Evolution Letters

A populations ability to adapt is determined by its levels of additive genetic variance (VA), and while it is agreed that most organisms have genetic variation for most traits, the extent to which it varies between species is poorly characterised. Here we investigate this question by compiling 3209 and 1852 estimates of heritability and evolvability (the additive genetic variance divided by the square of the mean) estimates respectively, for a variety of traits, from 220 and 172 multicellular eukaryotic species. Using phylogenetic generalised linear mixed models, we find substantial and highly significant interspecific variation in evolvability. Much of the variation is explained by phylogenetic relatedness, with plants in our data having substantially higher evolvability than animals. While heritability also varies between species, the differences are more subtle, and plants are not exceptional. We investigate whether the variation in evolvability and heritability between species is due to variation in the mutation rate, effective population size, genome size, ploidy and recombination rate, but find little evidence of any factor being important. However, the confidence intervals are large suggesting that we have little power to detect any associations between these factors and our estimates of VA.

Parasite defense is the ability of a host to minimize fitness loss to parasites, and it is among the most variable phenotypes in natural populations. We expect this variation in defense to facilitate rapid adaptation under parasite-mediated selection. What we do not know is what traits are most likely to evolve in response to this selection. A common assumption is that the most defended hosts are the most resistant, meaning they limit the establishment and growth of infecting parasites. Under this assumption, resistance traits should evolve readily under parasite selection. Resistance is, however, just one of many strategies hosts use to defend against parasites, and it does not consistently covary with parasite defense. We accordingly ask: which host traits covary with parasite defense and are thus likely to respond to parasite selection? We use controlled exposures to characterize genetic variation in defense of the nematode Caenorhabditis elegans against its natural microsporidian parasites. We report extensive variation in parasite defense among wild strains of C. elegans: some strains lost 60% of fecundity under parasite exposure, while others were unaffected. We then tested the covariance of defense with two prominent host traits, resistance and reproductive timing. Our results did not support the hypothesis that resistance covaries with defense: strains with lower parasite burden did not have higher relative fecundity under exposure. Our results instead supported the hypothesis that life history covaries with defense: host strains that reproduced quickly had higher relative fecundity under exposure, consistent with the idea that parasites diminish future reproductive opportunities. Moreover, we detected substantial heritability of fecundity traits but low heritability of resistance traits. Together, these findings indicate significant potential for adaptation of wild C. elegans populations to defend against their natural parasites. They further predict that life history traits will evolve rapidly in response to parasite selection. AUTHOR SUMMARYSome hosts fare much better than others in the face of parasite infection. What traits differentiate defended hosts from undefended hosts? The answer to this question is critical for identifying the strategies that best protect hosts from their parasites. It also allows us to predict and interpret the evolution of host populations over the course of epidemics. To address this question, we surveyed wild strains of a tractable model host, the nematode Caenorhabditis elegans, for their response to two species of microsporidian parasites. We found that, on average, parasite exposure substantially impaired the ability of hosts to reproduce. Host strains, however, varied widely: some experienced major losses in fecundity with exposure, while others were highly defended, showing little to no change. We identified reproductive timing as the trait that differentiated defended hosts from undefended hosts. Our results indicate that reproducing quickly was protective, because hosts were able to make most of their offspring before parasites impaired reproduction. We did not find evidence that resistance was protective - hosts with lower parasite burdens did not reproduce better than those with high parasite burdens. These findings give added weight to life history as a major component of host defense against parasites.

The expression of plant defensive traits against herbivores often incurs costs to other essential functions, such as growth and reproduction. Understanding how selection acts on putatively functional traits that are expected to trade off across space and time is therefore critical for predicting evolutionary responses to ongoing and future environmental change. Here, we used multiple replicated genotypes of woodland strawberry (Fragaria vesca; Rosaceae) grown over two years in three outdoor common gardens in Spain, Belgium, and Sweden. In each garden, genotypes were exposed to both a reduced-precipitation treatment simulating drought and an ambient precipitation treatment. We estimated directional and correlational selection on rosette diameter (a proxy for growth) and herbivore resistance (measured as the inverse of chewing damage) using fruit and stolon production as proxies for sexual and asexual fitness across all environments (i.e., every site x year x treatment combination). We then combined selection gradients with environment-specific genetic (co)variance among genotypes to quantify the expected response to selection ({Delta}z = G{beta}) and to identify covariance-driven constraints or facilitation therein. Selection consistently favored larger rosette diameter for both fitness proxies across nearly all environments, which, in combination with genetic covariances among genotypes, resulted in a general evolutionary response toward increased rosette diameter, with the strongest response at the wettest site (Belgium). In contrast, selection on resistance and the corresponding among-genotype evolutionary responses were strongly context-dependent. Correlational selection on rosette diameter x resistance occurred in only a few environments, primarily under reduced precipitation. Environment-dependent genetic covariances constrained or facilitated selection on both traits only at the site with the highest herbivory (Sweden) under drought conditions. Overall, our results reveal a context-dependent interplay between selection and genetic architecture, underlining the difficulty of predicting evolutionary trajectories under environmental change, and highlighting how spatially and temporally variable conditions may maintain standing genetic variation in plant traits.

Spontaneous mutation underlies all genetic variation, and thus influences the evolutionary dynamics of complex traits. Although much work has estimated mutation rates for fitness or at molecular scales, we have comparatively little information about mutational influences on other complex phenotypes. We conducted four mutation accumulation experiments with independent clones of Daphnia pulex, and then measured the effect of spontaneous mutation on size at birth, a complex trait whose connection to fitness depends on ecologically-mediated tradeoffs. Therefore it is unclear whether mutations, which are usually neutral or deleterious, should decrease or increase size at birth. In two experiments, individual instances of increased size at birth were common, whereas in the other two experiments, instances of decreased size at birth were common. Together, our data show that genetic background is an important determinant of the consequences of mutation for complex traits, and that mutation rates and direction can vary within species.

Intralocus sexual conflict (IaSC) results from opposing selection acting on traits with correlated expression between the sexes. We recently reported on a male-limited (ML) selection experiment in Drosophila melanogaster designed to investigate IaSC through a sex-limited evolution regime that theoretically resolves conflict in favour of males. However, this experiment did not universally or unambiguously improve male fitness, although female fitness declined as predicted. Here we examine sources of unintended selection: unusual genetic features of the breeding design and the special females used to enforce male-limited inheritance that may have complicated evolutionary outcomes. Specifically, we evaluate the effects of a foreign cytoplasm, genetically marked translocated autosomes, and a female-exposed Y chromosome derived from the clone-generator (CG) system, and the unique environment of sexual selection introduced by foreign CG females. We found that selected male fitness increased by 66% when expressed within the full ML genetic context, rising to over 100% when interacting with CG females. While there is no consistent fitness advantage in the "wild type" genetic background, there is a nearly significant trend of improved fitness with CG females (26% improvement). Further, outside this context, these males do not experience a fitness loss relative to controls, even showing a marginal gain of 6%. Uniformly, these gains were mediated by precopulatory traits: ML selection produced more attractive males with greater mating success and shorter mating latencies, while sperm competition remained unchanged. Intriguingly, ML-evolved males also exhibited reduced mate harm to females, contrary to the established narrative of escalating intersexual antagonism in this system. Dissecting individual components revealed significant fitness improvements associated with adaptation to the foreign cytotype (18%) and the female-exposed Y chromosome (33%), although responses varied across replicate populations. Moreover, when selected haplotypes were expressed together with the foreign cytotype in females, we observe a recovery in fitness. Together, these findings demonstrate extensive compensatory evolution to the ML selection environment, indicating that responses to the release of IaSC were shaped not only by sexually antagonistic selection but also by adaptation to the genetic manipulations and mating context inherent to the experimental design.

The breakdown of distyly, a polymorphism that promotes disassortative pollination between two floral morphs, has significant evolutionary implications. Here we examine the consequences of repeated loss of distyly in Linum by testing for relaxed selective pressure in homostylous relative to distylous lineages, and by characterising the evolutionary genomic patterns of the homostylous Linum leonii in comparison to its distylous close relative Linum perenne. We generated whole-genome sequences and target-capture data from sixteen Linum species, and additionally built a high-quality genome assembly and acquired population-level whole-genome sequencing data for L. leonii (n=20). We reconstructed plastome and nuclear phylogenies, estimated selective pressure for chloroplast and nuclear genes, inferred ancestral floral morph states, and tested for signatures of selfing in L. leonii. Compared to theoretical expectations, results were mixed, with partial identification of relaxed selective pressure in homostyles. One clade exhibited signs of potentially accelerated plastome evolution. Population genomic analyses of L. leonii revealed a moderate selfing rate of 0.32, suggesting that loss of distyly was associated with mixed mating rather than selfing, contrary to previous results on loss of distyly. Reduced nucleotide diversity and evidence for relaxed selection efficacy in L. leonii was likely due to a historical bottleneck. These results highlight the complex evolutionary dynamics associated with the breakdown of distyly. The genomic consequences are more heterogeneous than previously thought, and likely depend on clade- and species-specific evolutionary and demographic history dynamics. This study emphasizes the need for comparative population genomic studies to clarify how such transitions can shape evolutionary processes. Significance statementPlant mating system variation is central to evolution as it shapes genetic diversity, adaptability and fitness. Loss of distyly, an iconic example of a complex mating system favouring cross-pollination, can drives shift from outcrossing to selfing, with potentially severe evolutionary consequences for the long-term persistence of the species in which it occurs. Using high-quality genome assembly and omic data for multiple Linum species, we tested for relaxed selective pressure following loss of distyly in homostylous species and tested for a signature of selfing in homostylous Linum leonii compared to the closely related distylous Linum perenne. Contrary to theoretical expectations, evidence for relaxation of selection was mixed in Linum homostyles and L. leonii did not exhibit a genomic signature of selfing. Our study reveals multiple evolutionary pathways following the loss of distyly, and highlights how mating system transitions, together with complex demographic processes, can differentially shape plant genetic diversity and evolution.

The phenotypic effects of mutations often depend on the genetic background, yet general patterns remain poorly resolved. Here, we tested whether genotypes drawn from the same natural population, but differing in their breeding values for a polygenic trait, differed in their contribution of new mutational variation to that trait. We established >200 mutation-accumulation (MA) lines from four Drosophila serrata genotypes. Analysing >44,000 wing-size measurements, collected over 30 generations, we quantified mutational variance and mutational bias for size. Genotypes with the smallest and largest breeding values for size contributed similar (statistically indistinguishable) amounts of mutational variance. In contrast, the genotype with an intermediate breeding value exhibited remarkably low (statistically undetectable) mutational variance, low micro-environmental variance, and high line survival over time, consistent with limited mutational decay in fitness. The three genotypes with detectable mutational input showed declines in mean size over time, indicating a consistent mutational bias toward smaller size, as reported in other taxa. The magnitude of this bias appeared genotype dependent, with the MA populations founded from the larger ancestors declining nearly twice as fast as that founded from the smallest ancestor. Together, these results demonstrate substantial heterogeneity in mutational properties among genotypes within a single natural population where the trait value spans a relatively narrow range. Such genotype-specific mutational input is expected to shape both the standing genetic variance and the evolutionary trajectory of polygenic traits.

The evolution of plant resistance naturally occurs in complex, multifaceted environments that consist of multiple simultaneous stressors. Understanding how shifting environmental contexts may shape resistance evolution requires empirical studies that consider the combined effects of interacting stressors on fitness and selection. Here, we examined how exposure to an insecticide impacts the evolution of resistance to the herbicide glyphosate in Ipomoea purpurea (common morning glory). Through a factorial field experiment, we manipulated glyphosate and an insecticide to estimate selection on glyphosate and herbivory resistance. We found that glyphosate acted as the primary agent of selection, favoring higher levels of glyphosate resistance. In the presence of glyphosate alone, positive correlational selection favored a combination of higher glyphosate and herbivory resistance, supporting prior work that suggested these traits may be linked. Importantly, insecticide exposure modified both glyphosate resistance and the strength of selection acting upon the trait by increasing resistance and weakening selection. Together, our results indicate that the evolution of herbicide resistance is context-dependent and that secondary stressors like insecticide can alter the evolutionary trajectories of plant defense.

Sexual reproduction is considered to incur multiple costs relative to asexual reproduction. Although previous research has identified indirect selective advantages that help explain the widespread occurrence of sex, the emergence and maintenance of high rates of sexual reproduction remain a central puzzle in evolutionary biology, because indirect selection favoring sex becomes weak when the sexual rate is high. Using a modifier framework that allows the simultaneous evolution of sexual rate and sex allocation, I investigate the evolution of sex via direct selection by incorporating resource allocation trade-offs between sexual and asexual reproduction. The results show that such trade-offs can substantially facilitate the invasion of sex. Crucially, the evolutionarily stable sexual rate depends on the return exponents of female fertility and asexual fertility with respect to resource investment, as well as on the initial allocation to female function within sexual reproduction. Obligate sexuality is evolutionarily stable when asexual fertility exhibits linear or accelerating returns on investment and when both the initial sexual rate and female function allocation within sexual reproduction exceed certain levels. In contrast, facultative sexuality will be evolutionarily stable when female fertility within sexual reproduction and/or asexual fertility exhibit diminishing returns. Contrary to previous theoretical predictions, self-fertilization often inhibits the evolution of sex or reduces the evolutionarily stable sexual rate. This study provides insights into the prevalence of high sexual rates, as well as the continuous spectrum of sexual rates in some groups, highlighting the importance of key parameters in reproductive ecology in shaping the evolution of sex. Significance statementWhy sexual reproduction is so common despite its substantial costs remains a longstanding puzzle in evolutionary biology. Most previous explanations focus on indirect genetic benefits of sex, which generally become weaker as the rate of sexual reproduction increases, and therefore cannot explain the prevalence of intermediate to high sexual rates in nature. This study shows that with resource allocation trade-offs between sexual and asexual reproduction, obligate or facultative sexuality can evolve and be stably maintained via direct selection alone, depending on the marginal returns of asexual and female fertility, as well as the initial allocation to female function. These results highlight the underappreciated role of reproductive ecology in shaping the evolution of sex in nature.

Parthenogenesis is relatively rare and often regarded as an evolutionary dead end. Despite this, certain parthenogenetic animal species have endured for millions of years, but it is unclear what enables the persistence of some parthenogenetic lineages. Transitions from sexual to parthenogenetic reproduction can occur through different evolutionary processes that give rise to diverse cytological reproductive mechanisms. These mechanisms are likely to influence genetic diversity, especially in the early stages after the transition to parthenogenesis and may thus affect lineage persistence. To understand such evolutionary transitions, we used experimental crosses to investigate the mechanism of parthenogenesis and the immediate genetic consequences of switching from sexual to parthenogenetic reproduction in the facultatively parthenogenetic phasmid Megacrania batesii. We obtained DNA sequence data from multiple lineages propagated over three generations via sex, parthenogenesis, or transitions between reproductive modes. We quantified heterozygosity and within-family genetic variation and compared the genetic patterns with predictions for known mechanisms of parthenogenesis. We found that a single generation of parthenogenesis typically resulted in (near-)complete loss of heterozygosity and an absence of within-family genetic variation, consistent with automixis with gamete duplication or terminal fusion and little/no recombination. However, we also found evidence of variation in the mechanism of parthenogenesis among lineages and even within the same individual, associated with drastic differences in the amount of heterozygosity and within-family genetic variation maintained across generations. Our findings show that considerable variation in parthenogenetic mechanisms can exist within populations and suggest that such variation could influence the persistence and evolution of parthenogenetic lineages.

Hybridization is generally considered a temporary phenomenon, but it is actually widespread and may last for large time periods between species that stably coexist. Here, to test whether evolving with a closely-related species modifies or maintains partial reproductive isolation, we performed experimental evolution in artificial sympatry vs. allopatry with two closely-related colour forms of spider mites (Tetranychus urticae) that exhibit an asymmetrical pattern of pre-mating isolation despite almost complete postzygotic isolation. We assessed whether evolutionary changes occurred in traits associated to (i) pre-mating isolation, (ii) post-mating prezygotic and early postzygotic isolation, and (iii) late post-zygotic isolation. Our results revealed that reinforcement did not occur even under forced long-term sympatric evolution. Instead, the strength of some reproductive barriers decreased (e.g., premating isolation and fertilization failure), and some trait changes indicated convergence rather than divergence between species (e.g., mating propensity, latency to copulation). In fact, both types of males showed the same decreased preference for red-form females across generations in sympatry. In line with this, traits underlying fertilization success evolved in the same direction and with similar amplitude in heterotypic crosses and in their homotypic control, as the offspring sex ratio of green-form females decreased in sympatry irrespective of the male they mated with. Finally, other changes in reproductive barriers resulted from trait correlations (e.g., decreased zygote mortality but increased juvenile mortality). Hence, despite very high costs of hybridization, responses occurring following evolution in sympatry were un-related to selection directly associated to hybridization, but rather the by-product of other evolutionary forces, with cascading consequences for reproductive barriers. In particular, these results support the underappreciated hypothesis that within-species sexual interactions can constrain population divergence, or even drive trait convergence between species, thereby playing a role in the maintenance of partial reproductive isolation.

Many simultaneous hermaphrodites use selfing for reproductive assurance only when outcrossing opportunities are limited, owing to inbreeding depression in selfed progeny. However, scenarios that enforce substantial selfing (such as during recolonisation) can rapidly select for a high selfing propensity, a shift in mating system that is expected to eliminate both inbreeding depression and the delayed reproductive onset under selfing that is typically associated with it. We tested these predictions in the flatworm Macrostomum hystrix, using a line derived from an outcrossing population that had been subjected to enforced selfing for multiple generations followed by several years of relaxed selection. As predicted, isolated individual forced to self and individuals with constant partner access (i.e. outcrossing opportunities) did not differ in reproductive onset nor in inbreeding depression estimated through offspring survival. However, a third treatment group that provided intermittent partner access (to allow outcrossing but minimise potential competition effects) showed a different pattern: no inbreeding depression in offspring but a substantially accelerated reproductive onset. Whilst our results thus support the effective purging of inbreeding depression and increased selfing propensity under enforced selfing, we suggest that cues of an unstable social or physical environment nevertheless exert a major influence on reproductive timing.

Theory suggests sexual selection will enhance population viability by purging deleterious alleles. However, direct genomic evidence for this fundamental idea is scarce and contradictory. We combined long-term experimental evolution with whole-genome re-sequencing to directly test how sexual selection affects mutation load, genomic divergence and extinction risk in Tribolium castaneum. After 156 generations, populations evolving under strong sexual selection carried substantially fewer deleterious alleles than populations under weak sexual selection, based on both individual-level estimates of missense and nonsense variants and population-level Rxy analyses, indicating more efficient purging of deleterious alleles. In contrast, nucleotide diversity and runs of homozygosity were similar across treatments, indicating that purging was targeted at deleterious variation, and that reduced mutation load in populations under strong sexual selection was not explained by demographic effects. Importantly, population-level mutation load estimates provided best explained extinction risk under inbreeding, directly linking sexual selection to purging and population viability for the first time. Genome scans of high and low sexual selection populations revealed peaks of divergence, enriched for genes involved in courtship, sex discrimination, and seminal fluid proteins. Our results provide direct genomic evidence that sexual selection can reduce mutation load without eroding standing genetic diversity and thus adaptive potential, while driving adaptive divergence in reproductive traits. This beneficial purging may help explain the widespread prevalence of sexual reproduction in nature despite inherent costs and have important ramifications as to how we manage populations of conservation concern. Significance StatementA long standing and unconfirmed prediction is that sexual selection can improve population health by biasing reproduction away from individuals with high deleterious mutation load. However, direct genomic evidence is lacking, and the indirect data available are scant and contradictory. Now, using whole-genome resequencing of experimental evolved beetle populations, we show that populations evolving under stronger sexual selection carry fewer deleterious mutations and, importantly, are less vulnerable to extinction. Our results provide the first direct genomic support for this long-debated evolutionary process that may help explain the widespread prevalence of sexual reproduction in nature. Our findings also highlight the importance of allowing sexual selection to act in populations of conservation concern.

Microbial mutualists partially determine many host traits, including traits related to infection by parasites. However, while microbial effects on host trait plasticity is fairly well established, whether microbial mutualists contribute to genetic variation in infection-related remains an open question. Here we paired 10 mutualistic Sinorhizobium meliloti rhizobacteria strains with 20 Medicago truncatula plant genotypes in an incomplete factorial design, and experimentally infected the plants with parasitic root-knot nematodes. We used this design to estimate rhizobia contributions to genetic variation in four infection-related traits: host resistance, parasite virulence, host tolerance, and mutualism robustness. We find that rhizobia contribute to genetic variation in host resistance and mutualism robustness, and to genetic variation in parasite virulence via genotype-by-genotype interactions with the host. Rhizobia did not contribute to variation in host tolerance. The influence of rhizobia strains on parasite resistance was partially explained by their effect on host root growth. These results underscores the influence that microbial mutualists have on their hosts response to parasite infection, and suggests that resource mutualists may impact host-parasite evolution. Teaser TextMicrobial mutualists like nitrogen-fixing rhizobacteria influence their host traits. Past work indicates that different strains of rhizobia may influence their host plants interactions with nematode parasites. But how does this influence compare to the genetic variation present in hosts? We explore the contribution of genetic variation across rhizobia strains to infection-related traits in their host and find that rhizobia contribute to genetic variation for parasite resistance and virulence in their host.

Similar traits repeatedly evolve across independent populations in response to similar environmental conditions. For many repeatedly evolved traits it is unknown if populations evolve similar traits through the same or different genetic mechanisms. To address this question, we leveraged the Mexican tetra fish, Astyanax mexicanus, which has evolved repeatedly through altering many traits including reduced sleep duration, eye degeneration, and metabolic shifts to accommodate limited nutrient availability. We defined whether shared or independent genetic architecture govern the repeated evolution of sleep loss, increased food consumption, early onset adipose deposition, and eye loss in different evolutionary origins of the cavefish phenotype by using Quantitative Trait Locus (QTL) mapping across three cave x surface F2 mapping populations. We found that, among the traits evaluated, eye loss exhibits the most genetic repeatability, with [~]43% of QTL shared across lineages. Sleep loss and metabolic traits (i.e., feeding, adiposity) were genetically less repeatable, with only [~]25-33% of QTL shared across lineages. Next, we explored whether QTL for metabolism, eye loss, and sleep traits in cavefish co-localize in the cavefish genome and could be inherited together to facilitate potential cavefish adaptation. Although these traits have repeatedly co-evolved in cave populations, we did not find evidence for extensive genetic linkage among them. Overall, we found that genetic repeatability is a common feature in the repeated evolution of cave traits, the extent of genetic repeatability varies across cave traits, and that there is little evidence for widespread co-localization of sleep, eye loss, and metabolic traits within the genome. SummaryIndependent populations that evolve similar traits in response to similar environmental conditions provide us with natural replicates for studying what constrains evolutionary change. Iconic examples of repeated trait evolution often involve repeated mutations in the same genes, suggesting there are limits on the type of genes and mutations that can contribute to phenotypic evolution. Here we conduct a multi-trait, multi-population QTL analysis for similar eye loss, sleep loss and metabolic shifts across two lineages of Astyanax mexicanus. Genetic repeatability is present for most traits, but its extent is highly trait dependent and occurs at the level of genomic regions rather than specific genes, highlighting the mosaic of constraint and flexibility involved in genetic repeatability.

Adaptive radiation theory posits that speciation in such lineages is largely driven by ecological opportunity in concurrent morphological expansion in response to niche availability. Here, we use a phylogenomic estimate of Australasian diplodactyloid geckos in combination with meristic and ecological data to infer patterns of ecological diversification, quantify signatures of stabilizing selection, and the factors driving speciation processes. Specifically, we focus on two relatively young but speciose and ecomorphologically diverse assemblages from the ancient islands of New Caledonia and New Zealand. Models accounting for stabilizing selection recover shifts in morphospace along many branches that also experienced shifts in ecological guild as inferred from ancestral state reconstructions. We find convergent evolution to be present between the two insular lineages as they independently transitioned to similar guilds from different ancestral ecologies. Community assembly is integral to understanding the dynamics of adaptive radiations and various studies focused on identifying if biotic or abiotic factors drive character suits and sympatry in diverse lineages. Bayesian and multiple regression analyses suggest that abiotic factors rather than interspecific competition dictates phenotypic divergence in both insular lineages. Rather, species seem to diverge phenotypically in allopatry and environmental factors, such as climate, in combination with competitive exclusion drive phenotypic overlap in sympatry. This study provides the first modern assessment of convergence for diplodactyloid geckos and provides robust evidence indicating that similar selective pressures have shaped morphological diversity in these disparate as well the factors affecting sympatry.

Animal mating systems are hugely diverse, ranging from species where mating is essentially random to those exhibiting complex systems of mate choice by one or both sexes. While polygyny and mate choice are known to alter adaptation and persistence in a changing environment, there has been little exploration of the ways that adaptation and evolutionary rescue are modulated by other types of mating systems. We developed an individual-based model that allows random mating, female-only choice, and mutual mate choice to be compared between monogamous and polygynous frameworks and used it to explore how mating systems influence adaptive response, loss of heterozygosity, and extinction risk under worsening environmental conditions. We find that mating systems interact with population size in determining extinction risk: mate choice under polygyny lowers effective population size, small polygynous populations with either mutual or female-only mate choice lose heterozygosity quickly and so face higher extinction risks than randomly mating populations. However, in larger populations where inbreeding and genetic drift are less important, mate-choice-based polygynous systems enhance evolutionary rescue by allowing better-adapted males to dominate reproduction, accelerating adaptation and increasing resilience to environmental change. Among polygynous systems, female-only choice leads to slower loss of heterozygosity and facilitates population resilience better than mutual mate choice. These findings demonstrate that mating systems can critically shape a populations ability to adapt to environmental change and alter extinction risks, emphasizing the need to consider mating systems in designing effective conservation strategies. Significance StatementEnvironmental change threatens species survival, and sexual selection can have profound modulating processes that determine extinction risk. Sexual selection operates in a variety of mating systems, and the role of this diversity is often overlooked. Using individual-based simulations, we show that mating systems with mate choice boost evolutionary rescue in larger populations via "good genes," while in small populations, it has the opposite effect by elevating the loss of heterozygosity. These results have critical implications for conservation biology. Conservation strategies should consider mating system characteristics when assessing species vulnerability and planning management efforts to support evolutionary resilience and long-term population persistence.

Many animals change their behavior in response to social experiences by learning. Although social learning is adaptive, not all individuals learn. In Heliconius melpomene, H. m. malleti males respond to 2-day prior failed copulation experience by decreasing courtship, whereas H. m. rosina males do not. Here, we explore the transcriptomic differences in both the neural (brain) and sensory (eyes, antennae) tissues underlying this natural diversity in male aversive mate-preference learning. While the transcriptomic profiles of the two subspecies are inherently different across all three tissues, we found the greatest difference between the good (H. m. malleti), and bad (H. m. rosina) mate-preference learners in the brain, followed by the sensory tissues. Known learning genes and Gene Ontology terms were associated with differences in mate-preference learning, suggesting conserved learning pathways across animals. Genes within putative magic loci associated with colors, odors, and locomotion, were also differentially expressed between H. m. malleti and H. m. rosina, suggesting multimodal sensory processing may drive behavioral variance in these two subspecies. Overall, our study identifies genetic underpinnings for differences in preference learning, both in neural processing and sensory tissues. Selection on these genes/networks could result in preference learning-induced reinforcement, leading to reproductive isolation and speciation.

Recent reviews of isolating barriers in plants conclude that prezygotic barriers play an outsized role in plant speciation; yet these conclusions derive overwhelmingly from studies of sympatric, perennial herbs in temperate zones, and at later stages of speciation. Trees possess several traits that are expected to influence barrier evolution, including prolonged generation times and reproduction, predominant outcrossing, and long-distance gene flow. We examined early-evolving post-pollination barriers between ecologically diverged, vegetatively distinct varieties of the tree species, Metrosideros polymorpha, that have a common floral morphology and highly overlapping flowering times. We performed controlled crosses between each of Hawaii Islands four varieties and maternal trees of the high-elevation variety and examined pollen-tube growth, fruit set, seed germination, and seedling phenotype. We then monitored survivorship, maturation rate, and fertility of F1 hybrids over [≥]8 years alongside parental controls and a fourth F1 genotype derived from companion studies. The four F1 crosses showed four contrasting patterns and strengths of predominantly postzygotic isolation, including high F1 mortality that manifested over several years. Results from this and other tree studies suggest that ecological speciation in trees follows the classical speciation model of early postzygotic barrier formation followed by reinforcement, whenever stable environments promote recurring hybridization.

Phenotypic plasticity allows plants to rapidly respond to changing environments without the need for evolutionary change or migration. While selection can create variation in plasticity across natural populations, these responses are not adaptive in all environments. To predict whether plasticity will be adaptive requires evaluation of its fitness effects across a range of environments, including novel ones. Here, we test how traits and their plasticity vary for genotypes collected across a natural hybrid zone between two tree species with contrasting climatic niches. Fast-growing Populus trichocarpa inhabits maritime environments with relatively warm and stable temperatures, while P. balsamifera inhabits continental environments with cold winters and large temperature variance throughout the year. We planted 44 clonally replicated genotypes into thirteen common gardens and measured vegetative phenology, leaf morphology, stomata morphology and conductance, and photochemistry. Overall, genotypes from colder, more continental environments exhibited higher plasticity. P. balsamifera ancestry was associated with increased plasticity in timing of fall phenology, stomatal conductance, and leaf mass per unit area. We assessed the effects of trait plasticity on fitness estimated as yearly growth across common gardens and found that the plasticity-fitness relationship was often garden-specific, indicating that the planting environment did not consistently mediate plasticity-fitness relationships. When the effects of trait plasticity on growth varied by garden temperature, higher plasticity generally had neutral or negative associations with growth in warmer environments. These results suggest that elevated plasticity evolved in a P. balsamifera genomic background as part of a climate generalist strategy to seasonal temperature variability, but that there is a trade-off between plasticity and growth in warmer environments. Consequently, less-plastic but warm-adapted P. trichocarpa genotypes are likely to have a fitness advantage under warming climates. These results demonstrate that plasticity may sometimes be maladaptive and will not be universally beneficial in a warming world.