Heredity

Sexual selection arises from individual differences in reproductive success, which can drive the maintenance of genetic polymorphisms in genes subject to balancing selection by the pleiotropic effects that trade-off between survival and reproduction. However, the extent to which sexual selection maintains genetic polymorphisms in wild populations remains unclear. Here, we explored on genomic signatures of balancing selection and selective sweep in the northern medaka, Oryzias sakaizumii in Japan by performing whole-genome resequencing of wild individuals. In addition, we re-evaluated the population genetic structure and admixture of Oryzias latipes and O. sakaizumii across the Japanese archipelago and detected genomic regions affected by introgression. Regions with signatures of selection from multiple statistics were located on eleven chromosomes. In particular, a region spanning 4.25 to 6.80 Mb on chromosome 18 showed high genetic diversity that could not be explained by sex differentiation or introgression from O. latipes in Eastern Japan. This pattern suggests that balancing selection maintains genetic polymorphisms in O. sakaizumii. Specifically, because a previously reported quantitative trait locus associated with female mating behavior overlaps with this region, we infer that sexual selection contributes to the maintenance of genetic polymorphism at this locus.

Whole genome duplication is a common mutation in eukaryotes with far-reaching phenotypic effects. The resulting morphological, physiological, and fitness consequences and how they affect the survival probability of newly polyploid lineages are intensively studied, but very little is known about the effect of genome doubling on the short-term evolvability of populations. Understanding the effect of polyploidization on the adaptive potential of populations is of crucial importance to predict the future of polyploid populations. In this paper, I investigate the immediate consequences of genome doubling on the genetic variance of populations. To do so, I performed numerical iterations and simulations of how the genetic variance of a quantitative trait changes after polyploidization, under different genetic architectures (additivity, dominance, and epistasis). I found that genetic variance generally decreases after genome doubling. Non-additive gene actions can make autotetraploid populations genetically more diverse than their diploid progenitors in rare cases, notably with overdominance and directional epistasis. By collecting estimates from the agronomic literature, I found that both dominance and epistatic variance contribute to the genetic variance of polyploid populations. These results bring new insights into the adaptive potential of newly formed tetraploid populations, and call for further experimental investigations of how polyploidization is associated with a short-term decrease in evolvability.

The European flat oyster (Ostrea edulis), like numerous other oyster species, has been exploited for millennia and cultivated and translocated for centuries. Following a severe population decline, and in the context of ongoing conservation and restoration programs, genetic considerations must now be addressed to avoid mistakes. The objective of our study was to complement population genetic studies conducted at various scales along European coasts. Our sampling primarily targeted the French Atlantic, English Channel, and Mediterranean coasts, aiming to provide a fine-scale genetic characterization of populations in these regions. By integrating SNP array and low-coverage sequencing datasets, we obtained a comprehensive overview of the population genetic structure of Ostrea edulis across western Europe. Most previously identified clusters in Western Europe were confirmed. In France, populations assigned to these clusters exhibited notable within-patch homogeneity. However, two key findings emerged: (1) an extensive overlap zone between the Atlantic and western Mediterranean clusters, spanning at least from southern Portugal to southern France, and (2) the detection of a novel, clearly distinct cryptic cluster east of the English Channel, whose geographic range remains to be better delineated. These insights are critical for informing management decisions, particularly as restoration and conservation plans are currently being implemented across the species range.

Life-history theory predicts a trade-off between reproduction and survival, often invoked to explain human ageing through antagonistic pleiotropy, yet evidence for a genetic trade-off between fertility and longevity in humans remains mixed. We tested whether reproductive traits and lifespan are linked by additive genetic covariance in a large historical Dutch genealogical dataset comprising individuals born between 1850 and 1915. Using quantitative genetic animal models, we estimated heritabilities, cross-sex phenotypic and genetic correlations, and within-sex genetic correlations among lifespan, offspring number, and ages at first and last reproduction. Separate analyses were performed for individuals surviving beyond ages 13 and 45. Lifespan and reproductive traits were moderately heritable, and high cross-sex genetic correlations indicated substantial shared genetic architecture between the sexes. Genetic correlations between parity and lifespan provided limited evidence for a fertility-longevity trade-off: they were weakly negative in women, but close to zero or weakly positive in men. In contrast, age at first reproduction showed moderate positive genetic correlations with lifespan in the 13+ sample. Higher parity was strongly genetically associated with earlier first reproduction and later last reproduction, indicating that offspring number is partly embedded in the genetic architecture of reproductive timing. Age at first and last reproduction were also positively genetically correlated, suggesting a trade-off between reproductive investment in early versus late life. These findings suggest that shared genetic influences on viability, developmental tempo, and reproductive timing may be more important in shaping reproduction-survival associations than a simple allocation trade-off between fertility and somatic maintenance. SignificanceWhether reproduction genetically constrains human longevity is central to evolutionary theories of ageing. Using a large historical Dutch genealogical dataset, this study estimates genetic links between lifespan, number of children, and reproductive timing. The results show that lifespan and reproductive traits are moderately heritable and share substantial genetic influences across sexes. However, genetic correlations between parity and lifespan provided limited evidence for a fertility-longevity trade-off: they were weakly negative in women, but close to zero or weakly positive in men. Instead, reproductive success and lifespan appear closely genetically tied to the timing of reproduction. These findings help clarify how human life-history traits are genetically connected and how historical genealogies can complement modern genomic studies.

The cabbage stem flea beetle (CSFB) poses a growing threat to winter Brassica crops in Europe, yet the genetic basis of resistance remains poorly understood. To clarify the genetic architecture and evolutionary origins of resistance to CSFB adult feeding, we conducted a genome-wide association study (GWAS) by combining high-throughput pool-sequencing and a large-scale non-choice feeding assay on 113 Brassica oleracea accessions from wild (or feral) populations and major domesticated morphotypes. We demonstrate that resistance displays moderate heritability with a predominantly polygenic basis, revealing strong phenotypic divergence among morphotypes: B. oleracea var. capitata was generally susceptible, whereas var. botrytis and wild populations showed markedly higher resistance. Despite this polygenic background, we identified a major-effect candidate QTL on chromosome C01 with strong enrichment of resistance alleles in wild populations and susceptible alleles in var. capitata. Genome-wide F-statistics and heterozygosity scans revealed a recent selective sweep at this locus in wild lineages. Considering current evidence for the feral origin of contemporary "wild" populations, our results suggest that resistance evolved after domestication and subsequent feralization, independently of resistance in var. botrytis. This paraphyletic distribution underlines the critical importance of integrating demographic history into quantitative genetic analyses of domesticated plant systems.

The fungal crop pathogen Blumeria hordei, causal agent of powdery mildew on barley, presents life-history and epidemiological characteristics, as well as and selective pressures due to modern agriculture leading to expected sweepstakes reproduction, that is highly skewed offspring distributions. Using genome-wide polymorphism data and population genomics inferences, we aim to 1) infer the past demographic history and the strength of sweepstakes reproduction in B. hordei, and 2) quantify the contributions of these selective and neutral processes in the genome. An new inference method based on Neural Posterior Estimation and diversity and linkage disequilibrium statistics was developed and tested on simulated and B. hordei genomic data. We confirm that B. hordei exhibits a moderate sweepstakes reproduction (-parameter of 1.6). We highlight that the Site Frequency Spectrum (SFS) appears sensitive to the joint occurrence of sweepstakes and recent demographic changes, which may caution on the reliability of the SFS to infer sweepstakes reproduction. We then scan the genome for selective sweeps, adjusting the significance thresholds of the methods for demographic history and sweepstakes reproduction, thereby yielding a counterintuitive result. When conditioning the significance threshold for sweep detection on simulations under sweepstakes and demography, a very large number of putatively selected regions is found (11.6% of the genome). We suggest that sweepstakes reproduction in B. hordei is due to 1) neutrality (clonal/sexual phases and Boom-and-Bust cycles) generating a genome-wide level of background noise in the coalescent genealogies, and 2) selective sweepstakes due to pervasive positive selection. Our findings have important implications for both population genomic methodology and our understanding of pathogen evolution.

Despite being two of the most commercially important flatfish (order Pleuronectiformes) in Europe, little is known of the population structure of common sole Solea solea and European plaice Pleuronectes platessa. To address this gap, we generated full-genome resequencing data for 244 sole and 189 plaice in the Celtic Sea and western English Channel region to analyse both neutral and adaptive loci and quantify population processes, such as reproductive isolation or adaptive differentiation in each species. For sole, there was no evidence of reproductive isolation or population structure at neutral loci. There was, however, adaptive differentiation as adaptive loci indicated two subpopulations, with separation in the western English Channel. This is consistent with previous studies using RAD-seq and gene-linked SNPs. For plaice, there was no evidence of population structure at either neutral or adaptive loci in the Celtic Seas and Western English Channel region. However, when considering a larger geographical area and utilising previously published genomic data, three distinct populations of plaice were identified (Iceland; North Sea, Kattegat and Western Baltic; Celtic Sea and western English Channel), with clear reproductive isolation indicated by neutral loci and adaptive differentiation indicated by adaptive loci. Moreover, three large chromosomal inversions were identified, which differed in their frequency between regions. These large structural variants represent putative key regions for adaptive differentiation. This study shows the benefit from quantifying neutral and adaptive loci to better understand population structure and genetic diversity of commercially important fish.

Ectomycorrhizal (EM) fungi are vital to forest ecosystems, supporting tree growth and survival. However, their inclusion in conservation policy and action remains limited and little is known about the status of their genetic diversity, which is essential for their long-term survival and adaptation. The Global Biodiversity Framework adopted a genetic indicator based on the effective population size, Ne, to monitor genetic diversity in all species. To date, it is still uncertain how Ne, a key parameter, can be reliably assessed in species with complex life history traits. Ectomycorrhizal fungi are a highly diverse group of taxa displaying haplodiplontic life cycles with partially clonal reproduction. Here, we review the literature to understand how these life history traits might affect Ne and its estimation in six species of EM fungi. We estimated Ne in 19 populations using eight genetic and genomic datasets from selected studies. We compared Ne estimates using Linkage Disequilibrium (LD) and Sibship Frequency (SF) methods. We tested how Ne estimates change due to partial clonality and genetic structure gradients and whether the number of genetic markers influence the precision of the estimates. We show a systematic bias in Ne estimations when large clones are present and when populations are not correctly delimited. We found both methods are not robust to these factors, which makes them unreliable for conservation assessment purposes in EM fungi. This study provides new perspectives for further research into the links between life history traits and the effective population size of ectomycorrhizal fungi.

Genomic offset (GO) is increasingly used to predict population maladaptation risk under climate change, with larger offsets assumed to indicate greater vulnerability. Despite rapid adoption in conservation planning, it remains unclear how sensitive GO estimates are to key methodological choices, including SNP set composition, genotype-environment association (GEA) methods, and the specific GO metric used. Empirical validation against observed population dynamics also remains limited. Here, we evaluate the methodological robustness and predictive performance of GO using multidecadal demographic monitoring data from Lycaeides butterflies, a system with short generation times and high fecundity that may facilitate rapid adaptive responses. GO estimates were broadly consistent across SNP sets, regardless of composition or size, with climate-associated and randomly selected SNPs yielding largely concordant values. Consistency across GEA methods was moderate and depended on the SNP set used. In contrast, GO metrics differed substantially in the magnitude of maladaptation estimated, suggesting they capture distinct biological signals and should not be treated as interchangeable. Crucially, GO was a poor predictor of observed population trends, regardless of SNP set composition, GO metric, or GEA method, both at sites used to fit GEA models and when extrapolated to independent demographic sites. These findings suggest that, while GO provides a valuable conceptual framework for assessing potential maladaptation, its quantitative estimates and predictive power are sensitive to methodological choices and species-specific biological context. We therefore urge careful alignment of GO metric assumptions with conservation objectives, along with rigorous empirical validation, before GO estimates are used to inform management decisions.

Testing for Hardy-Weinberg equilibrium (HWE) is a fundamental component of genetic data analysis, widely used for quality control and model validation. Although HWE testing is well established for autosomal loci, inference on the X chromosome is more complex due to sex-specific genotype structures and potential sex differences in minor allele frequency (sdMAF). Existing tests differ in their assumptions about sdMAF and male sample inclusion, often leading to distinct but poorly characterized null hypotheses. We develop a general statistical framework for HWE inference using the robust allele-based regression model. By formulating HWE testing as an assessment of allele-level dependence, the framework directly parameterizes Hardy-Weinberg disequilibrium, unifies existing Pearson{chi} 2-based tests under explicit modeling assumptions, and clarifies their null hypotheses, degrees of freedom, and sensitivity to sdMAF. The framework also accommodates covariate and population-structure adjustment within a unified regression-based formulation. The proposed framework provides robust, interpretable, and flexible inference, establishing a unified statistical foundation for HWE testing across autosomal and X-chromosomal regions. Simulation studies and analysis of high-coverage 1000 Genomes Project data demonstrate that commonly used X-chromosome tests can exhibit inflated type I error or misleading inference when sdMAF is present.

Genomic forecasting approaches based on genotype-environment associations (GEAs) are increasingly used to estimate genomic offsets (GOs), which predict population maladaptation and extinction risk under current or future climatic conditions. Despite their widespread use, only a subset of studies have evaluated how accurately GOs predict (mal)adaptation, limiting their interpretation and application in policy and management. Here, we used GEA analyses to estimate GOs for past, present, and future climates in Lycaeides butterflies, focusing on the causes of variation in GOs among populations and their relationships with demographic parameters inferred from population genomic data. Using multivariate linear regression and genotyping-by-sequencing data from 42 Lycaeides populations (922 butterflies), we found that mean annual temperature, cumulative annual precipitation, and hybridization history together explained 47.6% of variation in genome-wide allele frequencies. Genomic offsets differed substantially among populations and across past, present, and future climates, with evidence for increasing maladaptation under more distant future climate scenarios. We found no relationship between GOs for present climates and contemporary effective population size. In contrast, genetic diversity, which reflects long-term effective population size, and local rates of gene flow together explained 27.3% of variation in contemporary GOs. Populations with higher genetic diversity and more gene flow exhibited lower GOs, consistent with the hypothesis that genetic diversity enhances adaptive capacity and that gene flow may introduce adaptive alleles. Overall, our results support the utility of GO predictions, particularly when validated with independent measures of adaptation, while cautioning against simplistic interpretations of GO as a direct measure of maladaptation in conservation and management contexts.

The climatic oscillations of the Quaternary have likely affected the demographic history of many species, and PSMC (Pairwise Sequentially Markovian Coalescent) has been widely used to investigate these histories. However, it is increasingly acknowledged that PSMC trajectories are difficult to interpret. First, they are influenced by connectivity changes, even without population size changes. Second, most PSMC curves exhibit a few humps when tens of cycles occurred during the Pleistocene. Finally, responses to ancient habitat change have been shown to be species-specific. To address these issues, we simulated structured populations where connectivity (or population size and connectivity) varied according to successive interglacial and glacial periods during the last 2.6 million years. We computed the IICR (Inverse Instantaneous Coalescence Rate), the function that PSMC estimates, and ran PSMC. We further varied the generation length and assumed that some species were positively or negatively affected by glacials. We found that the IICR carries information regarding the demographic oscillations, but that PSMC fails to recover it for times older than 300 ky. For the last 200 ky, PSMC was often able to reproduce qualitatively the demographic oscillations. We also tested SNIF (Structured Non-stationary Inferential Framework), which produced good results using the IICR curve as an input but not when using the PSMC curve. Altogether, our study suggests that the humps older than 300 ky in PSMC histories are unlikely to represent trends of population size or connectivity. However, improving the estimation of the IICR could potentially help reconstruct some of these past demographic changes.

A sudden reduction in population size increases the rate of genetic drift, reducing variability and increasing the mean level of homozygosity. The resulting increased exposure of recessive or partially recessive, strongly deleterious alleles to selection against homozygotes may lead to their being purged from the population, potentially allowing mean fitness to increase after an initial decline, and accelerating the decline in inbreeding depression associated with reduced variability. However, detailed population genetic theory on the effects of population bottlenecks on mean fitness and inbreeding depression remains limited. We develop a theoretical framework for small, randomly mating populations founded from a large population near mutation-selection-drift equilibrium, using both simulations and approximate analytical predictions. These provide quantitative predictions for the dynamics of the populations mean fitness and level of inbreeding depression following a bottleneck. In particular, we derive an approximate expression for the time needed for mean fitness to recover after an initial decline; such a recovery requires selection to be sufficiently strong relative to drift and mutations to be sufficiently recessive. In contrast, weakly deleterious mutations cause reductions in mean fitness and inbreeding depression that are similar in size to those predicted from increases in neutral homozygosity.

Japanese chum salmon supported by one of the world largest hatchery programs have experienced severe declines in marine survival and egg size. To investigate the underlying mechanisms, we analyzed a 21-year time series (1999-2019) of reproductive traits of age-4 chum salmon from 13 rivers together with climate and salmon abundance data using a bootstrap-supported Bayesian network. Here, we assumed that environmental variables can affect the chum salmon populations, but not vice versa, and that there could be maternal effect on reproductive traits, but not the other way around. These constraints enabled us to infer the causal links that shaped the biogeography of North Pacific chum salmon. Global warming caused a decline in Japanese chum salmon abundance, resulting in the increase of the competing Russian chum, which in turn decreased the female body size, fecundity, and egg size of Japanese chum. These findings suggest that climate-driven warming may have exposed genetic effects of hatchery practices, contributing to fitness decline in Japanese chum salmon and the ecological reorganization of chum salmon populations in the North Pacific.

Caenorhabditis nematodes are a powerful model clade for evolutionary genetics. Isogenic lines and panels of recombinant inbred lines (RILs) are among the most essential tools for genetic studies in these species. While most Caenorhabditis species are gonochoristic, large RIL panels have only been developed for self-fertilizing species. This gap biases our understanding and limits our ability to address questions related to the genetic architecture of traits in outbred populations, which have radically higher genetic diversity, heterozygosity, and effective recombination than selfers. Having previously identified Caenorhabditis becei as a tractable gonochoristic species due to its moderate inbreeding depression, we generated two panels of advanced-intercross RILs derived from three individual outbred C. becei worms collected from a single locality on Barro Colorado Island, Panama. One panel derives from a pair of worms sampled from a single rotting fig; the other derives from a cross between worms from two different figs. The panels share one founder in common, yielding two half-sib RIL panels. We sequenced and haplotyped the lines, identifying millions of variants and thousands of recombination breakpoints. Using simulations, we demonstrate the suitability of these lines for quantitative genetics studies and QTL mapping. In our single-fig panel, we observe abundant heritable variation in population growth rate, individual body size, and sexual dimorphism for body size. We detected four QTLs associated with population growth rate and show that estimated allelic effects are good predictors of selection that occurred during panel derivation.

Interest in quantifying linkage disequilibrium (LD, non-random associations of alleles at different loci) has skyrocketed in recent years as researchers have focused on use of LD in genome-wide association studies (GWAS), for studying historical demography, and for estimating effective population size (Ne). The most widely used LD metric is r2 = the squared correlation of alleles at a pair of loci. Despite a half century of efforts, developing an unbiased expectation of r2 as a function of the many factors that can affect it (physical linkage, genetic drift, selection, migration, mutation, mating systems) remains elusive. Furthermore, even when all of these other factors are absent, empirical estimates of r2 are upwardly biased by sampling a finite number (S) of individuals, and that must be accounted for if one wants to focus on the desired signal of LD. Previous approaches to estimate [Formula] have been shown to be biased to greater or lesser degrees. The purpose of this short paper is to demonstrate that a simple and apparently exact expression for [Formula] does exist for the special case where sampling error is the only factor contributing to r2, in which case [Formula] = 1/(S - 1). When other factors contribute heavily to LD, [Formula] shrinks toward 0 as empirical r2 [->] 1. However, for estimating contemporary Ne with unlinked markers, empirical r2 will generally be small and 1/(S - 1) will provide a robust estimate of [Formula].

Infection can substantially reduce host fitness and influence population dynamics, yet it is often difficult to detect and quantify in wild animal populations. Molecular tools offer a valuable means of identifying cryptic infection in natural systems. Using whole-genome bisulfite sequencing, we examined whether infection with the parasitic leech Ozobranchus margoi is associated with DNA methylation variation in loggerhead sea turtles (Caretta caretta), while also assessing the potential value of this variation as a biomarker of parasite infection. In nesting females, we identified infection-associated differentially methylated CpG sites associated with genes implicated in immune signalling and cellular regulation. Offspring of infected females also showed infection-associated methylation patterns, despite not being directly exposed to the parasite themselves. Differential methylation analyses identified genes involved in immunity, neurodevelopment and metabolic activity, with limited overlap in associated genes and no overlap in differentially methylated sites between generations. Maternal and offspring genome-wide methylation levels showed a non-linear association that differed subtly with maternal infection status, indicating that infection modifies intergenerational methylation associations. Finally, methylation profiles showed strong discriminatory power for maternal infection status in both maternal and hatchling samples using machine learning models, supporting their potential as candidate biomarkers of cryptic infection. Together, these results show that parasite infection is associated with distinct, generation-specific DNA methylation signatures, and highlight the potential value of epigenetic data for monitoring cryptic infection states in conservation-relevant systems.

During meiosis, homologous chromosomes pair to form synaptonemal complexes (SCs) and exchange genetic material through a process known as meiotic recombination. First, programmed DNA double-strand breaks form, followed by the assembly of recombination foci on SCs. These foci mark the sites of recombination intermediates and future crossovers. Distributions of recombination foci along SCs have been studied in many eukaryotes, revealing the interplay between recombination patterns and genome evolution. However, in fish, data on recombination patterns are scarce, and, for the majority of groups, completely absent. Here, we measure the positions of MLH1 foci in 3,504 SCs from 219 male meiotic cells of an African annual killifish Nothobranchius virgatus, a representative of a genus with remarkable karyotype and genome diversity, and present a detailed statistical analysis of its recombination patterns. We found that, in contrast to the several other fish species characterised to date, recombination in N. virgatus occurs across almost entire chromosome arms, excluding (peri)centromeres and telomeres. In the longest SCs, we observed a proximal and a distal peak of the recombination focus frequency and explained the peaks by chromosome pairing dynamics. We also revealed the typical positions of focus pairs, demonstrated interference between foci, with the minimal interfocus distance of 4 m, and described regions of the total recombination suppression near centromeres and telomeres. In sum, our study provides a detailed analysis of recombination patterns in a killifish with a fully acrocentric karyotype and contributes to cytogenomic and statistical methodology for future exploration of meiotic recombination patterns.

AbstractsThe Japanese giant salamander (Andrias japonicus), an apex predator and a Special Natural Monument in Japan, is threatened by hybridization with introduced Chinese giant salamanders (Andrias davidianus). This hybridization has caused genetic introgression and expansion of hybrid populations, posing a serious conservation risk. Because morphological identification of hybrids is occasionally unreliable and current genetic methods rely on limited markers, a genome-wide approach is required. However, the extremely large genome ([~]50 Gb) of giant salamanders has hindered whole-genome analyses. In this study, we conducted transcriptome-based analyses of Japanese giant salamanders, Chinese giant salamanders, and their hybrids, generating RNA-seq data from 34 individuals. A total of over 419,000 SNP candidates were identified, from which 4,457 high-confidence SNPs in highly expressed genes were selected for analysis. Population structure analyses for Nabari colony revealed that hybrid individuals form two major groups, corresponding to different degrees of genetic contribution from Japanese and Chinese lineages. Most hybrids were inferred to be F2 or backcross individuals, while F1 hybrids were rare. Mitochondrial analysis indicated that all hybrids possessed Japanese-type mitochondrial genome, suggesting male-mediated introgression from Chinese salamanders. Differential expression analysis revealed enhanced stress-response pathways in hybrids and stronger antiviral responses in Japanese individuals. Using the axolotl genome as a reference, we constructed a virtual chromosomal map, identifying large haplotype blocks and supporting recent hybridization with limited recombination. This study provides a genome-wide framework for understanding hybridization dynamics and supports future conservation and evolutionary studies.

Animals fight for resources to obtain fitness benefits; most contests are intrasexual, and males tend to fight more than females. Although the genetic basis of male aggression is well studied, we know little about the genetic variation of female aggression. Female aggression varies with reproductive status and is potentially influenced not only by her genotype, but also by the genotype of her mate. Here we measured both male and female aggression in a set of Drosophila melanogaster inbred lines by competing each line against a standard competitor. Aggression varied among lines for both sexes, but male and female aggression were not correlated. Female aggression for many lines increased with mating, as expected, but not all lines changed aggression. However, when females were mated to males of different lines, male genotype did not affect the post-mating change in aggression, suggesting that ejaculate-mediated effects do not vary across these lines. The aggression level of the standard opponent was positively correlated with that of focal individuals indicating that individuals modulate their behavior according to the genotype of their opponent.