The American Naturalist

Animal weapons are ecologically important traits that mediate contests over limiting resources and can strongly influence survival and reproduction. Weapon traits often exhibit substantial intraspecific morphological diversity, raising questions about the ecological drivers of this variation. Acrorhagi are weapons produced by sea anemones that are used in intraspecific territorial encounters. Although acrorhagial morphology varies widely within species, patterns of intraspecific variation remain poorly characterized, and the extent to which such variation reflects differences in local intraspecific competition is unclear. Here, we conduct morphometric analyses to characterize within-population variation and allometry in acrorhagial traits of the solitary anemone Anthopleura sola. We show that these traits covary with habitats differing in conspecific density. The number of acrorhagi scaled positively with body size, and individuals occupying a high-density habitat tended to possess more acrorhagi than did similar sized individuals from a low-density habitat. In addition, anemones from high-density habitats exhibited longer acrorhagial cnidae, a pattern that was not explained by differences in body size or acrorhagial density. Together, these results suggest that competitive context influences weapon-related traits at multiple levels of biological organization, potentially via phenotypic plasticity or selective processes. More broadly, our findings highlight how fine-scale ecological variation may contribute to the maintenance of trait diversity within and across species.

Many mobile animals move to locate and consume resources, making energy gain and growth dependent on activity. Yet the role of activity in shaping predator-prey interactions in food webs has not been broadly considered. Here, we synthesize empirical examples to examine how three activity traits (mean, variance, and timing) vary among taxa (fish, mammals, birds) and between predators and prey across temporal scales. We then use predator-prey models to explore how these diverse activity patterns influence stability. Motivated by emerging activity patterns, our theory shows that fluctuating activity rates can drive predator-prey interaction strengths with major consequences for stability. Future research is needed on activity trait patterning, links between activity and attack rates, and the consequences of activity for predator-prey interactions to whole food webs. This is especially critical as human-driven changes to abiotic cues increasingly alter animal activity rates and may rewire food webs.

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.

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.

Despite sharing the same genes and the same environment, individuals often develop substantial phenotypic differences. While this pattern has been documented across diverse species and traits, the processes giving rise to this "stochastic" or non-shared environmental variation remain unclear. Recent mathematical models of development in which phenotypes are gradually constructed may offer some clues. These models show that imperfect environmental cues can generate striking variation in developmental trajectories and adult phenotypes. At the population level, such imperfect cues produce increasing stability of individual differences across ontogeny (e.g. animal personality) and patterned distributions of mature phenotypes (e.g. normal or skewed) that resemble those observed in real organisms. Our paper synthesizes existing models in which stochastic phenotypic variation arises solely as a by-product of mechanisms missing their phenotypic targets because of imperfect cues. We then link these models to related, but independent, mathematical theory exploring the environmental conditions under which stochastic phenotypic variation is favoured by natural selection. Our integration shows that stochastic sampling is often favoured over classic bet-hedging strategies involving non-plastic generalist or specialist strategies. Our findings provide new directions of research on stochastic sampling as a mechanism for adaptive stochastic variation within and across generations.

Biotic interactions can drive evolutionary diversification, but the underlying mechanisms differ depending on the type of interaction. For instance, Ehrlich and Ravens escape-and-radiate coevolution provides a pathway of diversification in antagonistic interactions, whereas in mutualistic networks, coevolution is hypothesized to result in trait convergence rather than diversification. The combined effect of mutualism and antagonism on diversification remains unclear, even though organisms naturally engage in multiple types of interactions simultaneously. Using an eco-evolutionary simulation model, we investigate diversification in tripartite ecological networks such as plant-pollinator-herbivore networks. We find that diversification patterns vary according to the way mutualism and antagonism are connected on the trait level. If the two interactions are governed by uncorrelated plant traits, we observe little diversification in the mutualistic and substantial diversification in the antagonistic subnetwork. By contrast, if the same plant trait mediates both mutualism and antagonism (an example of ecological pleiotropy), diversification rates in all guilds become interdependent. In this case, even the mutualistic guild diversifies considerably when antagonism is strong, while strong mutualism restricts diversification also in the antagonistic guild. Our study underlines that the inclusion of multiple interaction types is necessary to advance our understanding of evolutionary dynamics in ecological networks.

Sexual selection is a major evolutionary force, yet its demographic consequences remain unclear. While experimental studies often report positive effects of sexual selection on traits linked to population performance, comparative studies often find null or negative associations with population persistence. One explanation for this discrepancy is that the demographic consequences of sexual selection depend on ecological context, particularly variation in mortality and fecundity. Here, we used six decades of abundance data and test whether sexual selection predicts population trends across 738 bird species from Europe and North America. We quantify sexual selection using complementary proxies capturing different components of sexual selection: mating system, sexual dichromatism, sexual size dimorphism and relative testes mass. We further assess whether the effect of sexual selection in population trends is mediated by mortality and fecundity. Across all proxies, we found no evidence that sexual selection is associated with population trends. This result is consistent across continents and robust to variation in mortality and fecundity. Our findings suggest that, despite its central role in shaping phenotypic evolution, sexual selection does not translate into consistent effects on long-term population trends at macroecological scales. More broadly, these results highlight a potential disconnect between evolutionary processes and population dynamics.

Habitat complexity (HC) in part determines the diversity, stability, and behavior of food webs and can influence predation according to a wide variety of functional relationships. Many aquatic species provide habitat complexity and are also consumed by other species (e.g., macrophytes, corals, mussels). However, food web theory does not readily account for these species that act as edible habitat complexity (EHC). Here, we combine existing theory on predator-prey interactions, HC, and prey switching to describe the role of EHC in benthic food web models. We dissect feedback loops in each model to demonstrate how self-regulation of the prey species, mediated by species densities and HC, drives that food webs behavior. HC can stabilize predator-prey interactions by coupling prey self-regulation with HC self-regulation. EHC can further stabilize predator-prey interactions across a wide variety of "HC functions" that relate HC to predation rates. Significance StatementHabitat complexity (HC) plays a critical role in trophic interactions, population dynamics, and food web stability. However, little theory exists to describe edible habitat complexity (EHC), where a species is both consumed and confers habitat complexity for other species. We provide a series of models demonstrating how HC and EHC alter the population dynamics and stability of simple aquatic food webs. HC is strongly stabilizing in food webs by providing safety in rarity for prey. EHC provides safety in rarity for both prey and the EHC species because their predators are omnivorous. Given the prevalence of EHC species in aquatic systems (e.g., macrophytes, corals, mussels), our models demonstrate the importance of maintaining EHC species in aquatic systems for stable food webs.

Existing theory examining the coevolutionary dynamics of species range borders assumes random dispersal, which causes maladaptive gene flow from the range core to the range margins and contributes to the formation of range limits. However, dispersal is unlikely to be random for many organisms in nature, calling into question existing theoretical predictions. For example, if individuals exhibit phenotype-dependent adaptive dispersal strategies such as matching habitat choice, then the resulting adaptive gene flow toward species range margins could facilitate range expansions and potentially prevent the formation of range limits by interspecific competition. To test this idea, we use a comprehensive mathematical model to develop a quantitative theory of range border coevolution that incorporates phenotype-optimal dispersal--a particular form of matching habitat choice in which individuals follow the gradient in an environmental optimum phenotype to settle in the habit best suited for their phenotype. We find that instead of preventing competitively formed range limits, adaptive dispersal leads to sharper range limits and reduced character displacement in sympatry. These differences are particularly remarkable when natural selection is weak, when individuals are specialized in their resource use, or when individuals are highly sensitive to environmental conditions. We show that matching habitat choice causes backward edge-to-core movements which dynamically interact with the effects of interspecific competition to establish the range limits. Thus, the formation of range limits by interspecific competition is robust to assumptions about individual dispersal. Further, our results identify the competitive advantage of evolving matching habitat choice in steep environmental gradients, especially for slowly-growing species in rapidly fluctuating climates.

Species tolerating the same environmental conditions can potentially colonize and thrive in the same habitats and eco-regions. Are any pair of those species equally probable to co-occur in the same community? Can we quantify the propensity of two species to co-occur together? Here, we focus on a simple but largely overlooked community-level pattern: the co-occurrence-occupancy curve, which relates the tendency of species to co-occur with others to their total occupancy across sites. We first define this empirical curve and then derive its expected shape under a random null model that assumes site equivalence and species independence. Building on these results, we introduce the Species Association Index (SAI), an occupancy-standardized measure that quantifies the tendency of a species to associate with others independently of its overall frequency of occurrence. The SAI enables meaningful comparisons among species with contrasting occupancies and provides a transparent benchmark against which departures from neutrality can be assessed. We illustrate the approach using two contrasting systems--tropical rain forest trees on Barro Colorado Island and organisms from Mediterranean rocky shores--highlighting both the generality of the co-occurrence-occupancy framework and its limitations.

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.

Ecological speciation is now regarded as one of the primary processes by which new species are generated. Adaptive divergence in allopatry begins this process, but it is often unclear when and how mechanisms that promote reproductive isolation, such as assortative mating and selection against hybrids, evolve. Here, we test for evidence of these mechanisms across replicated secondary contact experiments in natural settings. We introduced four to eight allopatric populations of threespine stickleback (Gasterosteus aculeatus), in both single-ecotype and mixed-ecotype treatments, into nine natural lakes, after which we inferred mating patterns by genotyping the resulting F1 generation. Contrary to expectations from the literature, we found no evidence of assortative mating or partial reproductive isolation among the introduced source populations. Instead, we detected evidence of disassortative mating by source population in three lakes and some evidence of disassortative mating by ecotype in one lake. These mating patterns were both context-dependent and population-dependent, varying substantially across lakes receiving the same source populations, and with some source populations generally displaying greater tendencies for disassortment. The absence of positive assortative mating in any replicate demonstrates that adaptive divergence in allopatry alone might be insufficient to generateassortative mating in many cases, while the possibility of disassortative mating in these contexts poses an additional hurdle on the path toward speciation.

Parasites play an outsized role in mediating the persistence and stability of host populations. Flour beetles (Tribolium spp.) have long served as classic examples of population dynamics under both disease-free and infected conditions, with elegant combinations of theory and experiments demonstrating, for example, that cannibalism rates can push populations from stability to chaos. As with most organisms in nature, however, flour beetles rarely face just one parasite species, and co-infecting parasites can antagonize or facilitate each other through resources and immunity. To test the prediction that non-neutral interactions would qualitatively alter population stability, we first raised flour beetles (Tribolium castaneum) in infection-free, single-infection, or coinfection microcosms and quantified relative prevalence and parasite intensity. Next, we reworked a classic stage-structured discrete-time model to include single and multiple infections and performed sensitivity and bifurcation analyses to identify the most important (co)infection-associated parameters for population stability. The model predicts that stability is highly sensitive to parasite transmission mode regardless of infection multiplicity, but facilitation among parasites rapidly drives populations into oscillations and chaos under realistic conditions. This study identifies an important mechanism for explaining population variability and highlights the importance of within-host mechanisms for driving dynamics at higher levels of biological organization.

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.

O_LISeasonal patterns of species appearances constitute a major component of diversity variation. Theory attributes this phenological structuring of communities to the alignment of life cycles to suitable moments and to constraints of seasonality on development, yet the specific mechanisms operating across taxa remain largely unresolved. In insects, body size and colour are key functional traits that contribute to driving spatial community assembly through their link to thermoregulatory performance and development. C_LIO_LIHere we analyse variation in mean body size and colour lightness of 483 butterfly assemblages across Great Britain and throughout the season to test whether trait alignment with seasonal environment and developmental constraints may shape the phenological structuring of communities. C_LIO_LIBoth body size and body colour varied more along season than across space, emphasizing the importance of phenology on diversity variation. Body size was larger early and late in the season, i.e. under conditions of low temperature and solar radiation. This pattern contrasted with the spatial trends found and was driven by species overwintering as adults, which we interpret as being likely due to energetic constraints. Body colour, conversely, was darker early and late in the season, mirroring the spatial pattern found, and suggesting a thermoregulatory alignment with seasonal conditions. Furthermore, covariation between body size and colour suggests a thermoregulatory interaction between both traits. C_LIO_LIOur findings suggest that life-cycle constraints and seasonal thermoregulatory alignment contribute to shaping the phenological structure of insect communities. C_LI

Darwinian fitness is equated here with invasion fitness and defined as the quantity determining the fate--certain extinction or possible spread--of a single mutant type. We derive it, together with its phenotypic derivative, for evolution in group-structured populations under limited genetic mixing, where the demography of the focal species and its environment is modeled as a discrete-time stochastic process. Reproduction, physiological development, dispersal, and survival are influenced by interactions within and between groups and by environmental fluctuations within and across generations. Using multitype branching processes in random environments, we show that invasion fitness is predicted by a stochastic growth rate that can be represented biologically in two meaningful genealogical ways. First, as the long-term geometric mean of the expected per-capita number of mutant copies produced per time step by a representative member of the mutant lineage. Second, as the the long-term geometric mean of the expected reproductive-value-weighted per-capita number of mutant copies produced by such an individual. This latter representation is useful for computing the phenotypic directional derivative of invasion fitness. Moreover, this derivative can be written as an actor-centered inclusive-fitness effect derived from properties of the resident population process. This effect depends on class-specific fitness differentials, relatedness, reproductive values, and class frequencies. However, unless generation- and class-specific fitness defines a stochastic matrix, the derivative does not separate stochastic reproductive values from relatedness and class frequencies, and must be evaluated by simulations. In summary, we formalize invasion fitness biologically quite generally and show how Hamiltons marginal rule is deduced from it.

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.

Phenotypic variation within a single genotype under the same environment (intragenetic variation), the biologically meaningful part of Verror, is frequently treated as a statistical nuisance rather than a biological reality, yet it represents an evolutionary driver of fitness that remains poorly integrated into evolutionary theory. The mechanism that translates such stochasticity into deterministic developmental phenotypic outcomes is not well understood. Here, we test a cumulative stochasticity model using wing polyphenism of the pea aphid (Acyrthosiphon pisum), where asexual mothers produce winged instead of wingless offspring in response to tactile cues. The model predicts that stochastic variation in maternal locomotor behavior alters the rate of tactile cue accumulation and thereby influences the probability of producing winged offspring. We demonstrate that maternal locomotor activity acts as a "stochastic pacemaker", where an individuals movement determines the rate at which it actively constructs its environment and accumulates environmental cues. Our results reveal that genotypes differ significantly in both mobility and the temporal pattern of wing induction, with behavioral variation explaining approximately 20% of the total phenotypic variance across genotypes. Crucially, we show that maternal mobility increases progressively during crowding, accompanied by significant temporal heteroscedasticity. This expanding variance and increase in mean suggest that initial, trivial stochasticity is magnified into systematic behavioral divergence through the integration of environmental signals. By demonstrating that total accumulated locomotor activity predicts offspring phenotype, we provide a mechanistic bridge between transient behavioral noise and stable morphological shifts. More broadly, our work reveals that Verror is a dynamic product of behavioral history, suggesting a fundamental role for individual-level niche construction in generating macro-phenotypic diversity.

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.

Batesian mimicry is a defensive adaptation where predators learn to avoid aposematic prey and generalize their warning signals to phenotypically similar mimics. The phenotypic accuracy needed for mimics to benefit from this adaptation depends on the relative densities of models and mimics and the models unpalatability. As aposematic models become more unpalatable or more common relative to their mimics, warning signals become stronger, allowing even poor mimics to benefit. However, few studies have disentangled the importance of relative frequencies of models and mimics from absolute density of the prey community (both models and mimics) in driving relaxed selection on imperfect mimics. Here, we test the hypothesis that increasing model unpalatability and absolute prey community density accelerates predator avoidance learning and enhances protection for imperfect mimics. Using replicas of the model Adelpha iphiclus (Linnaeus), its imperfect mimic Adelpha serpa (Boisduval), and the palatable control Junonia evarete (Cramer), we conducted field experiments that enhanced model unpalatability and doubled absolute prey density while maintaining a constant ratio of model, mimic, and control phenotypes. We found that enhanced model unpalatability and increased absolute density significantly reduced predation on all species, highlighting absolute community density as an underappreciated mechanism shaping selection on imperfect Batesian mimics.