Evolution

Understanding how anatomical structures evolve requires disentangling the roles of integration and modularity in shaping morphological variation. The vertebral column, a serially repeated and regionally differentiated structure, provides a powerful system for investigating these processes. Here, we examine how vertebral morphology evolves in relation to whole-body elongation across the adaptive radiation of Lake Malawi cichlid fishes. We tested for evolutionary integration between the precaudal and caudal domains, as well as assessed the contributions of vertebral count, centrum shape, and intervertebral spacing on body elongation. We find strong evolutionary integration between precaudal and caudal vertebral shape, with both vertebral shapes varying along shared axes of multivariate shape change. Despite this, precaudal and caudal vertebral counts evolve independently, indicating a decoupling between the evolution of identity and morphology. Whole-body elongation is significantly associated with coordinated changes in vertebral and rib morphology, including proportional increases in centrum size, posterior displacement of neural and haemal spines, and increased rib curvature. In contrast, centrum elongation and intervertebral spacing do not independently explain body elongation beyond vertebral counts. These results demonstrate that body elongation in cichlids necessitates integrated, multivariate changes in axial morphology. Our findings highlight the importance of morphological integration in facilitating coordinated evolutionary responses in anatomical systems.

Article summaryGene interactions are common, yet additive genetic models often predict short-term evolution and breeding response. This study argues that additivity can arise because populations sample only a small neighbourhood of a curved fitness landscape. In additive channels, genetic variation is small enough that local curvature contributes little to heritable fitness differences. The study defines an additivity index ([A]g) that compares variance from the local slope of log-fitness with variance from curvature, and links this ratio to expected prediction accuracy under Gaussian assumptions. A selection-inheritance framework shows when additive channels persist and when populations leave them. It yields testable predictions.

Classical models of protandry predict unimodal male emergence timing, yet empirical observations in butterflies and bees reveal dimorphism: early-emerging small males coexist with late-emerging large males. The evolutionary mechanisms underlying such discrete alternative reproductive strategies in emergence timing remain poorly understood. In this study, we developed a mathematical model using an adaptive dynamics framework to investigate the conditions under which dimorphic male emergence timing evolves. We explored two potential mechanisms: (1) a trade-off between emergence timing and male competitiveness, and (2) differences in the variance of emergence timing between the sexes. Our analysis demonstrates that both mechanisms produce evolutionary branching, and that extreme variance asymmetry between sexes can generate multiple branching events, yielding three or more distinct male clusters. These findings provide a theoretical foundation for understanding the evolution of alternative reproductive strategies in emergence timing, with implications for other systems where reproductive success depends on temporal overlap between the sexes. We provide testable predictions that a positive correlation between emergence timing and male body size or competitiveness should be observed under the trade-off mechanism, and that the variance in emergence timing within each male morph should be smaller than that of females under the variance asymmetry mechanism.

Reproductive Character Displacement (RCD) often occurs when species with mating-related polymorphism come into secondary contact, leading to divergence in reproductive traits. Ischnura elegans and Ischnura graellsii have formed two independent hybrid zones in Spain where reinforcement has strengthened a mechanical barrier, and RCD has shaped mating-related structures, although reinforcement is asymmetric only in gynochrome females. This study examines the link between asymmetric reinforcement and asymmetric RCD. Using geometric morphometrics, we analyze prothorax shape and size in both female morphs and males, and male caudal appendages, to assess morphological divergence, determine whether gynochrome females show stronger divergence, and test for morphological covariation between male traits involved in the tandem position. Our results reveal consistent patterns of size and shape variation across species and zones: in I. elegans, androchromes are larger and resemble males in size, with clear shape differentiation between female morphs that diminishes in hybrid zones. In contrast, I. graellsii shows less consistent size differences between males and morphs, and weaker shape differentiation. Our results confirm RCD in prothorax shape in I. elegans females from both hybrid zones, but reveal that RCD in prothorax size is asymmetric, occurring only in gynochrome females from the NC hybrid zone. We also detected RCD in the prothorax shape of I. elegans males from the NC hybrid zone, extending previous evidence of RCD in male caudal appendages, while morphological covariation between male cerci and the prothorax was limited to size in I. elegans. Together, these findings illustrate how hybridization may generate morph-specific patterns of reproductive divergence.

Mate preferences are often influenced by the magnitude of sexual signals, which are presumed to indicate underlying aspects of signaller quality. Although the perception of these signals depends on sensory processes, the role of perceptual adaptations and constraints in mate assessment is frequently overlooked. Many sensory systems follow Webers law of proportional processing, where discrimination between signals is based upon their proportional, or relative, difference rather than their absolute difference. Because preference strength varies with relative trait magnitude, Webers law could strongly influence sexual selection, changing the coevolution of traits and preferences. Here, we explore the consequences of Webers law for sexual selection using individual-based models, applying Scalar Utility Theory to mate choice. We investigate the coevolution of male ornaments and female preferences under both Fisherian and good genes scenarios, as well as scrutinizing the sexual selection of multiple ornaments and preferences. Including Webers law in these models either reduced ornament exaggeration, or promoted exaggeration and diversification of ornaments and preferences, depending on the costs of choice and how rapidly female survival decreases when preferences evolve away from the naturally selected optimum. These results highlight the importance of perception and cognitive processing in shaping sexual selection and its evolutionary impacts.

The body size of adults and immature stages are fundamental animal traits that influence animal physiology, ecology, and range distribution. While the importance of egg size has been acknowledged as a proxy of parental investment in animals, little work has addressed the tempo and mode of evolution of egg size and shape. Here, we present a comparative study of this trait using a phylogeny based on genome-wide markers together with measurements of egg size and adult body size from 29 drosophilid species. Our analyses revisit the allometric relationship between egg size and body size and show that egg size scales negatively with respect to adult size, even after accounting for shared evolutionary history. In other words, larger species tend to produce proportionally smaller eggs. We also detect a moderate phylogenetic signal in both egg size and egg shape, indicating that closely related species resemble each other in these traits. Model comparisons show that the evolution of egg morphology in drosophilids is best described by gradual divergence through time driven by stochastic evolutionary change. This pattern contrasts with findings from other animal groups, including birds, cephalopods, and reptiles, where alternative evolutionary models better explain trait evolution. Together, these results suggest that the evolutionary dynamics shaping egg morphology in drosophilids differ from those operating in other major lineages and underscore the importance of comparative analyses of early developmental traits across taxa.

In many systems, mutations can have background-dependent fitness effects due to genetic interactions between loci within a genome (intragenomic epistasis). In some cases, such as when species are coevolving, genetic interactions between loci can span across species; this is described as intergenomic epistasis. It is known that intragenomic epistasis can make adaptation more repeatable by constraining accessible mutational paths. Here, we investigate whether intergenomic epistasis leads to the same pattern of increased repeatability and how repeatability is influenced by the interplay of intra- and intergenomic epistasis. For this, we model a two-species system in which the fitness of a species depends on the combination of genotypes that are present in both species. We implement this system using an NKC model, which allows us to construct coevolutionary fitness landscapes on which we simulate adaptation by means of mutations in both species. To quantify the repeatability of adaptation, we track the realised endpoints of adaptive walks and record the distribution of fitnesses of the focal and partner species at these evolutionary endpoints. We find that intergenomic epistasis creates highly repeatable patterns of adaptation that depend on the underlying shape of the coevolutionary landscapes. The patterns of repeatability deviate from expectations based on intragenomic epistasis due to fitness trade-offs between species, which can lead to cycling and large co-evolutionary fitness loads.

How evolutionary and developmental processes interact to determine axes of neural variation that produce behavioural diversity has been debated for many decades, with alternative hypotheses giving differential emphasis to functional coupling, which favours co-evolution, and developmental constraint, which enforces it. A critical omission is data on the genetic architecture of brain size and structure, which more closely illuminates the shared developmental dependencies between components of an integrated system. Here, we exploit ecological divergence between Astatotilapia calliptera and Aulonocara stuartgranti, two closely related cichlid species from Lake Malawi, to explore the genetic architecture of brain evolution. Using computer vision and machine learning techniques to extract volumetric data from micro-tomographic images, we first demonstrate significant divergence in brain composition between these species. Genomic and micro-tomographic imaging data from a population of hybrids generated between the two species were used to investigate genetic factors shaping this differentiation. We show that the majority of brain components are integrated phenotypically in hybrids, but genetic correlations between them are generally weaker. We further show that variation in multiple brain components is associated with variation in largely structure-specific quantitative trait loci, rather than determined by genetic factors with broad effects across the entire brain. These results suggest a genetic architecture that can facilitate modular changes in brain structure, and imply that individual components are independently evolvable.

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.

AO_SCPLOWBSTRACTC_SCPLOWEnvironmental heterogeneity across freshwater systems often promotes phenotypic variation, yet disentangling environmentally induced variation from heritable differentiation remains a central goal in evolutionary ecology. We investigated the geographic distribution and morphological differentiation, and heritability of shell traits among populations of the freshwater lymnaeid snail Pectinidens diaphanus in Patagonia. Extensive field surveys across 196 freshwater sites revealed that the species occupies a broad range of lentic and lotic habitats and constitutes the only lymnaeid inhabiting southern Patagonia. While reproductive anatomical structures were conserved across populations, shell shape differed markedly among populations from contrasting habitat types, with population identity explaining nearly 50% of total shape variation. Populations from hydrologically unstable habitats (ponds and streams) exhibited more elongated shells and relatively smaller apertures, a pattern consistent with functional responses to hydroperiod variability and desiccation risk. To assess the heritability of this differentiation, we conducted a common-garden experiment across two generations. Shell shape differences between permanent- (lagoon) and temporary- (pond) habitat-derived populations persisted into the G2 generation reared under standardized laboratory conditions, indicating that the observed variation is not solely a response to local environmental conditions but includes a heritable component. Together, our findings demonstrate that P. diaphanus constitutes the sole lymnaeid across southern Patagonia, occupying a broader range than previously documented, and that populations show heritable shell differentiation potentially associated with contrasting freshwater habitats. By integrating large-scale biogeographic surveys with morphometric and experimental approaches, this study provides new insight into how habitat variation may contribute to ecological and evolutionary differentiation in freshwater gastropods.

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

Social interactions are ubiquitous in nature and have the potential to affect trait evolution, particularly in group-living animals such as cooperative breeders. Interactions among conspecific individuals can affect the amount of additive genetic variation for a trait when the phenotype of an individual is also affected by the genotype of its social partner(s) via indirect genetic effects. Thus, quantifying both direct and indirect genetic effects of social partners is critical for understanding and predicting evolutionary trajectories. While much is known about maternal indirect genetic effects, empirical estimates of indirect genetic effects from other social partners remain limited, particularly in wild populations. Here, we use animal models to assess the contribution of indirect genetic effects from all social partners in a family group (mothers, fathers, and helpers) on juvenile morphometric traits across ontogeny in the cooperatively-breeding Florida scrub-jay (Aphelocoma coerulescens). We found indirect genetic effects of helpers and fathers on nestling weight, but no indirect genetic effect of mothers. Across ontogeny, we found increasing additive genetic variation in both weight and tarsus length. Our study provides a comprehensive assessment of within-group indirect genetic effects in a cooperative breeder and highlights the importance of considering indirect genetic effects beyond maternal effects.

Recombination rate varies within and between individuals. One form of such variations is seen between sexes in dioecious populations, with males typically exhibiting a smaller recombination rate than females. This is true both for sex chromosomes and autosomes (so-called heterochiasmy). Although a large body of theory exists on the role of sex chromosomes in adaptation and population divergence, much less is known about the role of heterochiasmy. Recently, it has been suggested that heterochiasmy can facilitate local adaptation and divergence, but if, and when this is true has not been systematically studied theoretically to date. Here we use Individual-based simulations to assess the effect of sex differences in autosomal recombination rates on the process of divergence and adaptation in populations subject to divergent selection and migration. We found evidence supporting that sex differences in autosomal recombination rate between adaptive loci can facilitate, and especially maintain, divergence, but this is true only under very limited conditions, involving strong selection, high sex-averaged effective recombination rates and relatively high rates of migration compared to the strength of selection. We further found that this effect, when present, is typically weak but is amplified in cases of highly polygenic adaptation in comparison to cases with a few adaptive loci of strong effect. We conclude that, in most cases, sex differences in autosomal recombination rate alone are unlikely to noticeably contribute to the process of adaptation and divergence. Further studies are needed to evaluate their effect in combination with other processes not considered in the present study, such as assortative mating between the alike mates, or recombination suppression in heterozygotes. TeaserIn dioecious populations, recombination rate typically differs between males and females. This is true both for sex chromosomes and autosomes. While much theoretical research has focused on understanding how recombination rate differences in sex chromosomes shape local adaptation and divergence, we lack theoretical knowledge of the potential role of sex differences in autosomal recombination rates. Recombination has a dual role in local adaptation. Strong recombination can effectively purge deleterious alleles, but it can also break apart beneficial allele complexes (and vice versa for weak recombination). Thus, one may expect that in the presence of both strong and weak recombination exhibited by females, and males, respectively, population divergence can be efficiently facilitated. But is this true? Here, we study this question theoretically using computer simulations. Our main finding is that sex differences in autosomal recombination can facilitate divergence, but this effect is typically weak and present only under very stringent conditions.

Climate change is causing rapid changes to freshwater environments, driving selection for phenotypes that can cope with altered thermal conditions, while also changing developmental environments. This may promote local adaptation, migration to new habitats, and/or phenotypic plasticity. Climate change may also increase hybridization rates between locally adapted phenotypes, as populations migrate and spatially mix in new ways. Consequently, these conditions may facilitate the production of variation, including both adaptive and maladaptive outcomes. To examine this, we leveraged threespine stickleback (Gasterosteus aculeatus) that have locally adapted to either geothermally warmed or ambient environments in Iceland. We tested the effects of hybridization between thermal ecotypes on gene expression using a common garden experiment, where pure-strain ecotypes and their hybrids were reared under 12{degrees}C and 18{degrees}C. We performed RNA-seq on brain and liver to assess 1) ecotype divergence, 2) plasticity, and 3) the effects of hybridization and inheritance patterns. We identified a low degree of expression divergence between locally adapted ecotypes, despite a high degree of plasticity across rearing environments. Hybrid ecotypes were highly divergent from both geothermal and ambient ecotypes and exhibited transgressive expression under both rearing temperatures. Transgressive expression disrupted gene networks extensively, with broader effects at 18{degrees}C than at 12{degrees}C, primarily associated with metabolism and mitochondrial function. Hybridization between locally adapted thermal ecotypes appears to largely disrupt genes associated with energy balance and metabolic function. While demonstrating mechanisms underlying the rapid evolution of reproductive isolation, these findings also provide insights for how populations may cope or fail within a warming world.

Dormancy is a widespread adaptive strategy that allows organisms to survive in temporally varying habitats by suspending development and reproduction. Although environmental variability is expected to shape dormancy strategies, it remains unclear how differences in environmental variability and predictability influence both the production of dormant embryos and the termination of dormancy. We addressed these questions by comparing D. pulex and D. obtusa, two closely related species that inhabit environments differing in variability and predictability. We hypothesized that D. obtusa, which inhabits ephemeral environments, would exhibit a greater propensity for sexual reproduction and dormancy and would require stronger cues to break dormancy than D. pulex, which occurs in more permanent, predictable habitats. Consistent with our hypothesis, D. obtusa lineages produced significantly more males and ephippia than D. pulex when reared under identical laboratory conditions, indicating greater investment in sexual reproduction and dormancy. Contrary to our hypothesis, we found no difference in responsiveness to cues between the two species. Across species, embryos broke dormancy and hatched most readily after experiencing changes in cold and light, even if not experienced at the same time. In contrast, desiccation reduced the propensity to break dormancy. Together, these results indicate that species occupying more ephemeral environments invest more heavily in the production of dormant offspring, but that the environmental cues regulating dormancy termination appear broadly similar between species. This pattern suggests that while investment in dormancy may evolve in response to environmental variability, the mechanisms controlling dormancy termination are more conserved.

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.

Altruism, in which individuals sacrifice some of their own reproduction to help others, can evolve if it is preferentially directed toward relatives. Organisms may recognize relatives through phenotypic similarity. Under the models originally studied by Hamilton, the threshold relatedness at which altruism becomes beneficial depends on the overall relatedness of the population. Implicit in this result is that natural selection may favor context-dependent strategies, in which donors judge their similarity to potential recipients relative to their similarity to the overall population when deciding whether to help. In this manuscript, we use a combination of simulations and theory to determine the circumstances under which context dependence is favored over simple strategies that do not depend on the observation of other interacting individuals. We find that a "plastic" strategy that uses the population context in its rule for donating consistently beats strategies that use only information about the potential recipient.

Population genetic models excel at identifying the conditions for polymorphisms based on balancing selection but typically disregard the ecological processes that yield particular values of selection coefficients. We model a system that combines antagonistic pleiotropy, dominance reversal and heterozygote advantage: the wood tiger moth Arctia plantaginis, where alternative haplotypes at a major-effect locus determine male hindwing coloration. Yellow offers better protection against predators, while white is often associated with better mating success. The effects of mortality and reproductive success overlap in time because protandrous males can mate as long as they are alive, but they need to avoid predation for several days before the bulk of females emerge. We show that protandry aids polymorphism maintenance whenever the second-fittest genotype (after the heterozygote) is the poorly surviving but mating advantaged homozygote, while increased protandry harms polymorphism when the second-best fitness is that of the survival advantaged morph. Ecologically plausible protandry times predict that dominance reversal does not have to be strong for polymorphism to be maintained. Our study highlights the importance of timing traits in maintaining polymorphisms in Lepidoptera and showcases the benefits of deriving fitness explicitly in place of abstract selection coefficients that lack temporal components within the life cycle.

Multiple frameworks have been developed to investigate the evolution of species interactions on fitness landscapes, each with unique strengths and weaknesses. These include adaptive dynamics, which uses linear stability analyses to predict eco-evolutionary outcomes resulting from the invasion of rare mutants into a resident population, and population genetics, which mechanistically models finite populations and stochastic processes in finite time. Though there are some known correspondences between these frameworks, it is not clear that they will always result in the same eco-evolutionary outcomes. Moreover, while adaptive dynamics is very powerful for predicting outcomes, it is not always straightforward to relate these predictions to the data generated in experimental evolution studies. Here, we use a data-driven model of microbial species interactions to compare and contrast the predictions of population genetics and adaptive dynamics. We derive expected outcomes for one-species and two-species evolutionary trajectories by using the invasion fitness landscape concept from adaptive dynamics, and then use analytical theory and forward-in-time simulations to set these predictions within the context of population genetic models. In the context of our one-species models, we show that the timescale of evolution depends on mutation supply and effect sizes, when populations are initialized both along and off a trade-off function. For two-species competition models, we show that mutation supply, effect sizes, and asymmetries between competing species result in discrepancies between adaptive dynamics and population genetics, especially in cases where adaptive dynamics predicts stable coexistence. Our study provides insight into the role of finite timescales, mutation supplies and population sizes in the evolution of species interactions, and facilitates further research that leverages the invasion fitness landscape concept within the realm of population genetics.

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.