Journal of Evolutionary Biology

Aggression occurs in many forms and can be an important adaptive behaviour. Two distinct forms are predatory and intermale aggression. It remains unclear whether they share genetic and neurobiological regulatory mechanisms and thus whether evolution of one may influence the other. We tested whether selection for increased predatory behaviour leads to increased intermale aggression using an experimental evolution model comprising lines of bank voles (Clethrionomys = Myodes glareolus) selected for high predatory propensity towards crickets (P lines) and unselected control lines (C lines). Adult males were tested in a cricket-hunting test followed by two intermale aggression tests. As expected, P-line males showed higher hunting propensity and performance than C-line males. In the intermale aggression test, a greater proportion of P-line males displayed aggressive behaviours (93% vs. 80%), they did it earlier (mean{+/-}SD: 116 {+/-} 144 s vs. 349 {+/-} 320 s), more frequently (33 {+/-} 38 vs. 12 {+/-} 17), and for longer (92 {+/-} 137 s vs. 31 {+/-} 52 s). P-line males also showed a proactive behavioural profile, whereas C-line males were vigilant, spending more time observing the opponent and staying immobile. These results indicate that predatory and intermale aggression partly share genetic and neural regulatory mechanisms.

Transgenerational plasticity (TGP)- when parental environments influence offspring phenotypes - is ubiquitous across taxonomic groups and can have benefits for offspring beyond what is possible with developmental plasticity, particularly when selective pressures are high early in life. However, patterns of TGP vary widely across populations and species, and the evolutionary processes shaping this variation remain poorly understood. Here, we tested whether repeated evolutionary transitions result in parallel or population-specific evolutionary divergence in TGP relative to ancestral conditions. We examined sperm-mediated paternal effects across two ancestral marine and three derived freshwater populations of threespined stickleback fish (Gasterosteus aculeatus). We exposed fathers to dragonfly larvae (endemic to freshwater) or sculpin (endemic to all populations) predators and measured both paternal response to predators as well as antipredator behavior and growth in larval offspring. Fathers behaviorally responded to the presence of sculpin predators, but not dragonfly larvae. However, we found strong paternal effects in response to both predators in all populations. Further, the magnitude of TGP did not differ between marine and freshwater populations, suggesting that TGP does not become genetically accommodated as marine populations move into freshwater habitats. We found some evidence consistent with parallelism in both within and trans-generational plasticity: 1) personal exposure of larval stickleback to dragonfly larvae elicited strong antipredator responses in freshwater populations that were absent in marine populations, and 2) paternal predation exposure consistently increased offspring growth in marine populations while slowing growth in freshwater populations. In contrast, paternal effects altered offspring behavior in population-specific ways, with strong sex-specific effects of paternal exposure emerging in response to endemic predators. Adaptive evolution is a two-step process, in which heritable genotypic and phenotypic variation must first be present and then selected on. Therefore, high population-level variation in TGP suggests the capacity for rapid evolution of parental effects, while signatures of parallelism and sex-specific patterns suggest that TGP may evolve in targeted ways in response to ecological stressors.

Reproductive success often depends on coordinated combinations of morphology, dispersal ability, and mating behavior. Supergenes, genomic regions of suppressed recombination, allow such combinations to be inherited by offspring as a single unit. In ants, independently evolved supergenes control colony queen number, yet few studies have investigated their joint influence on morphology, mating, and colony-founding in sexuals. Formica cinerea provides a unique opportunity to address this question because it harbors two supergenes that together produce three queen and male morphs: large monogyne, large polygyne, and small polygyne. Here we show that these supergenes jointly shape an integrated suite of traits across the reproductive cycle. Wing area was primarily associated with the chromosome 3 supergene, with monogyne individuals having larger wings than polygyne individuals. Thorax volume was associated with the chromosome 9 supergene, with small polygyne individuals having reduced thorax volume regardless of social origin. Mating was assortative for both supergenes in large morphs but random in small polygyne queens. Independent colony founding was almost exclusively performed by large monogyne queens; initial egg production was unaffected by mate genotype. These findings show that the two supergenes jointly coordinate dispersal morphology, mate choice, and colony-founding into coherent reproductive strategies, preventing maladaptive intermediate phenotypes.

Copper is an essential micronutrient in most organisms that becomes toxic in large quantities. Repeated or prolonged sub-lethal exposure can lead to evolved resistance to copper toxicity over many generations, which may result in trade-offs between energetically expensive detoxification mechanisms and fitness. Alternatively, evolved resistance to chemical stressors may lead to correlated changes in other traits. This study focuses on a population of flies for which artificial selection for copper resistance led to an increase in both copper resistance and longevity. The apparent off-target benefit of copper selection on one component of fitness led us to investigate differences in fecundity and developmental viability in copper resistant and copper sensitive, non-selected populations. We assessed the effect of copper selection and copper exposure on multiple aspects of fecundity over the lifespans of females from the non-selected and copper-selected populations. Our study corroborated previously observed increased longevity in copper-selected flies. Controlling for variation in lifespan, copper-resistant females had comparable age-matched fecundity to copper-sensitive females and benefitted from increased longevity with higher lifetime fecundity. Overall, copper exposure negatively affected egg quality, but we found no difference in this trait between the copper-resistant and sensitive populations. Further, we found developmental viability under copper stress was significantly higher for eggs laid by copper-resistant females. Overall, we determined that copper resistant flies experienced a fitness benefit through both lifespan and fecundity. Costs of maintaining copper resistance may be associated with energetic costs, but these trade-offs may not always manifest in reproductive or lifespan fitness costs.

The between sex genetic correlation for traits has long been hypothesized as a constraint to the evolution of sexual dimorphism. Both empirical and theoretical work has suggested that this constraint is influenced by genotype-sex-environment interactions. We examine genotype-sex-environment interactions in both sexually exaggerated and non-exaggerated legs of Drosophila prolongata, to examine the role of organismal condition on evolvability of an extreme trait. We employed a nested full-sib half-sib crossing design, providing food either ad libitum, or restricting food during larval growth, to each brood. When provided food ad libitum, inter-sex genetic correlations between traits is high and positive, whereas under food restriction this correlation substantially weakens, with a modest negative sign. Similarly, comparisons of the G matrix across sexes becomes less associated under food restriction. We discuss these results in the context of the growing appreciation of the factors that facilitate sex-specific evolutionary change.

Rapid adaptation in complex environments depends not only on the amount of genetic variation, but also on patterns of covariation among traits targeted by selection. Anthropogenic stressors create rapidly changing and multifaceted environments and provide powerful systems in which to investigate the potential for adaptation to multiple coinciding stressors. We investigate the combined effects of heat and chemical stress on survival in the black scavenger fly, Sepsis neocynipsea, and determine the genetic basis for resistance. In a fully factorial experiment, we expose isofemale lines to combinations of heat stress and ivermectin, a veterinary antiparasitic to which these flies are naturally exposed in agricultural landscapes. Using a Bayesian quantitative genetic approach, we estimate broad-sense genetic variation and cross-environmental genetic correlations. First, we show that these two stressors have synergistic effects on survival, with heat stress exacerbating the lethal effects of ivermectin. Second, we find that the largest component of genetic variation is the response to heat and ivermectin in combination (genotype-by-environment-by-environment; GxExE). Third, cross-environmental genetic correlations are weak, implying that relative genetic performance is dependent on the specific combination of stressors. Together, these results suggest that incorporating GxExE is essential for understanding adaptive potential in multi-stressor environments.

Allee effects are positive relationships between components of individual fitness and the number or density of individuals in a population. Negative density effects are well documented in Drosophila melanogaster across life stages, while Allee effects are rare and largely confined to the larval stages. However, despite the costs of high density, adult flies are found to exhibit attraction to same-sex conspecifics, suggesting some fitness value to the presence of conspecifics. We measured fitness related traits of singly mated-females housed at same-sex densities of 1, 2, or 10 and found clear reductions in lifetime reproductive output at low densities. Additionally, these females concentrated reproductive effort within early adulthood, albeit without improving estimates of fitness. When housed at variable densities, females altered their reproductive output in response to immediate densities, but were unable to improve it unless remating was possible, indicating an interaction between mating and density. Overall, our findings suggest that reproductive plasticity in response to the presence of conspecifics mediates positive effects of density on fitness in female Drosophila melanogaster. Understanding the physiological and ecological bases of such plasticity may help explain the evolution of social tendency in the fly.

In many species with female sperm storage, ejaculates from multiple males overlap in the female reproductive tract, making sperm competitive ability a key component of male reproductive fitness and a target of rapid evolutionary change in the underlying genes. Here, we used controlled laboratory assays of Drosophila melanogaster sperm competition, with doubly-mated females and paternity assignment of offspring, to ask whether a Bradley-Terry framework can effectively summarize and predict competitive outcomes. The Bradley-Terry model is a probabilistic approach that estimates a latent "ability" score for each contestant based on outcomes of pairwise contests, and thus is naturally suited to data from sperm competition, which are intrinsically pairwise. We selected five distinct male genotypes: four carried strongly expressed RFP or GFP markers that allowed us to distinguish their heterozygous offspring under UV illumination, and the fifth was Canton-S, a standard wild-type genotype that served as our reference. Using Canton-S females, we assayed all 20 ordered pairwise combinations of first and second male, recorded successful double matings, and quantified the offspring sired by each male. We then extended the Bradley-Terry model to estimate genotype-specific competitive success separately for first-male "defense" (fertilization success following initial mating, also called "P1") and second-male "offense" (fertilization success following a remating, also called "P2"). This framework provides a flexible and efficient way to integrate results across large arrays of pairwise mating tests and to derive predictive scores for sperm competitive performance.

Eusocial Hymenoptera present the highest known recombination rates among metazoans, which evolved several times independently among bees, ants and wasps. Several hypotheses have been proposed to explain this observation, including stronger selection for recombination caused by coevolving parasites and pathogens, and strong sexual selection among haploid males due to male-biased sex ratios among reproductive individuals. In this article, we explore the effects of haplodiploidy and differential selection between sexes on the evolution of recombination, by analyzing a three-locus model in which selection for recombination stems from negative epistasis between selected loci. Our analytical predictions are compared with the results of individual-based simulations in which deleterious mutations occur along a linear chromosome. Our results show that, at mutation-selection balance for deleterious alleles, increasing the strength of selection against deleterious alleles (due to the effect of male haploidy and/or sexual selection) tends to reduce selection for recombination. However, an increase in the overall magnitude of negative epistasis (which may also be due to male haploidy and/or sexual selection) combined with the fact that recombination only occurs in females may increase selection for recombination substantially. Our model also shows that, in conditions favoring recombination, increasing recombination in meioses leading to parthenogenetic ovules (and male offspring) may yield stronger benefits than in meioses leading to fertilized ovules (and female offspring).

The number of chromosome sets per nucleus is a fundamental trait, but why this number is nearly always two for multicellular eukaryotes remains unclear. Chromosomes are made of nucleic acids, which possess abundant phosphorus (P). Therefore, producing new chromosomes, as well as generating new cells and organismal growth, demands substantial phosphorus. Yet, because P is often limiting in nature, P availability could influence the prevalence of diploidy versus polyploidy. Here, we compare growth rates of diploid and triploid Potamopyrgus antipodarum, a freshwater snail, relative to P availability. Because diploid P. antipodarum are obligately sexual while obligately asexual individuals are polyploid, costs associated with sensitivity to P limitation in polyploids could also help explain the maintenance of sexual P. antipodarum. We raised juvenile diploid and triploid snails on either P-adequate or P-deficient diets and found that independent of P availability, juvenile triploid asexual snails grew faster and harbored higher P content as adults than sexual diploid conspecifics. Together, these results suggest life-history advantages of polyploidy or asexual reproduction that exacerbate rather than ameliorate the cost of sex. These outcomes suggest that P availability is unlikely to be a main driver of ploidy polymorphism or the maintenance of sex in P. antipodarum.

Internal evolutionary conflicts arise when elements within an organism have diverging fitness interests. Examples range from meiotic drive and cytoplasmic male sterility to transposable elements and supernumerary B chromosomes. While once treated as genetic curiosities, they are now seen as widespread and major drivers of eukaryotic genome evolution. Yet their study remains fragmented, with no clear entry point not only for those who wish to gain an overview of theoretical advances, or those who wish to construct models of their own. Here, we discuss ways in which internal evolutionary conflicts have been modelled and develop a common population genetic framework for building such models. The framework provides explicit criteria for what counts as conflict, distinguishing it from fitness trade-offs, and formalises how and when internal conflicts arise. By treating different cases within the same structure, it shows that these diverse phenomena share a common logic.

Evolutionary diversity in metabolic rate underlies differences in physiology, morphology, and life history across the tree of life. Cell size has been proposed as an important determinant of metabolic rate. The mechanisms underlying this proposed connection are based on the lower surface area to volume ratios in larger cells. As relative surface area decreases, the cost of maintaining ion gradients across the cell membrane through action of the Na+/K+-ATPase pump are posited to decrease, lowering overall metabolic costs. Despite strong theoretical support for this model, and its incorporation into broader models of life history evolution, empirical measurement of Na+/K+-ATPase activity in species that differ in cell size has been lacking. Here, we study nine species of salamanders of the genus Plethodon that span a large range of cell sizes approaching the animal upper limit. We compare basal cellular respiration rates, relative cost of the Na+/K+-ATPase pump, and maximal mitochondrial respiration rates in liver and heart tissue. Contrary to predictions, we find no support for a relationship between cell size and any of these mitochondrial respiratory variables. We reconcile this surprising result with broader phylogenetic studies showing a lack of correlation between cell size and metabolic rate at the organismal level.

As one of the strongest selective forces, predation risk induces antipredator responses in prey that not only maximise survival probability but are energetically expensive. While these responses are known to affect foraging patterns and diet composition, the functional role of changes in dietary macronutrients remains unclear. We investigated the effect of dietary NPE (non-protein energy) concentration on the antipredator responses of the Indian rock agama Psammophilus dorsalis. In a manipulative experiment, wild-caught lizards were fed either a low or high NPE diet and exposed to repeated simulated predator attacks. We measured the space-use and hiding duration of lizards after each attack, as well as their circulating corticosterone concentrations at the end of the experiment. Predator exposure induced refuge use for all lizards. Diet had a context-dependent effect: lizards on the high NPE diet used riskier perch locations more frequently than those on low NPE diets, but only during safe periods and not during active threat. Physiologically, lizards on the low NPE diet had significantly higher baseline corticosterone levels, indicating a greater allostatic load. Overall, while dietary NPE did not alter reactive escape behaviour, it influenced the underlying physiological state and proactive behavioural decisions.

If an individuals niche is determined by its genotype, then competition for limiting resources should be most intense among individuals of the same genotype. Theory predicts this will act to maintain genetic variation, but whether this mechanism operates under natural conditions is unclear. Using long-term observations of a population of free-living Trinidadian guppies, we asked (i) whether competition was strongest between kin, and (ii) whether this process maintained genetic variation. Competition between kin was 1.5-1.8 times stronger than that between non-kin. This contributed to balancing selection: after [~]10 generations, variation was 29% higher than expected under drift. Our results show that relatedness can play a major role in structuring ecological competition, with broader consequences for theories of inclusive fitness. One-sentence summaryHeritable variation is maintained due to resource competition being more intense among kin.

Phenotypic differences among populations can arise through heritable genetic divergence, phenotypic plasticity, or both, making it difficult to determine whether trait-environment correlations observed in nature reflect adaptive evolution. Within threespine stickleback (Gasterosteus aculeatus) studies, numerous document morphological differences among allopatric-, parapatric-, and even sympatric populations. These phenotypic differences among populations are often correlated with diet and lake habitat (e.g., lake size), suggesting an adaptive value to the population differences. However, many studies of ecomorphological divergence in stickleback use wild-caught stickleback, which may differ due to evolution or plasticity. Although common garden experiments have confirmed that population differences can be heritable, such experiments typically entail small numbers of populations. Consequently, we still do not know to what extent well-known trait-environment correlations in stickleback are a result of evolution. To address this gap, we reared stickleback embryos from 27 lake populations on Vancouver Island, in a laboratory environment. Morphological differences among populations persist in common-garden fish, confirming a large role for divergent evolution. These heritable differences were associated with environmental variation among lakes, implying an adaptive value. However, some well-known trait-environment relationships in stickleback did not persist in common-garden fish and may be primarily plastic.

Empirical studies have demonstrated that mutation rates may change with individual condition, such as in the case of stress-induced mutagenesis. This has led to the hypothesis that condition-dependent (or "plastic") mutation rates could be selectively favoured, as the increased production of new mutants in times of maladaptation enhances evolvability, the ability to undergo adaptive evolution. However, while empirical evidence for condition-dependent mutation rates is accumulating, theoretical models studying their evolution are lacking. Here, we employ an individual-based simulation approach to examine the evolution of condition-dependent mutation rates in a changing environment. We find that condition-dependent mutation rates consistently evolve when the environment changes at an intermediate pace. Furthermore, populations with condition-dependent mutation rates are substantially better adapted to their (changing) environment. Finally, the evolutionary dynamics of condition-dependent mutation rates are both accelerated and destabilised when the mutation rate is self-referential (i.e., when mutator loci affect their own mutation rate). We conclude that condition-dependent mutation rates (and thus evolvability) can readily evolve in changing environments. Significance statementMutation provides the raw material for evolution. Mutation rates thus tune evolvability, the ability to undergo adaptive evolution: if mutation rates are too low, evolution is impeded; if mutation rates are too high, adaptive traits cannot be maintained. Using a theoretical model, we explore the evolution of plastic mutation rates that systematically depend on the condition of the organism and its environment. An example is stress-induced mutagenesis in bacteria, which is implicated in the evolution of antibiotic resistance. We show that plastic mutation rates readily evolve, providing "well-timed" variation specifically when organisms are poorly adapted. Such plastic mutation rates thus facilitate better adaptation to changing environments, and their evolution provides an example of evolvability itself evolving.

Understanding how divergence in reproductive traits can promote speciation remains a fundamental question in evolutionary biology. Sperm morphology and kinematics diverge rapidly across species. However, the effect of hybridization between recently diverged species on sperm traits remains unclear, limiting our understanding of how reproductive isolation evolves. Here, we evaluated sperm morphology, kinematics, and trait integration in species of a young (~10,000 years), sympatric Cyprinodon pupfish radiation from San Salvador Island, Bahamas, as well as fertile advanced-generation hybrids between two of these species. We found significant divergence in flagellum length, midpiece area, and sperm velocity among species. In contrast, hybrids displayed transgressive kinematic profiles defined by high velocities, reduced path curvature, and distinct patterns of sperm kinematic integration. Our findings suggest that hybridization between recently diverged species may reorganize the underlying control of sperm locomotor mechanisms, generating novel phenotypes that could contribute to reproductive isolation in the early stages of speciation.

The evolutionary patterns of trait diversification provide insights into the function of the trait. Early burst of trait evolution is often associated with adaptive radiation, rapidly diversifying the trait in response to vacant niches followed by the slowdown of the diversification with niche filling, whereas late burst is more likely to be associated with sexual selection, possibly contributing to reproductive barriers between closely related species. Here, we studied the diversification of tail fork depth through time in hirundines to infer its function, which remains unclear due to the competing two alternative hypotheses: the sexual selection hypothesis, which is a classic explanation of deeply forked tails, proposed that this trait has evolved via sexual selection, which was then challenged by the viability selection hypothesis, which proposed that deeply forked tails have mainly evolved via viability selection for enhancing aerodynamic performance during aerial foraging on large prey. We found a late burst of tail fork depth, but not of bill length, i.e., an index of prey size. The observed pattern is consistent with the sexual selection hypothesis but not with the viability selection hypothesis.

Phenotypic plasticity allows organisms to mitigate early-life adversity through compensatory growth, yet the long-term costs of such "catch-up" trajectories remain poorly understood, particularly when driven by social factors. While most research focuses on nutritionally induced compensation, we investigate how early social competition--independent of resource availability--shapes adult life-history trade-offs in the guppy (Poecilia reticulata). Our results show that scramble competition among peers during early development triggers compensatory growth once social constraints are removed. Crucially, we reveal a hidden reproductive cost: males exhibiting higher compensatory growth reach a similar adult size but produce significantly fewer sperm at maturity. This deficit persists even when controlling for adult body size, indicating a direct trade-off between somatic recovery and ejaculate investment. Furthermore, we find a negative association between gonopodium length and sperm count, suggesting competing allocations between pre- and postcopulatory traits during growth. These findings reveal a cryptic cost of compensatory growth, where adult morphology conceals underlying differences in reproductive quality. By demonstrating that social environments alone can recalibrate life-history trajectories, we highlight the "ghosts of competition past" as critical determinants of fitness. Our study underscores the necessity of considering ontogenetic history to fully understand the evolution of sexually selected traits in social vertebrates.

Injuries and infections pose a significant threat to fitness. Animals cope with this problem by performing self-medication or receiving social care from members of the group. While the benefits of wound care in increasing survival are clear, the forces driving the evolution of these behaviours are not fully understood. Contrary to the current hypothesis that social wound care is more likely to evolve in small groups due to the high relative value of an individual, we demonstrate that group size is not necessary for its evolution or retention. Instead, our theoretical model formalises how injury rate and lethality are fundamental drivers of care rather than group size. This is further evidenced by the presence of wound care in the army ant Eciton burchellii, a species with colonies of [~]1 million ants that hunts pugnacious prey. Here, wound care significantly increased survival in ants with infected wounds, occurring in two phases: direct care at the raiding site, and treatment with antimicrobial secretions in the bivouac. This species is the first to provide on-site care, thereby minimising the latency to receive care and thus potentially the likelihood of lethal wound infection. Our findings reject the notion that small group size is necessary for the evolution or retention of social wound care, revealing instead that injury-driven care can be a widespread and adaptive feature of even the largest insect societies. Significance StatementInjuries and infections threaten survival, but animals can counter these dangers through self-medication or social care. It has been suggested that helping behaviours directed towards vulnerable or injured individuals, such as social wound care, are more likely to evolve in small groups. This study in an army ant with [~]1 million workers shows otherwise, with injury frequency likely being the key component for the evolution or retention of wound-care behaviours. The unique strategy of on-site care at the raiding site, followed by antimicrobial care inside the bivouac, significantly improved survival outcomes. Our theoretical model further shows that even at low rates of care, fitness benefits are high, suggesting that social wound care may be far more widespread than previously thought.