Biology subjects

Bernatchez, L.

Publications and source records attributed to Bernatchez, L..

At least 19 recordsLinked to original sources

bioRxiv2026

From tropical rainforests to scorching deserts: biogeography shapes climate-change plasticity in Australian rainbowfishes

Thermal tolerance and the plasticity of regulatory mechanisms are likely to influence biodiversity persistence under global warming. Continental-scale assessments of physiological resilience and gene expression plasticity within a closely related clade are rare, yet they could reveal how bioregional climatic history shapes vulnerability to climate warming. We used a comparative approach across five climatic ecotypes of Australian rainbowfishes (tropical rainforest, tropical savannah, subtropical, desert, and temperate) to investigate variation in thermal tolerance and gene expression plasticity in response to warming. We reconstructed phylogenetic relationships among these ecotypes, estimated their ecological niches and environmental warming tolerance, and experimentally measured CTMAX and global gene expression responses to a projected summer heat event. Closely related ecotypes showed divergent bioclimatic niches, contrasting sensitivities to warming, and extensive but idiosyncratic expression responses to heat stress. Plastic responses to warming, including in key heat stress genes, were positively associated with thermal tolerance across ecotypes. The tropical savannah and subtropical ecotypes, both from environmentally variable bioregions, showed extensive transcriptional responses to warming and high thermal tolerance. The desert ecotype was intermediate for both traits, whereas the temperate ecotype showed the most limited transcriptional response and lowest thermal tolerance. In contrast, the tropical rainforest ecotype showed limited plasticity, potentially reflecting local adaptation to milder, more stable conditions and more specialised thermal responses. Our findings support the hypothesis that bioregional climatic history shapes broad patterns of climate resilience, including thermal tolerance and transcriptional plasticity, and may influence which combinations of traits are favoured under future climates.

ecology↗

bioRxiv2026

Tropical rainforest versus savannah: Biome-specific landscape structure mediates adaptive strategies and resilience to environmental change

As ecosystems face rapid environmental change, understanding the interplay between landscape structure, genetic diversity, and adaptive potential is critical for predicting resilience. We investigated how biome-specific connectivity and environmental heterogeneity mediate adaptive strategies and resilience in the tropical rainbowfish (Melanotaenia splendida splendida) across contrasting rainforest and savannah ecosystems in tropical Australia. Using an integrative framework combining genomic, morphological, and environmental analyses, we inferred that hydroclimatic variation has been a key driver of genetic and phenotypic divergence. Rainforest populations exhibited strong local adaptation to fragmented, stable environments, while savannah populations showed less genomic differentiation and morphological divergence, patterns consistent with weaker local adaptation. We hypothesise that greater reliance on phenotypic plasticity may facilitate adaptive responses in savannah populations, reflecting their exposure to more connected and variable environments. Variance partitioning highlighted the contrasting roles of neutral and adaptive processes across biomes, with implications for managing resilience in freshwater systems under climate change. Our findings underscore the trade-offs between connectivity, local adaptation, and plasticity, providing a model for understanding adaptation and resilience across diverse ecosystems.

ecology↗

bioRxiv2024

Chromosome-level genome assembly of a doubled haploid brook trout (Salvelinus fontinalis)

Brook trout (Salvelinus fontinalis) is a socioeconomically important fish species for fisheries, aquaculture and aquatic conservation. We produced a 2.5 Gb reference assembly by combining Hi-C chromosome conformation capture with high-coverage short- and long-read sequencing of a fully homozygous mitotic gynogenic doubled haploid fish, which facilitates assembly of highly complex salmonid genomes. The assembly has a N50 of 50.98 Mb and 88.9% of the total assembled sequence length is anchored into 42 main chromosomes, of which 63.44% represents repeated contents, including 1,461,010 DNA transposons. 56,058 genes were found with the NCBI annotation pipeline, with 99% of the 3,640 expected conserved orthologs BUSCO genes (actinopterygii_odb10 lineage database). Additionally, we found significant homology within the 42 chromosomes, as expected for this pseudo-tetraploid species, as well as with the sister species lake trout (Salvelinus namaycush) and Atlantic salmon (Salmo salar). This assembly will serve as a reliable genomic resource for brook trout, thus enabling a wider range of reference-based applications to support ongoing research and management decision-making for the species.

genomics↗

bioRxiv2024

Sex-biased gene expression across tissues reveals unexpected differentiation in the gills of the threespine stickleback

Sexual dimorphism can evolve through sex-specific regulation of the same gene set. However, sex chromosomes can also facilitate this by directly linking gene expression to sex. Moreover, differences in gene content between heteromorphic sex chromosomes contributes to sexual dimorphism. Understanding patterns of sex-biased gene expression across organisms is important for gaining insight about the evolution of sexual dimorphism and sex chromosomes. Moreover, studying gene expression in species with recently established sex chromosomes can help understand the evolutionary dynamics of gene loss and dosage compensation. The three-spined stickleback is known for its strong sexual dimorphism, especially during the reproductive period. Sex is determined by a young XY sex chromosome pair with a non-recombining region divided in three strata, which have started to degenerate. Using the high multiplexing capability of 3' QuantSeq to sequence the sex-biased transcriptome of liver, gills and brain, we provide the first characterization of sex-specific transcriptomes from [~]80 stickleback (40 males and 40 females) collected from a natural population during the reproductive period. We find that the liver is extremely differentiated between sexes (36% of autosomal genes) and reflects ongoing reproduction, while the brain shows very low levels of differentiation (0.78%) with no functional enrichment. Finally, the gills exhibit high levels of differentiation (5%), suggesting that sex should be considered in physiological and ecotoxicological studies of gill responses in fishes. We also find that sex-biased gene expression in hemizygous genes is mainly driven by a lack of dosage compensation. However, sex-biased expression of genes that have conserved copies on both sex chromosomes is likely driven by the degeneration of Y allele expression and a down-regulation of male-beneficial mutations on the X chromosome.

evolutionary biology↗

bioRxiv2023

Investigating structural variant, indel and single nucleotide polymorphism differentiation between locally adapted Atlantic salmon populations using whole genome sequencing and a hybrid genomic polymorphism detection approach

Genomic structural variants (SVs) are now recognized as an integral component of intraspecific polymorphism and are known to contribute to evolutionary processes in various organisms. However, they are inherently difficult to detect and genotype from readily available short-read sequencing data, and therefore remain poorly documented in wild populations. Salmonid species displaying strong interpopulation variability in both life history traits and habitat characteristics, such as Atlantic salmon (Salmo salar), offer a prime context for studying adaptive polymorphism, but the contribution of SVs to fine-scale local adaptation has yet to be explored. Here, we performed a comparative analysis of SVs, single nucleotide polymorphisms (SNPs) and small indels (< 50 bp) segregating in the Romaine and Puyjalon salmon, two putatively locally adapted populations inhabiting neighboring rivers (Quebec, Canada) and showing pronounced variation in life history traits, namely growth, fecundity, and age at maturity and at smoltification. We first catalogued polymorphism using a hybrid SV characterization approach pairing both short (16X) and long-read sequencing (20X) for variant discovery with graph-based genotyping of SVs across 60 salmon genomes, along with characterization of SNPs and small indels from short reads. We thus identified 115,907 SVs, 8,777,832 SNPs and 1,089,321 short indels, with SVs covering 4.8 times more base pairs than SNPs. All three variant types revealed a highly congruent population structure and similar patterns of FSTand density variation along the genome. Finally, we performed outlier detection and redundancy analysis (RDA) to identify variants of interest in the putative local adaptation of Romaine and Puyjalon salmon. Genes located near these variants were enriched for biological processes related to nervous system function, suggesting that observed variation in traits such as age at smoltification could arise from differences in neural development. This study therefore demonstrates the feasibility of large-scale SV characterization and highlights its relevance for salmonid population genomics.

genomics↗

bioRxiv2023

Widespread deviant patterns of heterozygosity in whole-genome sequencing due to autopolyploidy, repeated elements and duplication

Most population genomic tools rely on accurate SNP calling and filtering to meet their underlying assumptions. However, genomic complexity, due to structural variants, paralogous sequences and repetitive elements, presents significant challenges in assembling contiguous reference genomes. Consequently, short-read resequencing studies can encounter mismapping issues, leading to SNPs that deviate from Mendelian expected patterns of heterozygosity and allelic ratio. In this study, we employed the ngsParalog software to identify such deviant SNPs in whole-genome sequencing data from four species: Arctic Char (Salvelinus alpinus), Lake Whitefish (Coregonus clupeaformis), Atlantic Salmon (Salmo salar), and the American Eel (Anguilla rostrata), with low (2X) to intermediate (6X) coverage. The analyses revealed that deviant SNPs accounted for up to 62% of all SNPs in salmonid datasets and approximately 10% in the American Eel dataset. These deviant SNPs were particularly concentrated within repetitive elements and genomic regions that had recently undergone rediploidization in salmonids. Additionally, narrow peaks of elevated coverage were ubiquitous along all four reference genomes, encompassed most deviant SNPs and could be partially attributed to transposons and tandem repeats. Including these deviant SNPs in genomic analyses led to highly distorted site frequency spectra, apparent homogenization of populations and underestimating pairwise FST values. Considering the widespread occurrence of deviant SNPs arising from a variety of source, their important impact in estimating population parameters, and the availability of effective tools to identify them, we propose that excluding deviant-SNPs from WGS datasets is required to improve genomic inferences for a wide range of taxa and sequencing depths. Significance: Genomes can be very repetitive and hard to assemble into a reference, which can lead to biases when genotyping genetic markers in complex genomic regions. Here, we draw attention to this issue in various whole-genome datasets and validate a method to identify problematic SNPs at low coverage. We also explore processes creating such SNPs and their consequences on common population genomics analyses.

genomics↗

bioRxiv2022

Evidence for epigenetically influenced mutagenesis and genetic assimilation in nascent species complexes (Coregonus sp.)

Phenotypic diversification is classically associated with genetic differentiation and gene expression variation. However, increasing evidence suggests that DNA methylation is involved in evolutionary processes due to its phenotypic and transcriptional effects. Methylation can increase mutagenesis and could lead to increased genetic divergence between populations experiencing different environmental conditions for many generations, though there has been minimal empirical research on epigenetically induced mutagenesis in diversification and speciation. Whitefish, freshwater members of the salmonid family, are excellent systems to study phenotypic diversification and speciation due to the repeated divergence of benthic-limnetic species pairs serving as natural replicates. Here we investigate whole genome genetic and epigenetic differentiation between sympatric benthic-limnetic species pairs in lake and European whitefish (Coregonus clupeaformis and C. lavaretus) from four lakes (N=64). We found considerable, albeit variable, genetic and epigenetic differences between species pairs. All SNP types were enriched at CpG sites supporting the mutagenic nature of DNA methylation, though C>T SNPs were most common. We also found an enrichment of overlaps between outlier SNPs with the 5% highest FST between species and differentially methylated loci. This could possibly represent differentially methylated sites that have caused divergent genetic mutations between species, or divergent selection leading to both genetic and epigenetic variation at these sites. Our results support the hypothesis that DNA methylation contributes to phenotypic divergence and mutagenesis during whitefish speciation. Significance statementDNA methylation is an epigenetic mark known to change in response to the environment and induce genetic modifications such as point mutations, though its implications for evolution and speciation have not been thoroughly studied. We find considerable but variable genetic and epigenetic variation between whitefish benthic-limnetic species pairs, highlighting the potential for DNA methylation to contribute to mutagenesis and genetic evolution. Our study provides evidence that DNA methylation could have contributed to whitefish speciation, both through initially plastic methylation changes and by driving genetic divergence between species pairs.

evolutionary biology↗

bioRxiv2022

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. Author SummaryUnderstanding how historical processes, such as past glaciations, may have impacted variations in population size and genetic diversity along the genome is a fundamental question in evolution. In this study, we investigated how recent postglacial demographic expansion has affected the distribution of deleterious genetic variants and the resulting deleterious mutation load in Coho salmon (Oncorhynchus kisutch), throughout its native range in North America. By sequencing the entire genome of 71 Coho salmon, we reveal that postglacial expansion has led to allele surfing, a process where alleles increase in frequency in populations that are expanding or colonizing new environments. Here, allele surfing resulted in an increased deleterious mutation load at the colonization front. Furthermore, we demonstrated that the efficacy of natural selection scales with variation in effective population size among populations. We showed that the specific genomic features of Coho salmon, namely variation in local recombination rate and variation in chromosomal inheritance, strongly impacted the segregation of deleterious mutations.

evolutionary biology↗

bioRxiv2022

Natural hybridisation reduces vulnerability to climate change

Understanding how species can respond to climate change is a major global challenge. Species unable to track their niche via range shifts are largely reliant on genetic variation to adapt and persist. Genomic vulnerability predictions are used to identify populations that lack the necessary variation, particularly at climate relevant genes. However, hybridization as a source of novel adaptive variation is typically ignored in genomic vulnerability studies. We estimated environmental niche models and genomic vulnerability for closely related species of rainbowfish (Melanotaenia spp.) across an elevational gradient in the Australian wet tropics. Hybrid populations between a widespread generalist and narrow range endemics exhibited reduced vulnerability to projected climates compared to pure narrow endemics. Overlaps between introgressed and adaptive genomic regions were consistent with a signal of adaptive introgression. Our findings highlight the often-underappreciated conservation value of hybrid populations and indicate that adaptive introgression may contribute to evolutionary rescue of species with narrow environmental ranges.

evolutionary biology↗

bioRxiv2022

Captive rearing effects on the methylome of Atlantic salmon after oceanic migration: sex-specificity and intergenerational stability

Captive rearing in salmon hatcheries can have considerable impacts on both fish phenotype and fitness within a single generation, even in the absence of genetic change. Evidence for hatchery-induced changes in DNA methylation is becoming abundant, though questions remain on the sex-specificity of these effects, their persistence until spawning, and potential for transmission to future generations. Here we performed whole genome methylation sequencing of fin tissue for 16 hatchery and 16 wild Atlantic salmon (Salmo salar) returning to spawn in the Rimouski River, Quebec. We identified two cohorts of hatchery-reared salmon through methylation analysis, one of which was epigenetically similar to wild fish, suggesting that supplementation efforts may be able to minimize the epigenetic effects of hatchery rearing. We found considerable sex-specific effects of hatchery rearing, with few genomic regions being affected in both males and females. We also analysed the methylome of 32 F1 offspring from four groups (pure wild, pure hatchery origin, and reciprocal hybrids). We found that few epigenetic changes due to parental hatchery rearing persisted in the F1 offspring though the patterns of inheritance appear to be complex, involving nonadditive effects. Our results suggest that the epigenetic effects of hatchery rearing can be minimal in F0. There may also be minimal epigenetic inheritance and rapid loss of epigenetic changes associated with hatchery rearing. However, due to sex-specificity and nonadditive patterns of inheritance, methylation changes due to captive rearing are rather complex and the field would benefit from further research on minimizing the epigenetic effects of captive rearing in conservation efforts.

evolutionary biology↗

bioRxiv2022

Searching for intra-locus sexual conflicts in the three-spined stickleback (Gasterosteus aculeatus) genome

Differences between sexes in trait fitness optima can generate intra-locus sexual conflicts that have the potential to maintain genetic diversity through balancing selection. However, these differences are unlikely to be associated with string selective coefficients and as a result are challenging to detect. Additionally, recent studies have highlighted that duplication on sexual chromosomes can create artefactual signals of inter-sex differentiation and increased genetic diversity. Thus, testing the relationship between intra-locus sexual conflicts and balancing selection requires a high-quality reference genome, stringent filtering of potentially duplicated regions, and dedicated methods to detect loci with low levels of inter-sex differentiation. In this study, we investigate intra-locus sexual conflicts in the three-spined stickleback using whole genome sequencing (mean coverage = 12X) of 50 females and 49 males from an anadromous population in the St. Lawrence River, Quebec, Canada. After stringent filtering of duplications from the sex chromosomes, we compared three methods to detect intra-locus sexual conflicts. This allowed us to detect various levels of inter-sex differentiation, from stronger single locus effects to small cumulative or multivariate signals. Overall, we found only four genomic regions associated with confidence to intra-locus sexual conflict that displayed associations with long-term balancing selection maintaining genetic diversity. Altogether, this suggests that most intra-locus sexual conflicts do not drive long-term balancing selection and are most likely transient. However, they might still play a role in maintaining genetic diversity over shorter time scales by locally reducing the effects of purifying selection and the rates of genetic diversity erosion.

evolutionary biology↗

bioRxiv2022

Isolation-by-distance and 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 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 two chromosome-level genome assemblies and sequenced 24 RNA-seq libraries to better annotate the coho salmon genome assemblies. We also resequenced the genomes of 83 coho salmon across their North American range to identify nucleotide variants, characterize the broad effects of isolation-by-distance using a genome-wide association analysis approach, and understand the demographic histories of these salmon by modeling population size from genome-wide data. We observed that more than 13% of all SNPs were associated with latitude (before multiple test correction), likely an affect of isolation-by-distance. From demographic history modeling, we estimated that the SNP latitudinal gradient likely developed as recently as 8,000 years ago. In addition, we identified four genes each harboring multiple SNPs associated with latitude; all of these SNPs were also predicted to modify the function of the gene. Three of these genes have roles in cell junction maintenance and may be involved in osmoregulation. This signifies that ocean salinity may have been a factor influencing coho salmon recolonization after the last glaciation period - generating the current pattern of variation in these three genes.

genomics↗

bioRxiv2022

Two different mental disc forms in the Tashan cave Garra: different species or ecotypes?

In the Tashan Cave barb Garra tashanensis, inhabiting a small cave in south west Iran, two mental disc forms were observed. To assess their phylogenetic relationships, disc-less and disc-bearing individuals were analyzed using mitochondrial cytochrome oxidase subunit I (COI) partial DNA sequences. Both mental disc forms nested within one clade with absolute bootstrap support (BS = 100), and the genetic distances between the disc-bearing and disc-less individuals (0.3-0.7%) was considerably lower than inter-species mtDNA sequence distances reported among members of the genus Garra. Hence, the observed mental disc variation was not inferred to be a taxonomic feature or a consequence of character displacement. Instead, it was inferred as a case of character release to diversify among ecological niches in the limited subterranean habitat, which should be clarified in follow-up ecological and population genetic studies in more detail.

ecology↗

bioRxiv2022

Environmental selection, rather than neutral processes, best explain patterns of diversity in a tropical rainforest fish

To conserve the high functional and genetic variation in hotspots such as tropical rainforests, it is essential to understand the forces driving and maintaining biodiversity. We asked to what extent environmental gradients and terrain structure affect morphological and genomic variation across the wet tropical distribution of an Australian rainbowfish, Melanotaenia splendida splendida. We used an integrative riverscape genomics and morphometrics framework to assess the influence of these factors on both putative adaptive and non-adaptive spatial divergence. We found that neutral genetic population structure was largely explainable by restricted gene flow among drainages. However, environmental associations revealed that ecological variables had a similar power to explain overall genetic variation, and greater power to explain body shape variation, than the included neutral covariables. Hydrological and thermal variables were the best environmental predictors and were correlated with traits previously linked to heritable habitat-associated dimorphism in rainbowfishes. Additionally, climate-associated genetic variation was significantly associated with morphology, supporting heritability of shape variation. These results support the inference of evolved functional differences among localities, and the importance of hydroclimate in early stages of diversification. We expect that substantial evolutionary responses will be required in tropical rainforest endemics to mitigate local fitness losses due to changing climates.

evolutionary biology↗

bioRxiv2022

Thermal regime during parental sexual maturation, but not during offspring rearing, modulates DNA methylation in brook charr (Salvelinus fontinalis)

Epigenetic inheritance can result in plastic responses to changing environments being faithfully transmitted to offspring. However, it remains unclear how epigenetic mechanisms such as DNA methylation can contribute to multigenerational acclimation and adaptation to environmental stressors. Brook charr (Salvelinus fontinalis), an economically important salmonid, is highly sensitive to thermal stress, and is of conservation concern in the context of climate change. We studied the effects of temperature during parental sexual maturation and offspring rearing on whole-genome DNA methylation in brook charr juveniles (fry). Parents were split between warm and cold temperatures during sexual maturation, mated in controlled breeding designs, then offspring from each family were split between warm (8{degrees}C) and cold (5{degrees}C) rearing environments. We found 188 differentially methylated regions (DMRs) due to parental maturation temperature after controlling for family structure. In contrast, offspring rearing temperature had a negligible effect on offspring methylation. Stable intergenerational inheritance of DNA methylation and minimal plasticity in progeny could result in transmission of acclimatory epigenetic states to offspring, priming them for a warming environment. Our findings have implications pertaining to the role of intergenerational epigenetic inheritance in response to ongoing climate change.

evolutionary biology↗

bioRxiv2022

Genome assembly, structural variants, and genetic differentiation between Lake Whitefish young species pairs (Coregonus sp.) with long and short reads

Nascent pairs of ecologically differentiated species offer an opportunity to get a better glimpse at the genetic architecture of speciation. Of particular interest is our recent ability to consider a wider range of genomic variants, not only single-nucleotide polymorphisms (SNPs), thanks to long-read sequencing technology. We can now identify structural variants (SVs) like insertions, deletions, and other rearrangements, allowing further insights into the genetic architecture of speciation and how different types of variants are involved in species differentiation. Here, we investigated genomic patterns of differentiation between sympatric species pairs (Dwarf and Normal) belonging to the Lake Whitefish (Coregonus clupeaformis) species complex. We assembled the first reference genomes for both C. clupeaformis sp. Normal and C. clupeaformis sp. Dwarf, annotated the transposable elements, and analysed the genomes in the light of related coregonid species. Next, we used a combination of long-read and short-read sequencing to characterize SVs and genotype them at population-scale using genome-graph approaches, showing that SVs cover five times more of the genome than SNPs. We then integrated both SNPs and SVs to investigate the genetic architecture of species differentiation in two different lakes and highlighted an excess of shared outliers of differentiation. In particular, a large fraction of SVs differentiating the two species correspond to insertions or deletions of transposable elements (TEs), suggesting that TE accumulation may represent a key component of genetic divergence between the Dwarf and Normal species. Altogether, our results suggest that SVs may play an important role in speciation and that, by combining second and third generation sequencing, we now have the ability to integrate SVs into speciation genomics.

evolutionary biology↗

bioRxiv2021

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 behavior may promote the establishment of local adaptation. We genotyped 7,829 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. 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 candidates SNP 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.

evolutionary biology↗

bioRxiv2021

A supergene in seaweed flies modulates male traits and female perception

Supergenes, tightly linked allelic combinations that underlie complex adaptive phenotypes represent a critical mechanism protecting intra-specific polymorphism [1, 2]. Supergenes represent some of the best examples of balancing selection in nature and there is increasing evidence that disassortative mating, when individuals preferentially mate with dissimilar phenotypes, is a key force stabilizing supergene polymorphisms. Yet, the underlying biological mechanisms and genetic basis of disassortative mating remain poorly known. Here, we examine a possible mechanism of disassortative mating driven by female mate choice in relation to the overdominant Cf-Inv(1) supergene in the seaweed fly Coelopa frigida by investigating chemical communication and its genomic architecture. We show that Cf-Inv(1) strongly affects chemical signaling; cuticular hydrocarbon (CHC) composition differed between genotypes in males but not females across two continents. In tandem, Cf-Inv(1) affected female perception of these compounds; females are able to sense 36 compounds from the male CHC cocktail but show differential perception between genotypes for almost half of them. This indicates that the genetic underpinnings of male traits and female perceptions are tightly linked within Cf-Inv(1) which likely facilitates disassortative mating [3]. A differential expression approach based on candidate genes for CHC biosynthesis and odorant detection revealed differential expression for CHC biosynthesis in males alone but broad changes in odorant receptors across both sexes. Furthermore, odorant genes clustered together within Cf-Inv(1), with some of them differing between arrangements by 8.3% at the protein level, suggesting evolution via tandem duplication then divergence. We propose that the tight linkage between overdominant loci, male traits, and female perception has helped to maintain the Cf-Inv(1) polymorphism across its range in the face of supergene degeneration.

evolutionary biology↗