Biology subjects

Arnqvist, G.

Publications and source records attributed to Arnqvist, G..

11 recordsLinked to original sources

bioRxiv2026

Experimental evolution unveils a role for structural variants and sex-specificity in the genetic architecture of lifespan

Insights into the genetic basis of lifespan evolution can link evolutionary theory with an understanding of health, disease and adaptation. We leverage the power of >200 generations of experimental evolution in a seed beetle to unveil the genomic architecture of lifespan evolution. Replicated populations evolved under regimes favoring either a short or long life, resulting in a near doubling of lifespan. Whole genome re-sequencing revealed that short- and long-lived lines were strongly differentiated (global FST = 0.41) and more than 700 genes showed consistent signs of divergent selection. Remarkably, short- and long-lived lines were consistently divergent in a large number of regions harboring copy-number variants (CNVs), involving >600 genes. The evolution of a long life involved many distinct biological processes, such as DNA fidelity, mitotic integrity, reproduction, metabolism, immunity and stress response. A pedigree-based genome scan for quantitative trait loci (QTLs) uncovered several QTLs with large effects on lifespan, but the genetic basis of a long life was dominated by a very large number of regions with medium and small effects. The genome-wide spatial association with QTL effects was, if anything, stronger for CNVs than for sequence variants. The genetic effects of QTLs on lifespan were positively correlated overall between the sexes, but four regions showed pronounced sex-differences. Our results show that structural variants play a significant role in the evolution of an extended lifespan and the highly polygenic genomic architecture is to some extent sex-specific, consistent with differences in physiology and life history tradeoffs between the sexes.

evolutionary biology↗

bioRxiv2026

Sex-specific dominance maintains multilocus polymorphism and can resolve sexual conflict

Sexually antagonistic selection arises when females and males favour different phenotypes but share their genetic basis. Beneficial sex-specific dominance can alleviate this conflict by allowing each allele to be more dominant in the sex in which it is beneficial. Whether the coevolution of dominance and allelic diversity can generate and maintain polymorphism across a polygenic trait remains unclear. We investigate a quantitative trait encoded by multiple diploid loci, with allelic effects shared between the sexes and evolving sex-specific promoter affinities determining dominance. We show that sex-specific dominance can generate polymorphism across many loci, including under weak or asymmetric selection. Whereas additive allelic effects lead to the concentration of polymorphism at a single major locus, evolving dominance allows polymorphism to become distributed across loci. This distributed polygenic architecture generates sexual dimorphism while reducing within-sex phenotypic variance: increasing the number of polymorphic loci, as well as allelic diversity within loci, allows female and male phenotypes to approach their respective optima with lower segregation load. Sufficiently strong selection can instead cause polymorphism to collapse toward a single major locus, but the selection strength required for this transition increases sharply with the number of contributing loci. Thus, evolving sex-specific dominance can make widespread genetic polymorphism part of the resolution of sexual conflict.

evolutionary biology↗

bioRxiv2025

Sign epistasis extends the effects of balancing selection on genetic diversity

Balancing selection, a form of selection that maintains genetic diversity, is difficult to detect, and the importance of balancing selection for the maintenance of genetic variation may be larger than often assumed. We model the possibility that the diversity-promoting effects of balancing selection extend to other loci that show sign epistasis with a locus under balancing selection. Rather than focusing on overdominance, as was done in previous efforts, we explore the effects of negative frequency dependence and show that this has important effects on the conditions under which the diversity-promoting effect of epistasis can occur in diploids. Our results show that not only recombination rate but also the dominance of sign epistasis are key parameters that determine the maintenance of polymorphism beyond the locus under direct balancing selection. We suggest that the effect we explore may play a significant role, especially when balancing selection acts on major effect loci.

evolutionary biology↗

bioRxiv2024

Sex-specific dominance and its effects on allelic diversity in sexually antagonistic loci

Sexually antagonistic (SA) selection can promote genetic diversity. Current theory predicts biallelic polymorphism in SA loci primarily under strong selection or dominance reversal between the sexes. Yet, selection is often weak, several candidate SA loci harbour more than two alleles, and the prevalence of dominance reversal remains unclear. We present a model in which allelic effects at a quantitative-trait locus coevolve with sex-specific promoter affinities that determine allelic dominance, under distinct female and male phenotypic optima. We show that gradual coevolution between allelic values and promoter affinities can generate a positive feedback between beneficial sex-specific dominance and allelic divergence. Importantly, this feedback does not require an established balanced polymorphism, but can be initiated during selective sweeps, during evolutionarily transient protected polymorphism, or from variation maintained by mutation-selection-drift balance. Under weak or asymmetric selection, repeated diversification can generate polyallelic polymorphism, with several alleles forming dominance hierarchies that reduce segregation load. These results hold for both autosomal and X-linked loci and do not require complete dominance reversal. To assess these findings, we analyse segregating genetic variation in three insect populations and find stronger signals of polyallelic polymorphism in candidate SA loci and those showing sex-specific dominance, while genes with the strongest signals are enriched for functions associated with known SA phenotypes.

evolutionary biology↗

bioRxiv2024

A shared genetic basis for sexually antagonistic male and female adaptations in the toothed water strider

Sexual conflict can drive the divergence of male and female phenotypes and several cross-species comparative analyses have documented patterns of correlated evolution of sex-specific traits that promote the evolutionary interests of the sexes. However, male-female coevolution can be highly dynamic. Moreover, if male and female traits do not have an entirely distinct genetic basis, this can have profound effects on their coevolutionary dynamics. Here, we use water striders, a well-studied model system for sexually antagonistic coevolution, and ask whether sex-specific phenotypic adaptations covary across populations and whether they share a common developmental genetic basis. Using comparative analyses both at the population and species levels, we document an association between a derived male mate-grasping trait and a likely female anti-grasping counteradaptation in the toothed water strider Gerris odontogaster. Interestingly, in one population where males did not express their derived grasping trait, females had also regained the ancestral morphology. We then used experimental manipulation of gene expression, and show that these male and female traits are both linked to a common developmental genetic program containing Hox and sex determination genes, despite the fact that they are different structures on different segments. Our work thus suggests that the pleiotropic nature of developmental genetic programs can blur the distinction between inter- and intralocus genetic conflict.

evolutionary biology↗

bioRxiv2022

A possible genomic footprint of polygenic adaptation on population divergence in seed beetles?

Efforts to unravel the genomic basis of incipient speciation are hampered by a mismatch between our toolkit and our understanding of the ecology and genetics of adaptation. While the former is focused on detecting selective sweeps involving few independently acting or linked speciation genes, the latter states that divergence typically occurs in polygenic traits under stabilizing selection. Here, we ask whether a role of stabilizing selection on polygenic traits in population divergence may be unveiled by using a phenotypically informed integrative approach, based on genome-wide variation segregating in divergent populations. We compare three divergent populations of seed beetles (Callosobruchus maculatus) where previous work has demonstrated a prominent role for stabilizing selection on, and population divergence in, key life history traits that reflect rate-dependent metabolic processes. We derive and assess predictions regarding the expected pattern of covariation between genetic variation segregating within populations and genetic differentiation between populations. Population differentiation was considerable (mean FST = 0.23 - 0.26) and was primarily built by genes showing high selective constraints and an imbalance in inferred selection in different populations (positive Tajimas DNS in one and negative in one) and this set of genes was enriched with genes with a metabolic function. Repeatability of relative population differentiation was low at the level of individual genes but higher at the level of broad functional classes, again spotlighting metabolic genes. Absolute differentiation (dXY) showed a very different general pattern at this scale of divergence, more consistent with an important role for genetic drift. Although our exploration is consistent with stabilizing selection on polygenic metabolic phenotypes as an important engine of genome-wide relative population divergence and incipient speciation in our study system, we note that it is exceedingly difficult to firmly exclude other scenarios.

evolutionary biology↗

bioRxiv2020

Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

BackgroundSexual selection can have major effects on mating rates and sex-specific costs of mating and may thereby influence sex-differences in immunity as well as associated host-pathogen dynamics. Yet, experimental evidence linking the mating system to evolved sexual dimorphism in immunity are scarce and the direct effects of mating rate on immunity are not well established. Here, we use transcriptomic analyses, experimental evolution and phylogenetic comparative methods to study the association between the mating system and sexual dimorphism in immunity in seed beetles, where mating causes internal injuries in females. ResultsWe demonstrate that female phenoloxidase (PO) activity, involved in wound healing and defence against parasitic infections, is elevated relative to males. This difference is accompanied by concomitant sex-differences in the expression of genes in the pro-phenoloxidase activating cascade. We document substantial phenotypic plasticity in female PO activity in response to mating and show that experimental evolution under enforced monogamy (resulting in low remating rates and sexual conflict relative to natural polygamy) rapidly decreases female (but not male) PO activity. Moreover, monogamous females have evolved increased tolerance to bacterial infection unrelated to mating, implying that female responses to costly mating may trade off with other aspects of immune defence, an hypothesis which broadly accords with the documented sex differences in gene expression. Finally, female (but not male) PO activity shows correlated evolution with the perceived harmfulness of male genitalia across 12 species of seed beetles, suggesting that sexual conflict has a significant influence on sexual dimorphisms in immunity in this group of insects. ConclusionsOur study provides insights into the links between sexual conflict and sexual dimorphism in immunity at the molecular and phenotypic level and suggests that selection pressures moulded by mating interactions can lead to a sex-specific mosaic of immune responses with important implications for host-pathogen dynamics in sexually reproducing organisms.

evolutionary biology↗

bioRxiv2020

Selection in males purges the standing genetic load on female fitness

Theory predicts that the ability of selection and recombination to purge mutation load is enhanced if selection against deleterious genetic variants operates more strongly in males than females. However, direct empirical support for this tenet is limited, in part because traditional quantitative genetic approaches allow dominance and intermediate-frequency polymorphisms to obscure the effects of the many rare and partially recessive deleterious alleles that make up the main part of a populations mutation load. Here, we exposed the partially recessive genetic load of a population of Callosobruchus maculatus seed beetles via successive generations of inbreeding, and quantified its effects by measuring heterosis - the increase in fitness experienced when masking the effects of deleterious alleles by heterozygosity - in a fully factorial sex-specific diallel cross among 16 inbred strains. Competitive lifetime reproductive success (i.e. fitness) was measured in male and female outcrossed F1s as well as inbred parental selfs, and we estimated the 4x4 male-female inbred-outbred genetic covariance matrix for fitness using Bayesian Markov chain Monte Carlo simulations of a custom-made general linear mixed effects model. We found that heterosis estimated independently in males and females was highly genetically correlated among strains, and that heterosis was strongly negatively genetically correlated to outbred male, but not female, fitness. This suggests that genetic variation for fitness in males, but not in females, reflects the amount of (partially) recessive deleterious alleles segregating at mutation-selection balance in this population. The populations mutation load therefore has greater potential to be purged via selection in males. These findings contribute to our understanding of the prevalence of sexual reproduction in nature and the maintenance of genetic variation in fitness-related traits. Impact statementWhy do the large majority of eukaryotic species reproduce sexually if it means that females must spend half of their reproductive effort producing males, while males contribute few or no resources to offspring production themselves? In principle, a lineage of a mutant asexual female that simply clones herself into daughters would grow at twice the rate of her sexual competitors (all else equal). What prevents this from being the predominant mode of reproduction throughout eukaryotes? One hypothesis regards the role of males in facilitating the purging of deleterious mutations from the populations genome since very strong selection in males, unlike selection in females, can occur in many species without reductions in population offspring numbers. Due to the inherent difficulties of isolating this source of standing genetic variation for fitness, empirical evidence for this theory is mixed and limited to indirect evidence from manipulative experiments and experimental evolution studies. Here we demonstrate that recessive deleterious alleles in a population of the seed beetle, Callosobruchus maculatus, are selected against strongly in males but not females. Using a fully factorial diallel cross among 16 inbred strains, we measured the degree to which fitness in the outbred offspring of those crosses improved relative to their inbred parents. This measure is known as heterosis and offers an estimate of the relative amount of partially recessive deleterious alleles carried by a genetic strain. We then analyzed the relationship between the strains heterosis values and their additive genetic breeding values for fitness measured in males and females, revealing the extent to which segregating (partially recessive) deleterious alleles are selected against in males and females. We found that a strains heterosis value was strongly genetically correlated with its additive genetic breeding value for male fitness, but not female fitness. This suggests that mutations with deleterious effects on population growth rate due to their effects on females can be selected against (i.e. purged) more efficiently via their male siblings. This process would offer a benefit to sexual reproduction that may partly compensate for its costs, and therefore yields insight to the prevalence of sex in nature.

evolutionary biology↗

bioRxiv2018

Sexual selection, environmental robustness and evolutionary demography of maladapted populations: a test using experimental evolution in seed beetles.

Whether sexual selection impedes or aids adaptation has become a pressing question in times of rapid environmental change and parallels the debate about how the evolution of individual traits impacts on population dynamics and viability. The net effect of sexual selection on population viability results from a balance between genetic benefits of \"good genes\" effects and costs of sexual conflict. Depending on how these facets of sexual selection are affected under environmental change, extinction of maladapted populations could either be avoided or accelerated. Here, we evolved seed beetles under three alternative mating regimes (polygamy, monogamy and male-limited selection) to disentangle the contributions of sexual selection, fecundity selection and male-female coevolution to individual reproductive success and population fitness. We compared these contributions between the ancestral environment and two new stressful environments (temperature and host plant shift). Evolution under polygamy resulted in the highest individual reproductive success in competitive context for both sexes. Moreover, females evolving only via sexual selection on their male siblings in the male-limited regime had similar reproductive success and higher fertility than females evolving under monogamy, suggesting that sexual selection on males had positive effects on female fitness components. Interestingly, male-limited sexual selection resulted in males that were robust to stress, compared to males from the two evolution regimes applying fecundity selection. We quantified the population-level consequences of this sex-specific adaptation and found evidence that costs of socio-sexual interactions were higher in male-limited lines compared to polygamous lines, and that this difference was particularly pronounced at elevated temperature to which males from the male-limited regime were more robust compared to their conspecific females. These results illustrate the tension between individual-level adaptation and population-level viability in sexually reproducing species and suggest that sex-specific selection can cause differences in environmental robustness that may impact population demography under environmental change.

evolutionary biology↗

bioRxiv2018

The efficacy of sexual selection under environmental change

Sexual selection can promote adaptation if sexually selected traits are reliable indicators of genetic quality. Moreover, stronger sexual selection in males, as often reported in empirical studies, may help purge deleterious alleles at a low cost to population productivity. However, to what extent this remains true when a changing environment affects sexual selection dynamics has been debated. Here, we show that even if sexually selected traits remain honest signals of male quality in new environments, the efficacy of sexual selection will often be reduced under stress. We model the strength of sex-specific selection under different levels of environmental stress in a population in which males compete with each other for fertilization success and in which females experience fecundity selection. We observe that the strength of sexual selection is reduced relative to fecundity selection, resulting in a lowered potential for selection on males to aid adaptation under environmental change.

evolutionary biology↗

bioRxiv2017

Postmating sexual selection and the enigmatic jawed genitalia of Callosobruchus subinnotatus

Insect genitalia exhibit rapid divergent evolution. Truly extraordinary structures have evolved in some groups, presumably as a result of post-mating sexual selection. To increase our understanding of this phenomenon, we studied the function of one such structure. The male genitalia of Callosobruchus subinnotatus (Coleoptera: Bruchinae) contain a pair of jaw-like structures with unknown function. Here, we used phenotypic engineering to ablate the teeth on these jaws. We then experimentally assessed the effects of ablation of the genital jaws on mating duration, ejaculate weight, male fertilization success and female fecundity, using a double-mating experimental design. We predicted that copulatory wounding in females should be positively related to male fertilization success. However, we found no significant correlation between genital tract scarring in females and male fertilization success. Male fertilization success was, however, positively related to the amount of ejaculate transferred by males and negatively related to female ejaculate dumping. Ablation of male genital jaws did not affect male relative fertilization success but resulted in a reduction in female egg production. Our results suggest that postmating sexual selection in males indeed favors these genital jaws, but not primarily through an elevated relative success in sperm competition but by increasing female egg production.

evolutionary biology↗