Conducted analyses cover several main areas of evolutionary biology, such as an initial description of the evolutionary history of a given species or the identification of genes targeted by natural or artificial selection. In addition to the practical advices, we performed re-analyses of two cases studies with different kind of data: a domesticated cereal (African rice) and a non-domesticated tree species (sessile oak). All the code needed to replicate this work is publicly available on github ( https://github.com/ThibaultLeroyFr/Intro2PopGenomics/ ).

Demographic history shaped geographical patterns of deleterious mutation load in a broadly distributed Pacific Salmon.

A thorough reconstruction of historical processes is essential for a comprehensive understanding of the mechanisms shaping patterns of genetic diversity. Indeed, past and current conditions influencing effective population size have important evolutionary implications for the efficacy of selection, increased accumulation of deleterious mutations, and loss of adaptive potential. Here, we gather extensive genome-wide data that represent the extant diversity of the Coho salmon (Oncorhynchus kisutch) to address two objectives. We demonstrate that a single glacial refugium is the source of most of the present-day genetic diversity, with detectable inputs from a putative secondary micro-refugium. We found statistical support for a scenario whereby ancestral populations located south of the ice sheets expanded recently, swamping out most of the diversity from other putative micro-refugia. Demographic inferences revealed that genetic diversity was also affected by linked selection in large parts of the genome. Moreover, we demonstrate that the recent demographic history of this species generated regional differences in the load of deleterious mutations among populations, a finding that mirrors recent results from human populations and provides increased support for models of expansion load. We propose that insights from these historical inferences should be better integrated in conservation planning of wild organisms, which currently focuses largely on neutral genetic diversity and local adaptation, with the role of potentially maladaptive variation being generally ignored.

Copy number variants outperform SNPs to reveal genotype-temperature association in a marine species.

Copy number variants (CNVs) are a major component of genotypic and phenotypic variation in genomes. To date, our knowledge of genotypic variation and evolution has largely been acquired by means of single nucleotide polymorphism (SNPs) analyses. Until recently, the adaptive role of structural variants (SVs) and particularly that of CNVs has been overlooked in wild populations, partly due to their challenging identification. Here, we document the usefulness of Rapture, a derived reduced-representation shotgun sequencing approach, to detect and investigate copy number variants (CNVs) alongside SNPs in American lobster (Homarus americanus) populations. We conducted a comparative study to examine the potential role of SNPs and CNVs in local adaptation by sequencing 1,141 lobsters from 21 sampling sites within the southern Gulf of St. Lawrence, which experiences the highest yearly thermal variance of the Canadian marine coastal waters. Our results demonstrated that CNVs account for higher genetic differentiation than SNP markers. Contrary to SNPs, for which no significant genetic-environment association was found, 48 CNV candidates were significantly associated with the annual variance of sea surface temperature, leading to the genetic clustering of sampling locations despite their geographic separation. Altogether, we provide a strong empirical case that CNVs putatively contribute to local adaptation in marine species and unveil stronger spatial signal of population structure than SNPs. Our study provides the means to study CNVs in nonmodel species and highlights the importance of considering structural variants alongside SNPs to enhance our understanding of ecological and evolutionary processes shaping adaptive population structure.

Demographic history and genomics of local adaptation in blue tit populations.

Understanding the genomic processes underlying local adaptation is a central aim of modern evolutionary biology. This task requires identifying footprints of local selection but also estimating spatio-temporal variations in population demography and variations in recombination rate and in diversity along the genome. Here, we investigated these parameters in blue tit populations inhabiting deciduous versus evergreen forests, and insular versus mainland areas, in the context of a previously described strong phenotypic differentiation. Neighboring population pairs of deciduous and evergreen habitats were weakly genetically differentiated (F ST = 0.003 on average), nevertheless with a statistically significant effect of habitat type on the overall genetic structure. This low differentiation was consistent with the strong and long-lasting gene flow between populations inferred by demographic modeling. In turn, insular and mainland populations were moderately differentiated (F ST = 0.08 on average), in line with the inference of moderate ancestral migration, followed by isolation since the end of the last glaciation. Effective population sizes were large, yet smaller on the island than on the mainland. Weak and nonparallel footprints of divergent selection between deciduous and evergreen populations were consistent with their high connectivity and the probable polygenic nature of local adaptation in these habitats. In turn, stronger footprints of divergent selection were identified between long isolated insular versus mainland birds and were more often found in regions of low recombination, as expected from theory. Lastly, we identified a genomic inversion on the mainland, spanning 2.8 Mb. These results provide insights into the demographic history and genetic architecture of local adaptation in blue tit populations at multiple geographic scales.

Shared ancestral polymorphisms and chromosomal rearrangements as potential drivers of local adaptation in a marine fish.

Gene flow has tremendous importance for local adaptation, by influencing the fate of de novo mutations, maintaining standing genetic variation and driving adaptive introgression. Furthermore, structural variation as chromosomal rearrangements may facilitate adaptation despite high gene flow. However, our understanding of the evolutionary mechanisms impending or favouring local adaptation in the presence of gene flow is still limited to a restricted number of study systems. In this study, we examined how demographic history, shared ancestral polymorphism, and gene flow among glacial lineages contribute to local adaptation to sea conditions in a marine fish, the capelin (Mallotus villosus). We first assembled a 490-Mbp draft genome of M. villosus to map our RAD sequence reads. Then, we used a large data set of genome-wide single nucleotide polymorphisms (25,904 filtered SNPs) genotyped in 1,310 individuals collected from 31 spawning sites in the northwest Atlantic. We reconstructed the history of divergence among three glacial lineages and showed that they probably diverged from 3.8 to 1.8 million years ago and experienced secondary contacts. Within each lineage, our analyses provided evidence for large Ne and high gene flow among spawning sites. Within the Northwest Atlantic lineage, we detected a polymorphic chromosomal rearrangement leading to the occurrence of three haplogroups. Genotype-environment associations revealed molecular signatures of local adaptation to environmental conditions prevailing at spawning sites. Our study also suggests that both shared polymorphisms among lineages, resulting from standing genetic variation or introgression, and chromosomal rearrangements may contribute to local adaptation in the presence of high gene flow.

Massive postglacial gene flow between European white oaks uncovered genes underlying species barriers.

Oaks are dominant forest tree species widely distributed across the Northern Hemisphere, where they constitute natural resources of economic, ecological, social and historical value. Hybridisation and adaptive introgression have long been thought to be major drivers of their ecological success. Therefore, the maintenance of species barriers remains a key question, given the extent of interspecific gene flow. In this study, we made use of the tremendous genetic variation among four European white oak species (31 million single nucleotide polymorphisms (SNPs)) to infer the evolutionary history of these species, study patterns of genetic differentiation and identify reproductive barriers. We first analysed the ecological and historical relationships among these species and inferred a long-term strict isolation followed by a recent and extensive postglacial contact using approximate Bayesian computation. Assuming this demographic scenario, we then performed backward simulations to generate the expected distributions of differentiation under neutrality to scan their genomes for reproductive barriers. We finally identified important intrinsic and ecological functions driving the reproductive isolation. We discussed the importance of identifying the genetic basis for the ecological preferences between these oak species and its implications for the renewal of European forests under global warming.

Using Haplotype Information for Conservation Genomics.

The particular combinations of alleles that define haplotypes along individual chromosomes can be determined with increasing ease and accuracy by using current sequencing technologies. Beyond allele frequencies, haplotype data collected in population samples contain information about the history of allelic associations in gene genealogies, and this is of tremendous potential for conservation genomics. We provide an overview of how haplotype information can be used to assess historical demography, gene flow, selection, and the evolutionary outcomes of hybridization across different timescales relevant to conservation issues. We address technical aspects of applying such approaches to nonmodel species. We conclude that there is much to be gained by integrating haplotype-based analyses in future conservation genomics studies.

Comparing Pool-seq, Rapture, and GBS genotyping for inferring weak population structure: The American lobster (Homarus americanus) as a case study.

Unraveling genetic population structure is challenging in species potentially characterized by large population size and high dispersal rates, often resulting in weak genetic differentiation. Genotyping a large number of samples can improve the detection of subtle genetic structure, but this may substantially increase sequencing cost and downstream bioinformatics computational time. To overcome this challenge, alternative, cost-effective sequencing approaches, namely Pool-seq and Rapture, have been developed. We empirically measured the power of resolution and congruence of these two methods in documenting weak population structure in nonmodel species with high gene flow comparatively to a conventional genotyping-by-sequencing (GBS) approach. For this, we used the American lobster (Homarus americanus) as a case study. First, we found that GBS, Rapture, and Pool-seq approaches gave similar allele frequency estimates (i.e., correlation coefficient over 0.90) and all three revealed the same weak pattern of population structure. Yet, Pool-seq data showed F ST estimates three to five times higher than GBS and Rapture, while the latter two methods returned similar F ST estimates, indicating that individual-based approaches provided more congruent results than Pool-seq. We conclude that despite higher costs, GBS and Rapture are more convenient approaches to use in the case of species exhibiting very weak differentiation. While both GBS and Rapture approaches provided similar results with regard to estimates of population genetic parameters, GBS remains more cost-effective in project involving a relatively small numbers of genotyped individuals (e.g., <1,000). Overall, this study illustrates the complexity of estimating genetic differentiation and other summary statistics in complex biological systems characterized by large population size and migration rates.