Invasive species with native ranges spanning strong environmental gradients that establish in new habitats are particularly well-suited for examining the roles of selection and population history in rapid environmental adaptation, providing insight into potential evolutionary responses to climate change. The Atlantic oyster drill (Urosalpinx cinerea) is a marine snail with a native range spanning the strongest marine thermal gradient in the world that has established invasive populations on the U.S. Pacific coast. Here, we leverage this system using genome-wide SNPs and environmental data to examine invasion history and identify genotype-environment associations indicative of local adaptation across its native range, and then assess evidence for predicted allelic frequency shifts signaling rapid adaptation in invasive populations. We demonstrate strong genetic structuring among native regions aligned with life history expectations and identify southern New England as the source of invasive populations. We also identify putatively thermally adaptive loci across the native range, for which two invasive populations show significant divergence from source populations. However, we find no evidence of directional shifts in allele frequencies as would be predicted by environmental selection, suggesting that divergence is likely due to genetic drift rather than rapid adaptation. Alternatively, the success of new populations in environments differing from their origin may be due to relaxed selection pressures associated with more benign conditions, and/or standing capacity for phenotypic plasticity. This demonstrates the utility of invasive species for understanding evolutionary responses to changing environments, and the importance of considering population history and environmental selection pressures when evaluating adaptative capacity.

Adaptation enables natural populations to survive in a changing environment. Understanding the mechanics of adaptation is therefore crucial for learning about the evolution and ecology of natural populations, and for better conservation and management of natural resources such as fish stocks. In this review we focus on the impact of random sweepstakes on selection in highly fecund populations. In random sweepstakes the distribution of individual recruitment success is highly skewed, resulting in a huge variance in the number of offspring contributed by the individuals present in any given generation. We also describe selective sweepstakes which are well approximated by recurrent selective sweeps of strongly beneficial allelic types arising by mutation. We demonstrate that both types of sweepstakes reproduction may facilitate rapid adaptation. Finally, we review an important case study in which a model of recurrent selective sweeps is shown to essentially explain population genomic data of the highly fecund Atlantic cod, with broad implications for studying the evolution and ecology of highly fecund populations across domains of life.

Microevolutionary processes shape adaptive responses to heterogeneous environments, where these effects vary both among and within species. However, it remains largely unknown to which degree signatures of adaptation to environmental drivers can be detected based on the choice of spatial scale and genomic marker. We studied signatures of local adaptation across two levels of spatial extents, investigating complementary types of genomic variants–single nucleotide polymorphisms (SNPs) and polymorphic transposable elements (TEs)–in populations of the alpine model plant species Arabis alpina. We coupled environmental factors, derived from remote sensing digital elevation models at very high resolution (0.5m), with whole-genome sequencing data of 304 individuals across four populations. By comparing putatively adaptive loci detected between each local population versus a regional assessment including all populations simultaneously, we demonstrate that responses of A. alpina to similar amounts of abiotic variation are largely governed by local evolutionary processes. Furthermore, we find minimally overlapping signatures of local adaptation between SNPs and polymorphic TEs. Notably, functional annotations of candidate genes for adaptation revealed several symbiosis-related genes associated with the abiotic factors studied, which could represent selective pressures from biotic agents. Our results highlight the importance of considering different spatial extents and types of genomic polymorphisms when searching for signatures of adaptation to environmental variation. Such insights provide key information on microevolutionary processes and could guide management decisions to mitigate negative impacts of climate change on alpine plant populations.

Fish often spawn eggs with ovarian fluids that have been hypothesized to support sperm of some males over others (cryptic female choice). Alternatively, sperm reactions to ovarian fluids could reveal male strategies. We used wild-caught lake char (Salvelinus umbla) to experimentally test whether sperm react differently to the presence of ovarian fluid, depending on male breeding coloration, male inbreeding coefficients (based of 4,150 SNPs), or the kinship coefficients between males and females. Male coloration was positively linked to body size and current health (based on lymphocytosis and thrombocytosis) but was a poor predictor of inbreeding or kinship coefficients. We found that sperm of more colorful males were faster in diluted ovarian fluids than in water only, while sperm of paler males were faster in water than in ovarian fluids. We then let equal numbers of sperm compete for fertilizations in the presence or absence of ovarian fluids and genetically assigned 1,464 embryos (from 70 experimental trials) to their fathers. The presence of ovarian fluids significantly increased the success of the more colorful competitors. Sperm of less inbred competitors were more successful when tested in water only than in diluted ovarian fluids. The kinship coefficients had no significant effects on sperm traits or fertilization success in the presence of ovarian fluids, although parallel stress tests on embryos had revealed that females would profit more from mating with least related males rather than most colored ones. We conclude that sperm of more colorful males are best adapted to ovarian fluids, and that the observed reaction norms suggest male strategies rather than cryptic female choice.

Several recent publications have stated that epistatic fitness interactions cause the fixation of inversions that suppress recombination among the loci involved. Under this model, however, the suppression of recombination in an inversion heterozygote creates a form of heterozygote advantage, which prevents the inversion from becoming fixed by selection. This process has been explicitly modelled by previous workers.

Processes governing genetic diversity and adaptive potential in reef-building corals are of interest both for fundamental evolutionary biology and for reef conservation. Here, we investigated the possibility of “sweepstakes reproductive success” (SRS) in a broadcast spawning coral Acropora hyacinthus at Yap Island, Micronesia. SRS is an extreme yearly variation in the number of surviving offspring among parents. It is predicted to generate genetically differentiated, low genetic diversity recruit cohorts, containing close kin individuals. We have tested these predictions by comparing genetic composition of size classes (adults and juveniles) at several sites on the island of Yap, Micronesia. We did see the genome-wide dip in genetic diversity in juveniles compared to adults at two of the four sites; however, both adults and juveniles varied in genetic diversity across sites, and there was no detectable genetic structure among juveniles, which does not conform to the classical SRS scenario. Yet, we have identified a pair of juvenile siblings at the site where juveniles had the lowest genetic diversity compared to adults, an observation that is hard to explain without invoking SRS. While further support for SRS is needed to fully settle the issue, we show that incorporating SRS into the Indo-West Pacific coral metapopulation adaptation model had surprisingly little effect on mean rates of coral cover decline during warming. Still, SRS notably increases year-to-year variation in coral cover throughout the simulation.

The major histocompatibility complex (MHC) plays a critical role in the immune response against pathogens. Its high polymorphism is thought to be mainly the consequence of host-pathogen co-evolution, but elucidating the mechanism(s) driving MHC evolution remains challenging for natural populations. We investigated the diversity of MHC class II genes in a wild population of pied flycatchers Ficedula hypoleuca, and tested its associations with two key components of individual fitness: lifetime reproductive success and survival. Among 180 breeding adults in our study population, we found 182 unique MHC class II exon 2 alleles. The alleles showed a strong signal of positive selection and grouped into 9 functional supertypes based on physicochemical properties at the inferred antigen-binding sites. Three supertypes were found in > 98% of the sampled individuals, indicating that they are nearly fixed in the population. We found no rare supertypes in the population, as all supertypes were present in >70% of individuals. Three supertypes were related to different components of individual fitness: two were associated with lower offspring production over time, while the third was positively associated with survival. Overall, the substantial allelic and functional diversity and the relationship between specific supertypes and fitness is in accordance with the notion that balancing selection maintains MHC class II diversity in the study population, possibly with fluctuating selection as the underlying mechanism. The absence of rare supertypes in the population suggests that the balancing selection is not driven by rare-allele advantage.

Adaptation to changing environments often requires meaningful phenotypic modifications to match the current conditions. However, obtaining information about the surroundings during an organism’s own lifetime may only permit accommodating relatively late developmental modifications. Therefore, it may be advantageous to rely on inter-generational or trans-generational cues that provide information about the environment as early as possible to allow development along an optimal trajectory. Transfer of information or resources across generations, known as parental effects, is well documented in animals and plants but not in other eukaryotes, such as fungi. Understanding parental effects and their evolutionary consequences in fungi is of vital importance as they perform crucial ecosystem functions. In this study, we investigated whether parental effects are present in the filamentous fungus Neurospora crassa, how long do they last, are the effects adaptive, and what is their mechanism. We performed a fully factorial match / mismatch experiment for a good and poor quality environment, in which we measured mycelium size of strains that experienced either a matched or mismatched environment in their previous generation. We found a strong silver spoon effect in initial mycelium growth, which lasted for one generation, and increased fitness during competition experiments. By using deletion mutants that lacked key genes in epigenetic processes, we show that epigenetic mechanisms are not involved in this effect. Instead, we show that spore glycogen content, glucose availability and a radical transcription shift in spores are the main mechanisms behind this parental effect.

Feathers comprise a series of evolutionary innovations but also harbor colour, a key biological trait known to co-vary with life history or complex traits. Those relationships are particularly true in melanin-based pigmentation species due to known pleiotropic effects of the melanocortin pathway – originating from melanin-associated phenotypes. Here we explore the molecular basis of melanin coloration and expected co-variation at the molecular level in the melanin-based, colour polymorphic system of the tawny owl (Strix aluco). An extensive body of literature has revealed that grey and brown tawny owl colour morphs differ in a series of life history and behavioral traits. Thus, it is plausible to expect co-variation also at molecular level between colour morphs. To investigate this possibility, we assembled the first draft genome of the species against which we mapped ddRADseq reads from 220 grey and 150 brown morphs - representing 10 years of pedigree data from a population in Southern Finland - and explored genome-wide associations with colour phenotype. Our results revealed putative molecular signatures of cold adaptation strongly associated with the grey phenotype, namely a non-synonymous substitution in MCHR1, plus 2 substitutions in non-coding regions of FTCD and FAM135A whose genotype combinations obtained a predictive power of up to 100% (predicting grey colour). These suggest molecular basis of cold environment adaptations predicted to be grey-morph specific. Our results potentially reveal part of the molecular machinery of melanin-associated phenotypes and provide novel insights towards understanding the functional genomics of colour polymorphism in melanin-based pigmented species.

not-yet-known not-yet-known not-yet-known unknown Invasive species are a major challenge to managers worldwide due to their ability to rapidly change their niche space and behavior in order to reproduce and survive in a novel environment. One globally distributed invasive species, the Pacific oyster, Crassostrea (Magallana) gigas, first arrived in Sweden in 2006. To date, they have not colonized the low salinity waters of the Baltic Sea, and it has generally been assumed that the inability of Pacific oysters to reproduce in low salinities has acted as a barrier. We have studied differences in fertilization rates among oysters along the invasion range, and examined heritability of salinity tolerance through classic mating designs across five different salinity levels. We found that fertilization rates in low salinities increased with proximity to the range front, and that there was a strong heritable component to these differences. We then used whole genome sequence data to identify genomic regions that diverged significantly from expected Mendelian inheritance in larval full-sib families that survived in low salinities. Our results show that a chromosomal region containing coding sequences for all histones forming the nucleosome, as well as a region containing LSU and SSU subunit ribosomal DNA in the sperm, are involved in low-salinity tolerance at fertilization and early development. We also found no evidence of recent bottlenecks or reductions in genetic diversity along the invasion front compared to more established populations. We therefore conclude that the Pacific oyster has the potential to adapt further to low-salinity conditions and may invade the Baltic Sea.

Genetic analyses of host-specific parasites can elucidate the evolutionary histories and biological features of their hosts. Here, we used population-genomic analyses of ectoparasitic seal lice (Echinophthirius horridus) to shed light on the postglacial history of seals in the Arctic Ocean and the Baltic Sea region. One key question was the enigmatic origin of relict landlocked ringed seal populations in lakes Saimaa and Ladoga in northern Europe. We found that that lice of four postglacially diverged subspecies of the ringed seal (Pusa hispida) and Baltic gray seal (Halichoerus grypus), like their hosts, form genetically differentiated entities. Using coalescent-based demographic inference, we show that the sequence of divergences of the louse populations is consistent with the geological history of lake formation. In addition, local effective population sizes of the lice are generally proportional to the census sizes of their respective seal host populations. Genome-based reconstructions of long-term effective population sizes revealed clear differences among louse populations associated with gray vs. ringed seals, with apparent links to Pleistocene and Holocene climatic variation as well as to the isolation histories of ringed seal subspecies. Interestingly, our analyses also revealed ancient gene flow between the lice of Baltic gray and ringed seals, suggesting that the distributions of Baltic seals overlapped to a greater extent in the past than is the case today. Taken together, our results demonstrate how genomic information from specialized parasites with higher mutation and substitution rates than their hosts can potentially illuminate finer scale population genetic patterns than similar data from their hosts.

In response to global climate change, numerous taxa are expanding their living ranges. In species with highly migratory aptitudes such as sea turtles, this expansion may be driven by individuals either from nearby or distant areas. Recent observations suggest a range expansion of the philopatric green turtle (Chelonia mydas) to the central and western Mediterranean. To assess the origin of the turtles found in these novel habitats, we first built a genomic baseline, using 2bRAD sequencing on individuals from regular nesting areas in three Regional Management Units (RMU): North Atlantic, South Atlantic and Mediterranean (5 individuals from each RMU). Secondly, we compared this baseline with genotyped hatchlings from three nests laid in new Mediterranean sites and four mature-size green turtles tagged with satellite telemetry in the western Mediterranean basin. Our analyses revealed that the nest in Tunisia was sired by turtles from the South Atlantic RMU, while the two nests in Crete were sired by turtles from the Mediterranean RMU. In addition, the three adult turtles sampled in southwestern Mediterranean were genetically assigned to the South Atlantic RMU while the remaining individual within reproductive size, sampled in northwestern Mediterranean, was genetically assigned to the Mediterranean RMU. These results suggest a simultaneous potential colonisation by two distant regions. We propose that the range expansion of green turtles into the central and western Mediterranean, as also already observed in loggerhead turtles (Caretta caretta), is likely driven by climate change and these populations may become globally important as temperatures continue to increase.

Ecological differences among species influence population response to historical environmental changes, and genetic simulations now allow us to directly incorporate this variation into inferential models. However, the impact of life history strategies in demographic inference has been far less explored relative to the impact of other ecological differences, such as dispersal capacity and habitat preference. Here, we utilize individual-based simulations of a non-Wright-Fisher population to ask whether differences in the average age of first reproduction of individuals, the average adult mortality and the average number of mates per reproductive season lead to consistent and predictable differences in summary statistics of genetic diversity commonly used for simulation-based parameter estimation and demographic inference. Using a Random Forest model, we estimate three population parameters (variance in reproductive success, generation time, and effective population size) from genome-wide SNP variation for two bird species with distinct life history strategies that are directly built into the simulation machinery. Our results show that life history variation leads to predictable differences in patterns of genetic diversity. While prediction accuracy is low, parameter estimates from empirical datasets agree with the expectation that species with extreme polygamy, long adult longevity and later onset of reproduction will exhibit higher variance in reproductive success, longer generation time and smaller effective population sizes. Since the signal of life history differences is observed in the genetic summary statistics, we suggest that simulation- and model-based multi-species demographic inference should incorporate life history parameters.

Plants adapt to their local environment through complex interactions between genes, gene networks, and hormones. Although the impact of gene expression on trait regulation and evolution has been recognized for many decades, its role in the evolution of adaptation is still a subject of intense exploration. We used a Multi-parent Advanced Generation Inter-Cross (MAGIC) population, which we derived from crossing multiple parents from two distinct coastal ecotypes of an Australia wildflower, Senecio lautus. We focused on studying the contrasting gravitropic behaviors of these ecotypes, which have evolved independently multiple times and show strong responses to natural selection in field experiments, emphasizing the role of natural selection in their evolution. Here, we investigated how gene expression differences have contributed to the adaptive evolution of gravitropism. We studied gene expression in 600 pools at five time points (30, 60, 120, 240, and 480 minutes) after rotating half of the pools 90°. We found 428 genes with differential expression in response to the 90° rotation treatment. Of these, 81 genes (~19%) have predicted functions related to the plant hormones auxin and ethylene, which are crucial for the gravitropic response. By combining insights from Arabidopsis mutant studies and analyzing our gene networks, we propose a preliminary model to explain the differences in gravitropism between ecotypes. This model suggests that the differences arise from changes in the transport and availability of the hormones auxin and ethylene. Our findings indicate that the genetic basis of adaptation involves interconnected signaling pathways that work together to give rise to new ecotypes.

not-yet-known not-yet-known not-yet-known unknown How species boundaries are maintained among sympatric closely related species experiencing gene flow is a puzzling question in evolutionary biology. Although introgression is commonly documented, the dynamics and gene function of introgression have rarely been explored to probe why frequent introgression does not necessarily destroy species boundaries in sympatry. In this study, we employ whole-genome resequencing data to examine introgression among five closely related species of Roscoea that co-exist in a “sky island” with seventeen distinct morphological traits. Our findings reveal that introgression has led to the phylogenomic discordance between nuclear and chloroplast genomes among these morphologically distinct species. Additionally, introgression is predominantly asymmetrical in both intensity and gene function, particularly concerning recombination. Notably, the majority of gene functions associated with introgressed loci are unrelated to reproductive processes. Our results suggest that closely related species with incomplete allele assortment can coexist despite theoretical predictions, highlighting the semipermeable nature of species boundaries as reproductive isolation develops. This provides a critical conceptual framework for understanding the interplay between introgression and species persistence. Our finding offers insights into how related sympatric species boundaries can be maintained in the face of frequent asymmetrical gene introgression.

Understanding speciation is a fundamental goal in evolutionary biology. Genomic regions of accentuated differentiation among populations often reveal patterns and mechanisms of species formation. While substantial progress has been achieved on this front for genetic variation, the contribution of epigenetic mechanisms to divergence patterns remains unclear. Here, we present evidence that DNA methylation is associated with regions exhibiting accentuated genetic differentiation between populations of Timema cristinae stick insects. We do so by integrating analyses of differentially methylated regions (DMRs) between individuals from different host-plant species with genomic sequencing. Our results reveal that DMRs exhibit accentuated genetic differentiation (FST) between populations. Strikingly, the strength of this association increases with the geographical distance between populations. We present results evaluating the contributions of mutation, reduced recombination, gene flow and selection to these divergence patterns. The overall results are consistent with a role for a balance between selection and gene flow, a finding further supported by evidence for selection in a previously-published survival field experiment. Nevertheless, details of our results suggest that selection on DMRs might be indirect and not strictly host-related. Our results establish associations between methylation and genetic change, but further work is required to clarify the exact causes of this association. Nonetheless, our results provide insight into how the interplay of epigenetic and genetic variation may influence population divergence and potentially contribute to speciation.

Pollinators harbour diverse RNA viromes that play a vital role in their health. Yet, factors that shape viral communities are often unclear. The European honey bee (Apis mellifera) is experiencing a viral epidemic since the emergence of the parasitic mite Varroa destructor (varroa) introduced vector-borne transmission, which has also been linked to increased viral spillover into wild pollinator communities. Varroa-free island populations provide natural laboratories to study the effect of varroa, while also allowing us to ask how islands affect viral communities. Barriers that restrict the dispersal of wild pollinators and their pathogens to islands may be overcome by human-mediated transport in managed honey bees. In this study, we used islands with and without varroa and matched mainland populations of honey bees (A. mellifera) and bumble bees (Bombus terrestris) from 2015 and 2021 to explore how varroa presence and island location affect the virome of managed and wild bees. We find lower viral richness on islands in both species. Bumble bee viromes were not affected by varroa and showed a distinct community that was geographically structured. In honey bees, however, viral abundance was more evenly distributed on varroa-free islands but dominated by deformed wing virus (DWV) in varroa-present populations. Within the six years between the sampling events, DWV underwent a shift from DWV-B towards recombinant strains. Surprisingly, these shifts appeared independent of varroa. Viewing pollinator virome composition within an ecological framework provides valuable insights into the barriers to virus spread and could help to predict drivers of disease emergence.

European (Anguilla anguilla) and American eel (A. rostrata) represent a remarkable case of interspecific hybridization. They are both panmictic and spawn in partial sympatry in the Sargasso Sea, occasionally producing viable, fertile hybrids, primarily found in Iceland. We studied introgressive hybridization from American into European eel based on whole-genome sequences of 78 individuals, encompassing European, American and 21 putative hybrid eels. Previous studies using few genetic markers could not resolve whether hybridization involved simple unidirectional backcrossing or a more complex hybrid swarm scenario. However, local ancestry inference along individual chromosomes revealed Icelandic hybrids were primarily F1 hybrids or first-generation backcrosses toward European eel, with a few showing more complex backcrossing histories. All European eels outside Iceland contained short chromosomal blocks from American eel, indicating a porous genome. We found no evidence for previously stated hypotheses about geographical gradients of introgression in European eel outside Iceland. Several chromosomal regions showed high divergence between the species, but haplotype blocks introgressed from American eel were identified both within and outside these regions. There was little correspondence between regions of high relative and high absolute divergence (dXY), and they presumably reflect selective sweeps within species or regions of reduced recombination rather than barrier loci. We identified a single genomic region with evidence of introgression from American into European eel at multiple occasions, under positive selection in both species. Thus, although the two species maintain genetic integrity, their gene pools are not independent and represent a common pool of standing variation for future adaptive responses.