Evolution Letters

Adaptive phenotypic plasticity can bolster fitness in changing environments, but the extent to which plasticity evolves rapidly, and which forces shape this evolutionary trajectory, is largely unknown. To empirically study the evolution of plasticity we first conducted a replicated field experiment in which Drosophila melanogaster populations adapted to insecticide exposure and a subset of these populations received high diversity assisted gene flow. We then reared individuals from each population across temperature and insecticide treatments in common garden to test the following questions: 1. Has prior selection and rapid adaptation of insecticide resistance led to evolved shifts in plasticity relative to naive populations? 2. Does gene flow from genetically diverse populations contribute to adaptive plasticity evolution relative to gene flow-restricted low diversity populations? Both gene flow and prior evolution of resistance influenced the evolution of plasticity for multiple traits and were often maladaptive for resistant and gene flow-restricted populations, suggesting a trade-off between trait and plasticity evolution. Assisted gene flow minimized maladaptive plasticity potentially through relaxation of underlying epistatic or pleiotropic constraints. Together, these results demonstrate the dynamic interactions between trait evolution, the evolution of plasticity, and forces that shape genetic diversity with implications for conservation of threatened populations.

Does the distribution of fitness effects of new mutations vary across the genome? Under the classical Fisher Geometric Model (FGM) we might not expect it to. In FGM, phenotypic traits are envisioned as dimensions of a landscape, with fitness determined by position in the landscape, i.e., the particular combination of traits of an individual. New mutations are represented by vectors that move from an ancestral to a new phenotype. In classical FGM these vectors affect all trait dimensions simultaneously (universal pleiotropy). However, introducing partial and modular pleiotropy into an FGM framework leads to an expectation that parameters of the DFE will vary with mutational pleiotropy-the number of traits affected by individual mutations. Here we address this prediction by investigating whether traits related to mutational pleiotropy, expression level and network connectivity, affect the parameters of the DFE using whole genome data from A. thaliana and C. grandiflora, two closely related Brassica species that vary significantly in their demography and mating system, and therefore, in effective population size and the effects of linked selection. Results were similar across both species. We found that expression level and network connectivity were predictive of the parameters of the deleterious DFE, even once co-correlations among genome biology traits were accounted for. Our results suggest that, across the genome, molecular evolutio(high mutational pleiotropy). nary patterns agree with the predictions of FGM, albeit relaxing the assumption of universal pleiotropy, and that variation in mutational pleiotropy among genes is sufficient to have detectible effects on the DFE. Significance statementHow do the effects of new mutations vary across the genome? If mutations in some genes affect many traits (high mutational pleiotropy), we hypothesise they will be more strongly deleterious, with lower variance in their selective effects. We test this by investigating the distribution of effects of new mutations across genes that vary in features that are related to mutational pleiotropy: expression level, gene network connectivity, and number of associated GO terms. The mean strength and coefficient of variation of selection of new mutations varied across genes with different features in the manner expected by our hypothesis. This demonstrates that important parameters of molecular evolution can vary across the genome with genome architecture.

While life-history strategies are typically fixed within species, evolutionary transitions between perenniality and annuality can occur. In clonal seagrasses, annual and perennial plants often coexist in the same population, providing a unique model for studying the genetic basis of this transition. Two seagrass Zostera marina populations in South Korea display a striking dichotomy: shallow-water sub-populations follow a typical perennial strategy, whereas their deep-water counterparts are annual. Here we show that this shift from perenniality to annuality, potentially caused by the SAPK7 gene, is genetically coupled with the CAO gene, which is under strong positive selection for low-light adaptation. The up-regulation of the SAPK7 gene triggers early flowering in seedlings, before the formation of any lateral shoots via asexual reproduction. In this special case where the genet contains only one ramet, the post-reproductive death of the ramet is equivalent to the death of the whole genet, which explains the annual phenotype. Our findings reveal a mechanistic example where annuality overcomes perenniality by hitchhiking on a positively selected gene. Given that the ancestral state of plants is perennial, this coupling of annuality with beneficial alleles may represent one of the pathways for the repeated evolution of annual life histories across flowering plants.

Population-specific immunity can drive variation in infection outcomes, but studying immune variation in the wild is challenging because exposure histories are unknown. Comparing wild populations with those reared in a common environment can disentangle genetic and environmental drivers of immunity. We applied this approach in freshwater threespine stickleback, where populations vary in their use of intraperitoneal fibrosis to defend against the helminth parasite Schistocephalus solidus. We combined a 46-lake immune survey with a common garden experiment using 20 representative populations to examine variation in fibrosis and infection. Laboratory assays included exposures to live tapeworms and immune challenges with tapeworm proteins and aluminum phosphate (Alum). We found heritable variation in both constitutive fibrosis and inducible fibrosis. Inducible responses to tapeworms were associated with lake environmental conditions, with fish from more eutrophic-like lakes showing stronger fibrosis induction than those from more oligotrophic-like lakes. Together, these results show how integrating wild immune variation with common garden experiments can reveal novel heritable defenses and link their evolution to ecological variation.

Parasites can alter host populations in fundamentally different ways depending on whether exposure results in infection. Yet, most epidemiological and evolutionary inference focuses on established infections, leaving the fitness consequences of parasite exposure comparatively understudied. This gap is consequential because hosts are frequently exposed to diverse parasite genotypes, and these encounters can impose substantial fitness costs even when infection does not occur. Theory predicts that hosts may mitigate these costs when interacting with commonly encountered parasite genotypes, such that exposure to sympatric parasites incurs lower fitness consequences than exposure to novel, allopatric parasites. Here, we examine the fitness consequences of exposure and infection in the first intermediate host of the trophically transmitted tapeworm Schistocephalus solidus, a cyclopoid copepod that serves as the first host in a three-host life cycle. Using sympatric (Vancouver Island, Canada) and allopatric (Norway) host-parasite combinations, we found a striking reciprocal asymmetry. Sympatric parasites were significantly more infective, yet exposure to sympatric parasites imposed weaker fitness costs when infection did not establish. In contrast, allopatric parasites were less infective, but exposed females produced fewer eggs and had lower hatching success than both controls and females exposed to sympatric parasites, indicating substantial genotype-dependent costs of exposure. Moreover, we found that infection was highly virulent across all genotypes: a single parasite caused near-complete reproductive suppression and reduced host survival across all host-parasite pairings, confirming S. solidus as a castrating parasite in copepods. Together, these results demonstrate that exposure, not just infection, acts as a critical ecological filter with potentially large and underappreciated consequences for host population dynamics and parasite transmission.

O_LIWhen species hybridize, resistance to introgression is presumably due to selection against hybridizing alleles. While many studies have characterized direct selection at these sites, alleles may resist introgression through correlational selection. Here we investigate the role of direct and correlational selection in reducing introgression at the color locus in Ipomoea cordatotriloba. C_LIO_LIWe used recombinant inbred lines that varied in limb color, flower size and sugar concentration to estimate the fitness advantage of the flower color allele via direct and correlational selection. To assess the effect of correlational selection on fitness, we ask if floral size or nectar sugar concentration is correlated with fecundity in pink- but not white-limbed lines. C_LIO_LIWe find no evidence for direct selection on flower color across four fitness components - germination, survival, fecundity, and siring success. Instead, both flower size and sugar concentration significantly correlate with fecundity in pink, but not white limbed lines. As a result, correlational selection on the color allele opposes introgression when recurrent migration is low (<3%). C_LIO_LIThese results demonstrate that correlational, rather than direct, selection is sufficient to resist introgression via hybridization and suggest that correlational selection is an underexplored mechanism to generate resistance to introgression across multiple loci. C_LI

There are some disputed hypotheses for the recurrent observations of insular gigantism and dwarfism, like the island rule: small organisms would become larger on islands, while large organisms would become smaller. But, why is the latter? In addition, not all the observations fit this rule. Here I propose a causal model. Following the Island Biogeography Theory (IBT), insular aspects influence the census N. Observations suggest that variation in N is associated with variation in effective population size (Ne). The body size of insular colonisers might change, following Damuths law, as Ne can decrease at a differential rate from the island area A, resulting in a distinctive effective density [Formula]. Interestingly, a prediction of the drift-barrier hypothesis is that Ne is affecting mutation rates. Consequently, body mass, genome size and {micro} may be predicted to some extent by island area, as they are influenced by De and Ne. Falsification of the latter hypothesis is feasible by determining changes in genomic features of insular species. We now have the opportunity to interrogate the extensive data available. Here I ask: (i) How is decreasing island area predicting average body sizes? (ii) To which levels does this prediction apply (species, cells, genomes)? (iii) How well does the model fare on predicting {micro} over paradigmatic case studies? The resolution of these questions may provide a more reliable diagnosis of the evolutionary causes for somatic size variation. Significance statementNaturalists have long reported that insular species tend to become unusually large or small compared to their mainland relatives. Despite the familiarity of this "island rule", there is still no broad mechanistic explanation for why these changes occur so consistently across different groups of organisms. This work proposes that an important neutral factor can be the change in effective density of isolated populations. By combining the expectations of Damuths law, the IBT model, and the nearly-neutral theory it offers unified predictions on how sudden constraints in island area can influence not only the evolution of body size, but also the direction of changes in genome size and evolutionary rates.

The potential for environmental change to compound the detrimental effects of inbreeding depression in small and isolated populations is a significant concern in conservation biology. Previous evidence syntheses suggested that environmental stress exacerbates inbreeding depression, but were based on limited data. Here, we comprehensively test the relationship between inbreeding depression and environmental stress in natural populations using Bayesian mixed-effects meta-analysis on a large, high-quality data set of 2127 inbreeding depression effect sizes from animals and plants. Our results show that inbreeding depression is significantly higher in benign than in stressful environments. Analyses of both inbreeding depression and stress-induced changes in genetic load supported a unimodal (humped) relationship between the costs of inbreeding and stress intensity, with a peak at intermediate stress. At the highest levels of stress there was, on average, a significantly greater inbreeding load in benign than in stressful environments. We suggest that the lower cost of inbreeding associated with extreme stress results from constraints on the expression of inbreeding depression as fitness and phenotypes decline towards zero. Our findings help to resolve long-standing uncertainty around how inbreeding and environmental change interact, revealing that inbreeding responses vary non-linearly with environmental stress intensity, but showing that stress does not generally amplify inbreeding depression. As such, they will inform both the management of populations of conservation concern and predictions of species responses to global environmental change.

Matching habitat choice provides a mechanism for individuals to maximise their expected fitness by selecting an environment that better fits their phenotype. Many animals choose their local environment by evaluating levels of perceived predation risk against possible resource gain. To test if predation risk is a major driver of habitat choice, we quantify scototaxis, or preference for dark versus light backgrounds, in juvenile guppies. As light backgrounds increase visibility to predators, this aspect of habitat choice captures variation in boldness in small fishes. By rearing and testing 586 fish descended from ten natural populations from Trinidad under common garden conditions, we first quantify (broad sense) heritable variation, i.e. evolutionary potential, within populations. Next, we test for evolutionary divergence among populations in mean preference, and if present, whether ancestral predation regime is a mediator of divergence. Finally, we ask whether families and/or populations differ in the amount of behavioural variation they contain. Habitat choice varied among families (12% of total variance), consistent with heritable variation (0.2). We also found mean preference varies among populations (11% of total variance explained). Evolutionary divergence among-populations is partly explained by ancestral predation regime, with populations from low-predation sites showing a stronger average preference for dark backgrounds than high-predation populations from the same river. Additionally, we find that within-population behavioural variation is greater in high-predation populations. We conclude that guppy populations contain heritable variation that could facilitate adaptive evolution if scototaxis is subject to natural selection. Furthermore, while genetic drift may also contribute to evolutionary divergence among-populations, observed patterns are qualitatively consistent with local adaption to predation regime. Our results suggests that high predation sites favour bolder habitat choice on average, but also that local predation regime shape the evolutionary dynamics of variation, perhaps by maintaining shy-bold variation among-individuals or by favouring individuals with less-predicable behaviour.

Antibiotics impose strong selection on bacteria, resulting in the emergence and spread of antimicrobial resistance. To date, the consequences of resistance evolution for other traits, especially virulence as a key life-history characteristic of high medical relevance remain poorly understood. A central limitation of existing work is reliance on clinical isolates with complex evolutionary histories, hindering causal inferences on resistance-virulence relationships. Such causal information is critical for our understanding of the distribution of resistance-associated evolutionary trade-offs, which may additionally guide optimization of treatment designs. The objectives of our study are to address these knowledge gaps using an experimental evolution framework with the human pathogen Pseudomonas aeruginosa. We quantified changes in resistance, life-history characteristics, in-vivo virulence with a Caenorhabditis elegans infection model, and whole genome sequences for bacterial clones, which had been independently evolved under three antibiotics with distinct cellular targets. We found that the resistance-virulence trade-off depended on the used antibiotic and was additionally driven by the underlying evolutionary path to resistance. Evolved resistance to the fluoroquinolone ciprofloxacin correlated positively with virulence, dependent on genetic changes in either the antibiotic target or efflux regulation. Conversely, evolved resistance to piperacillin/tazobactam, a {beta}-lactam/{beta}-lactamase inhibitor combination, was negatively correlated with virulence, contingent on the coincidental spread of resistance mutations and a large genomic deletion, containing numerous virulence genes. Lastly, evolved resistance to the aminoglycoside streptomycin led to only minor virulence changes. Overall, these antibiotic-specific evolutionary trajectories challenge the assumption of a universal resistance-virulence trade-off and demonstrate that antibiotic choice itself shapes pathogen virulence potential. Significance StatementAntimicrobial resistance and bacterial virulence are typically studied in isolation, yet they are shaped by the same evolutionary pressures and may directly compete for cellular resources. We addressed a fundamental but unresolved question: does evolution of resistance to an antibiotic make a pathogen more or less dangerous to a host? By characterizing experimentally evolved Pseudomonas aeruginosa, a leading cause of drug-resistant infections, we show that the answer depends on which antibiotic drove resistance. A positive resistance-virulence relationship occurred upon adaptation to a fluoroquinolone antibiotic, whereas it was negative upon {beta}-lactam resistance, and unchanged upon aminoglycoside resistance evolution. These antibiotic-specific evolutionary trajectories challenge the assumption of a universal resistance-virulence trade-off and suggest that antibiotic choice shapes pathogen danger beyond drug susceptibility.

Early embryonic development involves the coordination of gene expression from two distinct genomes, as mothers load eggs with gene products prior to the beginning of zygotic transcription. Because the maternal transcriptome is controlled by the mothers regulatory genotype rather than that of the embryo, these two sequential developmental programs may experience distinct evolutionary constraints and selection pressures despite both existing within the embryo. To infer modes of selection on gene expression at maternal and zygotic developmental stages, we used single-embryo RNA-sequencing and conducted variance tests of selection on transcriptomes of parents and F2 segregants of tropical and temperate Drosophila melanogaster embryos. We found that approximately 10% of maternal transcripts and 5% of zygotic transcripts showed signals of selection. Genome-wide, directional selection was more common than stabilizing selection. However, among core early developmental genes and transcription factors, maternal transcription showed patterns of both stabilizing and directional selection, whereas zygotic transcription was predominantly under stabilizing selection. Many heat shock genes showed patterns of directional selection between tropical and temperate embryos, consistent with local adaptation. Additionally, directional selection in piRNA-pathway genes suggests a role for germline defense during embryogenesis. Overall, while our data support the canonical view that core developmental networks are constrained by stabilizing selection, the genome-wide prevalence of directional selection highlights a substantial and previously underappreciated contribution of diversifying selection to the evolution of early development. Article SummaryThe evolution of embryonic gene expression remains poorly characterized on microevolutionary timescales. We conducted genetic crosses between tropical and temperate Drosophila melanogaster, combining single-embryo RNA sequencing with variance tests of selection, to infer patterns of adaptive evolution in gene expression. We found pervasive signals of selection. While core developmental genes were largely under stabilizing selection, directional selection was the predominant mode of selection genome-wide. These findings challenge the paradigm that early embryogenesis is evolutionarily inflexible, suggesting that diversifying selection and local adaptation play key roles in the evolution of development on short evolutionary timescales.

Pleiotropic genes control multiple traits. This can result in evolutionary antagonism because adaptation that favors one trait can interfere with the function of another. While pleiotropic genes show statistical signatures of evolutionary constraint, many of them contain multiple domains that may evolve under different selective pressures. This could either strengthen or alleviate gene-level constraint. Here, we study pleiotropy within the immune system of six Drosophila species to disentangle gene and domain-level evolution. We hypothesized that the multifunctional nature of pleiotropic genes may promote within-gene variation in evolutionary rates of their domains compared to non-pleiotropic genes. Consistently, we found a greater within-gene variation in evolutionary rate among domains of pleiotropic genes than other gene classes, despite relatively low between-gene variation in evolutionary rates among pleiotropic genes. Non-pleiotropic genes, on the other hand, show a more heterogeneous selective pressure at the gene level. Regardless of pleiotropy status, domains within antiviral proteins show elevated evolutionary rates, while signaling protein domains show elevated ratios of radical to conservative amino acid substitutions, which likely have a significant effect on protein structure and function. Finally, an examination of plasticity in infection-induced gene expression responses across species revealed that non-pleiotropic genes with elevated evolutionary rates were also more likely to demonstrate variation in plasticity, but this relationship did not extend to pleiotropic genes. Overall, our results identify differences in evolutionary patterns across various biological levels (i.e., gene, domain, protein, and expression), showing that domain-specific evolution can potentially alleviate gene-level constraints.

The Red Queen Hypothesis proposes that genetic variation is maintained in populations through antagonistic coevolution of hosts and parasites. A major assumption of the Red Queen Hypothesis is tight genetic specificity for infection. However, it has been argued that this genetic interaction of host and parasite (GHxGP) is sensitive to environmental context (GHxGPxE). Environmental change could accordingly disrupt coevolutionary oscillations on relevant time scales, calling into question antagonistic coevolution as a general and robust explanation for the maintenance of genetic diversity. To evaluate this critique, we used the plant-parasitic nematode Meloidogyne arenaria and its natural bacterial parasite Pasteuria penetrans to determine if specificity is altered by temperature. We exposed six isofemale host lines to five parasite sources at three ecologically relevant temperatures. We found that, at two of three temperatures, susceptibility to infection depended on the specific combination of host line and parasite source (GHxGP). This specificity varied across temperatures, consistent with a GHxGPxE effect. This three-way interaction was driven both by quantitative changes in the strength of specificity across temperatures and shifts in the susceptibility rankings of host-parasite combinations. Our study contributes a rare experimental test of a proposed challenge to the Red Queen Hypothesis and suggests the potential for environmental context to change host-parasite specificity.

In androdioecious species like Caenorhabditis elegans, where the primary mode of reproduction is self-fertilization, the evolutionary role of males has long puzzled biologists. One proposed benefit of males is the potential to escape inbreeding depression. We tested this by enforcing seven generations of inbreeding across nine C. elegans strains differing in baseline male frequency and measuring competitive relative fitness before and after inbreeding. We then relaxed inbreeding for four generations to assess recovery. We predicted that strains with higher male frequency, and greater opportunity for outcrossing, would exhibit faster recovery once inbreeding was relaxed. Strains varied substantially in their responses with most showing significant fitness declines and partial recovery but neither the magnitude of inbreeding depression nor the extent of recovery correlated with male frequency. These results show that male frequency is a poor predictor of inbreeding responses and does not reliably reflect realized outcrossing or its fitness consequences.

Conspecific sperm precedence via cryptic female choice is a post-ejaculatory selection process that reduces hybridization, and can be pronounced in sympatric species. In their native Europe, Atlantic salmon (Salmo salar) and brown trout (Salmo trutta) exert conspecific sperm precedence under heterospecific sperm competition, which is at least partially enabled by female reproductive fluid. We examined post-ejaculatory selection of both species in Newfoundland, Canada, where Atlantic salmon evolved in absence of brown trout, but now experience hybridization threats due to anthropogenic introductions. Using split-ejaculate and split-clutch in-vitro fertilizations we evaluated whether allopatric evolution has relaxed this selection in Atlantic salmon, and found that they had no ability to bias paternity towards conspecific males, whereas naturalized brown trout retained a strong ability to do so. Female reproductive fluid influenced this, as when fluid associated with a species eggs was swapped, hybridization increased. In the artificial situation of no female reproductive fluid during sperm competition, paternity changed dramatically, but sperm swimming performance did not predict it. Our findings contribute to understanding the evolution of cryptic female choice and how the mechanisms of reproductive isolation can be reinforced through sympatry, while also highlighting a new potential conservation concern for North American Atlantic salmon.

In most species, unmated individuals run the risk of dying with zero fitness. This strong selection on virgin females to mate may also explain why females subsequently remate, despite fitness costs; all that is required is a genetic correlation between virgin and non-virgin mating propensity. Despite being the null model for the evolution and maintenance of polyandry, this hypothesis has received no empirical test. We performed separate quantitative genetic and artificial selection experiments to test the presence of this cross-context genetic correlation in the cow-pea weevil, Callosobruchus maculatus. A quantitative genetic experiment did not find evidence of the hypothesised genetic correlation. However, after 13 generations of artificial selection on virgin mating latency, we found strong evidence for evolutionary divergence in remating latency. Females from lines selected for longer virgin mating latency took approximately twice as long to remate and, were less polyandrous if their virgin mating latency was longer. There was no evidence that females could mate indiscriminately and then trade-up, rather, trading up could only occur if virgin discrimination was present. Selection against virgin death will thus constrain both the evolution of non-virgin discrimination and trading up, increasing rates of polyandry. These findings reveal a genetic correlation between virgin and non-virgin latency to mate suggesting that polyandry may be maintained because of the need to breed.

Gene regulatory divergence has emerged as a key feature in speciation, influencing gene expression differences that accumulate between diverging populations. Transcriptional regulation, mediated by cis- and trans-acting factors, modulates diverse developmental processes and is responsible for distinct species-specific gene expression profiles. Within interspecies hybrid individuals, negative interactions between divergent cis- and trans-acting factors can lead to gene misregulation and hybrid dysfunction at the organismal level. Such gene regulatory mismatch might disproportionately impact sex-biased and tissue-biased gene regulatory networks due to their unique selective pressures. To address these issues, we investigated the role of regulatory divergence in asymmetric hybrid incompatibility between sister species of Caenorhabditis nematodes (C. remanei, C. latens) by analyzing gene expression of reciprocal hybrids for each sex and key tissue types. Despite severe hybrid male sterility, hybrid males showed less misexpression of sex-biased genes than hybrid females, suggesting that the organismal phenotypic outputs of male-biased gene regulatory networks are more vulnerable to disruption than female-biased genetic networks. Additionally, we found more genes associated with cis- than trans-regulatory divergence, supporting the notion of a disproportionate role for cis-regulatory divergence between species. Moreover, we document extensive cis-trans compensatory X-linked regulatory divergence specifically from male transcriptomes, indicating distinct molecular evolutionary outcomes of stabilizing selection on regulatory controls in males and females. These insights derived from asymmetric hybrid misexpression expand our understanding of the evolution of sex-biased gene regulation in the face of stabilizing selection and identify candidate genes contributing to Caenorhabditis post-zygotic reproductive isolation.

Rapid environmental change and biodiversity loss make it increasingly important to identify factors influencing population extinction risk. Previous studies examining how mating systems can affect persistence of populations under environmental stress generally report higher extinction risks in monogamous than polygynous systems but have largely ignored extra-pair copulations (EPC) and paternity (EPP), despite the prevalence of genetic polyandry in socially monogamous species. Here, using an individual-based model, we study how EPP in socially monogamous systems affects population resilience under directional environmental change. We assume that in socially monogamous species, both sexes carry costly sexual ornaments, the elaboration of which depends on the strength of preference. The effect of EPPs on extinction risk depended on the strength of mate preference, population size, and the degree to which homozygosity affected fitness. Systems with EPCs are not simply intermediate in resilience between strict monogamy and polygyny: the preference strength interacts with mating system, leading to superior resilience of EPC systems compared to strictly monogamous and polygynous systems when choosiness and the negative consequences of heterozygosity loss are low, and EPP rates are high. However, this benefit was reduced in small populations due to faster loss of heterozygosity. At high choosiness, EPC systems exhibited lower resilience than socially polygynous choice systems because the higher reproductive skew of the latter system allowed them to adapt faster while not suffering from the demographic consequences of sexual signaling costs borne by females. Overall, our results suggest that EPCs can enhance population resilience when females obtain fertilizations from higher-condition extra-pair males compared to systems without EPC.

The fitness of immigrants and their descendants determines the effectiveness of gene flow. Genetic incompatibilities or outbreeding depression can limit the spread of novel alleles, while highly fit immigrant lineages can hasten introgression. These fitness effects of gene flow can also differ between generations as immigrant and resident haplotypes recombine. Understanding the genetic factors that shape immigrant fitness over multiple generations is increasingly important as habitat fragmentation threatens populations by reducing genetic variation and leading to increased levels of inbreeding. Few studies have measured the multigenerational fitness of immigrant lineages, especially within populations that had histories of high gene flow. We used 33 years of life history and pedigree data on a population of Florida scrub-jays (Aphelocoma coerulescens) with historically high immigration to quantify the fitness of immigrants and their descendants. We compared the fitness of immigrants and residents as well as their resulting descendants (F1, F2, etc.) to determine the composite genetic effects responsible for fitness differences. We found evidence of additive benefits of immigrant ancestry and heterosis driven by non-additive effects that persists for multiple generations. These results are promising for conservation efforts aiming to increase connectivity and illustrate the complex dynamics that determine the rates of introgression in natural populations.

Bird migration evolved as an adaptation to seasonally changing habitats. Migratory behaviour can vary within the same species in case of partial migratory behaviour, i.e. one population (or individual) is migratory and another one is resident. Species that exhibit a wide variety of migratory phenotypes provide valuable systems to understand the evolutionary drivers behind different phenotypes and how populations adapt to habitats with distinct seasonality. The European robin (Erithacus rubecula) expresses migratory behaviour in central and northern areas of the species distribution range, whereas populations in the South and on the Macaronesian islands are predominantly resident, providing a suitable system to investigate these questions. We use high coverage whole genome re-sequencing data of 125 European robins to investigate how migration behaviour affects population structure and demography, and how it affects the selection landscape in the genome. Genetic structure in European robins coincides with migratory phenotype and geography and populations are characterised by distinct demographic histories. Our results suggest that both the continental resident population as well as the Macaronesian island populations have derived independently from an ancestral migratory population. Unexpectedly, tests for differential selection revealed extensive positive selection pressure acting across all chromosomes in the resident populations, while selective sweeps are largely absent from migrants. We speculate that this might be an analytical artifact due to mismatching timescales between what population genomics methods can detect and the scale on which migration behaviour likely evolved in the robin. We suggest that future studies on the genomics of migration should more focally account for different time scales on which these processes happen, such as including the wider phylogenomic background of the target species, to capture the full evolutionary history of migratory traits.