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When should adaptation arise from a polygenic response versus few large effect changes?

The question of when adaptation involves genetic changes of large effect versus a polygenic response traces back to the foundation of evolutionary biology. While there are compelling reasons to expect polygenic adaptation to be common, direct evidence is still lacking. In turn, there are hundreds of examples of large effect adaptations across species, but it is unclear whether they are a common occurrence in any given species. Synthesizing the different lines of evidence is further complicated by differences in study designs. Here, we reframe this long-standing question in terms of properties of the trait under selection. We ask how the genetic basis of adaptation is expected to depend on key aspects of the genetic variation in the trait and on the extent of changes in selection pressures on it (i.e., the "traits ecology"). We consider a quantitative trait subject to stabilizing selection and model the response to selection when a population at mutation-selection-drift balance experiences a sudden shift in the optimal value. Using this model, we delimit how the contributions of large effect and polygenic changes to adaptation depend on the genetics and ecology of the trait, as well as on other salient factors. We thus formulate testable predictions about when different modes of adaptation are expected and outline a framework within which to interpret disparate sources of evidence about the genetic basis of adaptation.

evolutionary biology↗

Influence of geography, seasonality and experimental selection on Chironomus riparius recombination rates

BackgroundUnderstanding recombination rates is crucial in evolutionary biology, as recombination shapes genetic diversity, natural selection, and adaptation. We investigated recombination rate variation in Chironomus riparius across different latitudes, seasons, and experimental treatments using Pool-seq data from five studies and the ReLERNN neural network-based method. We examined its relationship with genetic diversity, GC content, and FST, assessing causality through structural equation modeling. ResultsIn natural populations, recombination rates showed no clear latitudinal pattern, likely due to interactions between climate-driven selection and regional environmental heterogeneity. However, seasonal variation was evident, with higher recombination rates in autumn than winter, possibly due to temperature-induced plasticity or seasonal bottlenecks. A cold snap in March 2018 triggered a sharp recombination increase, potentially suggesting a stress-induced adaptive response. In experimental populations, thermal regimes had no direct effect on recombination, but adaptation to lab conditions was significant. Environmental stressors produced distinct responses: microplastic exposure reduced recombination genome-wide, likely due to stress-induced DNA repair prioritizing genome integrity, while cadmium exposure generally suppressed recombination. ConclusionsOur findings reveal recombination as a highly dynamic process influenced by environment, selection, and genetic background, underscoring the importance of the context in shaping genomic architecture under both natural and experimental conditions.

evolutionary biology↗

Chromosomal plasticity can drive rapid adaptation in bacteria

Understanding the molecular mechanisms underlying rapid adaptation to stress is a fundamental question in evolutionary biology. A common mechanism is copy number changes, which can affect single genes, larger genomic regions, or even entire chromosomes in the case of eukaryotes (aneuploidy). Bacterial species with genomes comprising more than one chromosome are common, yet the role of adaptive copy number changes affecting entire chromosomes is unknown. Here, by using a bacterium with two chromosomes (chrI and chrII) as model system and combining evolution experiments in the presence of severe nutrient stress with whole-genome sequencing, we show that chromosomal copy number changes can drive rapid adaptation. We detected increased copy number of the entire chrII in almost half of the sequenced clones, isolated from twelve independent populations. In most cases, copy number increases were driven by mutations in the replication protein of chrII. A higher chrII copy number is likely to be beneficial because chrII codes for the operon responsible for metabolizing D-gluconic acid, the only carbon source present in the medium. Our results revealed a novel mechanism for rapid adaptation in bacteria. Given the prevalence of bacteria with secondary chromosomes, and the enrichment of secondary chromosomes in genes associated with interaction with the environment, this may be an important mechanism for adapting to novel environments that has been overlooked.

evolutionary biology↗

Inversion frequencies and phenotypic effects are modulated by the environment

Understanding how environmental variation drives phenotypic diversification within species is a major objective in evolutionary biology. The seaweed fly Coelopa frigida provides an excellent model for the study of genetically driven phenotypes because it carries an /{beta} inversion polymorphism that affects body size. Coelopa frigida inhabits highly variable beds of decomposing seaweed on the coast in Scandinavia thus providing a suitable test ground to investigate the genetic effects of substrate on both the frequency of the inversion (directional selection) and on the phenotype (genotype x environment effects). Here we use a reciprocal transplant experiment to test the effect of the /{beta} inversion on body size traits and development time across four suitable natural breeding substrates from the clinal distribution. We show that while development time is unaffected by GxE effects, both the frequency of the inversion and the relative phenotypic effects of the inversion on body size differ between population x substrate combinations. This indicates that the environment modulates the fitness as well as the phenotypic effects of the inversion karyotypes. It further suggests that the inversion may have accumulated qualitatively different mutations in different populations that interact with the environment. Together our results are consistent with the idea that the inversion in C. frigida likely evolves via a combination of local mutation, GxE effects, and differential fitness of inversion karyotypes in heterogeneous environments.

evolutionary biology↗

Summer rainfall drives adaptation with gene flow in a widespread butterfly

Understanding how environmental variation interacts with gene flow to shape population genomic patterns is a central goal in evolutionary biology. We investigated how geographic and environmental differences impact genomic variation in the clouded sulfur butterfly (Colias philodice eriphyle) by conducting whole-genome resequencing across replicated transects consisting of paired high- and low-elevation sites on both sides of a major mountain range. Despite sampling across steep environmental gradients, we found no evidence of discrete population structure, indicating high connectivity across the region. Nonetheless, significant isolation by distance - strongest in eastern populations - revealed that geographic distance still imposes limits on gene flow, and genetic diversity was also elevated in the east. Genotype-environment association analyses identified more than 16,000 loci associated with elevation, precipitation, and solar radiation. Our redundancy analysis identified precipitation as the strongest predictor of adaptive genomic differentiation, and candidate genes included those linked to melanization and thermoregulation (e.g., TH and yellow). These results demonstrate that even in a largely panmictic population, environmental variation can maintain regional-scale signals of local adaptation. Because insects are declining globally and remain underrepresented in genomic monitoring, conducting whole-genome analyses in a widespread species provides valuable context for assessing how insects today persist across such diverse landscapes and their potential for withstanding future environmental change.

evolutionary biology↗

Reconstructing The Demographic History Of Atlantic Salmon (Salmo salar) Across Its Distribution Range Using Approximate Bayesian Computations

Understanding the dual roles of demographic and selective processes in the buildup of population divergence is one of the most challenging tasks in evolutionary biology. In the Northern hemisphere in particular, species genetic makeup has been largely influenced by severe climatic oscillations of the Quaternary Period. Here, we investigated the demographic history of Atlantic Salmon across the entire species range using 2035 anadromous individuals from 77 sampling sites from North America and Eurasia genotyped at 4,656 SNPs. By combining results from admixture graphs, geogenetic maps and an approximate Bayesian computation framework, we validate previous hypotheses pertaining to secondary contact between European and Northern American populations, but also demonstrate that European populations from different glacial refugia have been exchanging alleles in contemporary times. We further identify the major sources of admixture from the southern range of North America to more northern populations along with a strong signal of secondary gene flow between genetic regional groups. We hypothesize that these patterns reflects the spatial redistribution of ancestral variation across the entire American range. Results also point to a role for linked selection in the form of background selection and or positive hitchhiking. Altogether, differential introgression and linked selective effects likely played an underappreciated role in shaping the genomic landscape of species in the Northern hemisphere Therefore we conclude that such heterogeneity among loci should be systematically integrated into demographic inferences of the divergence process, even between incompletely reproductively isolated populations.

evolutionary biology↗

Indirect genetic effects improve female extra-pair heritability estimates.

The question of why females engage in extra-pair behaviours is long-standing in evolutionary biology. One suggestion is that these behaviors are maintained through pleiotropic effects on male extra-pair behaviors and lifetime reproductive success (genes controlling extra-pair behaviours are shared between sexes, but only beneficial to one, in this case, males). However, for this to occur extra-pair behaviour must be heritable and positively genetically correlated between sexes. Although previous studies have suggested low heritability with no evidence for between-sex genetic correlations in extra-pair behaviours, indirect genetic effects (those derived from the behaviour of others, IGEs) from the social partner, the influence of the social partners genotype on the phenotype of an individual, have not been considered, despite the potential to uncover hidden heritability. Using data from a closed house sparrow population with a genetic pedigree spanning two decades, we tested the influence of IGEs on heritability and genetic correlation estimates of extra-pair behaviour. We found that the inclusion of IGEs improved model fit for both male and female extra-pair heritability. While IGEs did not change between-sex genetic correlations, we found a reduction in uncertainty in our estimates. Future studies should consider the effect of IGEs on the mechanisms of sex specific extra-pair behaviour.

evolutionary biology↗

SLiM 3: Forward genetic simulations beyond the Wright-Fisher model

With the desire to model population genetic processes under increasingly realistic scenarios, forward genetic simulations have become a critical part of the toolbox of modern evolutionary biology. The SLiM forward genetic simulation framework is one of the most powerful and widely used tools in this area. However, its foundation in the Wright-Fisher model has been found to pose an obstacle to implementing many types of models; it is difficult to adapt the Wright-Fisher model, with its many assumptions, to modeling ecologically realistic scenarios such as explicit space, overlapping generations, individual variation in reproduction, density-dependent population regulation, individual variation in dispersal or migration, local extinction and recolonization, mating between subpopulations, age structure, fitness-based survival and hard selection, emergent sex ratios, and so forth. In response to this need, we here introduce SLiM 3, which contains two key advancements aimed at abolishing these limitations. First, the new non-Wright-Fisher or \"nonWF\" model type provides a much more flexible foundation that allows the easy implementation of all of the above scenarios and many more. Second, SLiM 3 adds support for continuous space, including spatial interactions and spatial maps of environmental variables. We provide a conceptual overview of these new features, and present several example models to illustrate their use. These two key features allow SLiM 3 models to go beyond the Wright-Fisher model, opening up new horizons for forward genetic modeling.

evolutionary biology↗

Maternal X chromosome upregulation in both sexes initiates dosage compensation evolution

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100044).\n\nSex chromosomes have repeatedly evolved from a pair of autosomes1. Consequently, X and Y chromosomes initially have similar gene content, but ongoing Y degeneration leads to reduced Y gene expression and eventual Y gene loss. The resulting imbalance in gene expression between Y genes and the rest of the genome is expected to reduce male fitness, especially when protein networks have components from both autosomes and sex chromosomes. A diverse set of dosage compensating mechanisms that alleviates these negative effects has been described in animals2-4. However, the early steps in the evolution of dosage compensation remain unknown and dosage compensation is poorly understood in plants5. Here we show a novel dosage compensation mechanism in the evolutionarily young XY sex determination system of the plant Silene latifolia. Genomic imprinting results in higher expression from the maternal X chromosome in both males and females. This compensates for reduced Y expression in males but results in X overexpression in females and may be detrimental. It could represent a transient early stage in the evolution of dosage compensation. Our finding has striking resemblance to the first stage proposed by Ohno for the evolution of X inactivation in mammals.

evolutionary biology↗

Evolution of genetic (co)variances during the worldwide invasion of Drosophila suzukii

The extent to which phenotypic evolution can be constrained by genetic correlations is an important question in evolutionary biology. To address this question, biological invasions are opportune models where derived, invasive populations can be compared to their extant ancestors, allowing to track the evolution of genetic correlations from the ancestor, throughout the invasion process. In this paper, we focused on the worldwide invasion of Drosophila suzukii (Matsumara, 1931), and investigated the evolution of the genetic covariance matrix G of wing shape between ancestral native, and derived invasive populations. Leveraging demographic history resolved by population genetics approaches, we tested whether G remained stable during the invasion. Using a multivariate QST-FST approach, we further tested whether or not the observed phenotypic divergence in wing shape aligned with a neutral scenario of evolution. Our results show moderate yet significant quantitative genetic differentiation of wing shape among D. suzukii populations and a relative stability in the structure of G, presenting a roughly spherical shape but slightly different volumes. These characteristics likely reflect the demographic history of populations and suggest a low level of genetic constraint on wing shape evolution. The divergence between populations was greater than expected under a purely neutral model of evolution, compatible with an effect of divergent selection among them. Overall, our study suggests that selection and drift, but not ancestral genetic constraints, affected the early stages of wing shape evolution during D. suzukii invasion.

evolutionary biology↗

A Molecular Portrait Of De Novo Genes

New genes, with novel protein functions, can evolve \"from scratch\" out of intergenic sequences. These de novo genes can integrate the cells genetic network and drive important phenotypic innovations. Therefore, identifying de novo genes and understanding how the transition from noncoding to coding occurs are key problems in evolutionary biology. However, identifying de novo genes is a difficult task, hampered by the presence of remote homologs, fast evolving sequences and erroneously annotated protein coding genes. To overcome these limitations, we developed a procedure that handles the usual pitfalls in de novo gene identification and predicted the emergence of 703 de novo genes in 15 yeast species from two genera whose phylogeny spans at least 100 million years of evolution. We established that de novo gene origination is a widespread phenomenon in yeasts, only a few being ultimately maintained by selection. We validated 82 candidates, by providing new translation evidence for 25 of them through mass spectrometry experiments. We also unambiguously identified the mutations that enabled the transition from non-coding to coding for 30 Saccharomyces de novo genes. We found that de novo genes preferentially emerge next to divergent promoters in GC-rich intergenic regions where the probability of finding a fortuitous and transcribed ORF is the highest. We found a more than 3-fold enrichment of de novo genes at recombination hot spots, which are GC-rich and nucleosome-free regions, suggesting that meiotic recombination would be a major driving force of de novo gene emergence in yeasts.

evolutionary biology↗

Sex-allocation trade-offs and their genetic architecture revealed by experimental evolution

The theory of sex-allocation is hailed as one of evolutionary biologys great successes. But while it has successfully predicted strategies of resource allocation to sons versus daughters under a wide range of conditions in species with separate sexes, it has been difficult to apply to hermaphroditic species because of the repeated failure to verify the fundamental assumption of a direct genetic trade-off between male and female allocations made by hermaphrodites. This assumption supposes that mutations that increase an individuals male allocation reduce its female allocation in equal measure, yet there is almost no evidence for such trade-off loci in hermaphroditic populations. Here, we use experimental evolution to generate wide variation in hermaphroditic sex allocation in an annual plant and demonstrate a clear trade-off between the two sexual functions within populations as well as over time, with populations evolving both increased male and reduced female allocation. Quantitative trait locus (QTL) analysis performed on multiple crosses further reveals the segregation of allelic variation at trade-off loci. Taken together, our results demonstrate a phenotypic trade-off in sex allocation in hermaphrodites and provide compelling evidence for sex-allocation trade-off loci, verifying the fundamental assumption of sex-allocation theory and securing its general applicability to both dioecious and hermaphroditic species.

evolutionary biology↗

Common genetic variants shape broad patterns of within-population variation in gene expression.

Understanding the persistence of genetic variation within populations has long been a goal of evolutionary biology. One promising route towards achieving this goal is using population genetic approaches to describe how selection acts on the loci associated with trait variation. Gene expression provides a model trait for addressing the challenge of the maintenance of variation because it can be measured genome-wide without information about how gene expression affects traits. Previous work has shown that loci affecting the expression of nearby genes (local or cis-eQTLs) are under negative selection, but we lack a clear understanding of the selective forces acting on variants that affect the expression of genes in trans. Here, we identify loci that affect gene expression in trans using genomic and transcriptomic data from one population of the obligately outcrossing plant, Capsella grandiflora. The allele frequencies of trans-eQTLs are consistent with stronger negative selection acting on trans-eQTLs than cis-eQTLs, and even more strongly on trans-eQTLs associated with the expression of multiple genes. However, despite this general pattern, we still observe the presence of a trans-eQTL at intermediate frequency that affects the expression of a large number of genes in the same coexpression module. Overall, our work highlights the different selective pressures shaping variation in cis- and trans- gene regulation.

evolutionary biology↗

Phylogenetic comparative methods are problematic when applied to gene trees with speciation and duplication nodes: correcting for biases in testing the ortholog conjecture

How gene function evolves is a central question of evolutionary biology. It can be investigated by comparing functional genomics results between species and between genes. Most comparative studies of functional genomics have used pairwise comparisons. Yet it has been shown that this can provide biased results, since genes, like species, are phylogenetically related. Phylogenetic comparative methods should allow to correct for this, but they depend on strong assumptions, including unbiased tree estimates relative to the hypothesis being tested. Such methods have recently been used to test the "ortholog conjecture", the hypothesis that functional evolution is faster in paralogs than in orthologs. Whereas pairwise comparisons of tissue specificity ({tau}) provided support for the ortholog conjecture, phylogenetic independent contrasts did not. Our reanalysis on the same gene trees identified problems with the time calibration of duplication nodes. We find that the gene trees used suffer from important biases, due to the inclusion of trees with no duplication nodes, to the relative age of speciations and duplications, to systematic differences in branch lengths, and to non-Brownian motion of tissue-specificity on many trees. We find that incorrect implementation of phylogenetic method in empirical gene trees with duplications can be problematic. Controlling for biases allows to successfully use phylogenetic methods to study the evolution of gene function, and provides some support for the ortholog conjecture using three different phylogenetic approaches.

evolutionary biology↗

Regulatory co-option of a homeobox gene drives parasitoid venom evolution

How gene regulatory networks are rewired to generate phenotypic and functional innovation remains a central question in evolutionary biology. Parasitoid wasp venoms provide a powerful system for addressing this question, as their repertoires evolve rapidly through extensive lineage-specific turnover, yet the regulatory principles underlying such flexibility are largely unknown. Here we integrate tissue-resolved transcriptomic, chromatin-accessibility and histone-modification profiling to reconstruct the venom regulatory network of the parasitoid wasp Pteromalus puparum. We show that venom expression is embedded in distinct chromatin states and shaped by regulatory elements associated with venom-gland transcription. Comparative and functional analyses support a general model in which regulators related to the endoplasmic reticulum stress and unfolded protein response pathways have been repeatedly recruited to venom regulation across venomous lineages. Unexpectedly, we identify the recently co-opted homeobox gene Lbx as a lineage-specific hub that regulates more than half of venom genes and is linked to enhancer evolution. These results reveal a nested model of venom regulatory evolution, in which an ancestral secretory programme provides a reusable regulatory backbone, while newly co-opted homeobox gene specify a lineage-specific venom expression. Our study highlights regulatory co-option as a mechanism by which conserved developmental genes can acquire new physiological functions during adaptive evolution.

evolutionary biology↗

Independent origins of fish endothermy converge on a developmental regulatory signature

Why independent origins of the same complex physiological trait repeatedly produce similar body forms and physiological changes remains central in evolutionary biology. Endothermy, the internal production and retention of metabolic heat, evolved at least four times in ray-finned fishes, providing natural replicates for convergent genomic signatures. We present a chromosome-scale analysis of three transitions (opah, tunas, and swordfish), including a new chromosome-level genome of the rare, charismatic Pacific oarfish, analyzed with 31 other teleost genomes. The strongest signal is regulatory: of 253,680 conserved noncoding elements, 577 are rate-accelerated in endothermic lineages, with 67 accelerated in all three, exceeding matched ectothermic controls and enriched near developmental transcription factors and Wnt-signaling genes (e.g., irx1a, irx5a, her9, and lmo1). These elements overlap zebrafish developmental enhancers more than expected by chance but are not tied to genes emphasized by expression or coding-selection studies of endothermic lineages, marking a regulatory layer distinct from that metabolic layer. This convergence is part of a broader mosaic: endothermic lineages also share transition-biased substitution and convergent duplication signatures, including excess tandem duplications and lineage-specific gene-family expansion, whereas chromosome organization and protein-coding sequence change little. Endothermic convergence therefore leaves its clearest signal in regulatory remodeling, alongside shifts in substitution bias and gene-family evolution.

evolutionary biology↗

The dynamics of preferential host switching: host phylogeny as a key predictor of parasite prevalence and distribution

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (https://doi.org/10.24072/pci.evolbiol.100049).\n\nNew parasites commonly arise through host-shifts, where parasites from one host species jump to and become established in a new host species. There is much evidence that the probability of host-shifts decreases with increasing phylogenetic distance between donor and recipient hosts, but the consequences of such preferential host switching remain little explored. We develop a mathematical model to investigate the dynamics of parasite host-shifts in the presence of this phylogenetic distance effect. Host trees evolve under a stochastic birth-death process and parasites co-evolve concurrently on those trees, undergoing host-shifts, co-speciation and extinction. Our model indicates that host trees have a major influence on these dynamics. This applies both to individual trees that evolved under the same stochastic process and to sets of trees that evolved with different macroevolutionary parameters. We predict that trees consisting of a few large clades of host species and those with fast species turnover should harbour more parasites than trees with many small clades and those that diversify more slowly. Within trees, large clades should exhibit a higher infection frequency than small clades. We discuss our results in the light of recent cophylogenetic studies in a wide range of host-parasite systems, including the intracellular bacterium Wolbachia.

evolutionary biology↗

The Tangled History and Taxonomy of an Iconic Chorus Frog Complex Clarified using Genomic Analyses

Species represent a fundamental unit of biodiversity in evolutionary biology, but the nature of the speciation continuum and inadequate sampling of organisms with broad distributions provide substantial challenges to species delimitation. The Pacific Treefrog complex (Pseudacris regilla sensu lato) is an iconic but systematically poorly understood group of chorus frogs inhabiting a vast portion of western North America. Current studies tentatively recognize three species in this complex (P. hypochondriaca, P. regilla, P. sierra), but disagreement remains among morphological, mitochondrial, and nuclear genetic data. In this study, we used thorough geographic sampling and thousands of nuclear loci, along with an integrative, multi-method approach to clarify the phylogenetic relationships and divergence history of P. regilla s.l. lineages and recommend a new taxonomic arrangement for the group. Pseudacris regilla and P. sierra fall firmly within the "gray zone" of speciation, composing a combined "north" lineage. Based on the degree of congruence in inferences from our analyses and evidence for isolating mechanisms, we propose a two species taxonomy for this complex, recognizing the "north" lineage as P. regilla and retaining P. hypochondriaca as a species. Our study shows how extensive geographic sampling, high-throughput sequencing, and multiple analytical approaches can resolve systematic uncertainties in challenging species complexes.

evolutionary biology↗