The American Naturalist

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.

Fishing deeply alters marine food webs structure and can drive the evolution of species traits, whether the species are directly targeted or not. Yet, studies rarely account for fisheries-induced evolution, and consequences are generally interpreted at the single-species level. Theory however predicts that eco-evolutionary dynamics within food webs can either promote biodiversity maintenance or accelerate its decline. In this study, we investigate how evolution affects the robustness of trophic networks under fishing pressure. Modifying evolution speed and the allocation of fishing effort across 458 structurally distinct allometric networks enables us to show that evolution most often enhances robustness. Network evolutionary response however becomes more variable (and possibly negative) as evolutionary rates increase and when fishing preferentially targets predators. By contrast, fishing strategies that concentrate effort on lower trophic levels, or distribute it more evenly, promote network persistence through evolutionary rescue while substantially reducing the risk of evolutionary collapse. Moreover, our results appear to be sensitive to the main forces governing ecological dynamics within the network such as competition or predation intensity. Finally, the consequences of network evolution differ across trophic levels. Evolution often drives the collapse of higher trophic levels while simultaneously promoting evolutionary rescue and enhancing diversity at lower levels through increased diversification, thereby generating a trade-off between vertical diversity (number of trophic levels) and total diversity. This highlights the importance of accounting for evolutionary dynamics and food web functioning in fisheries management, and suggests that reducing predator mortality may help prevent network evolutionary collapse.

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.

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.

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

Fisheries-induced evolution (FIE) affects multiple life-history traits, most notably body size. This evolutionary response is often examined at the single-species level and attributed to direct size-selective harvesting. However, fishing also targets other community members, reshaping trophic interactions and thereby modifying evolutionary constraints due to community changes. Here, we disentangle two forms of fishing-induced selection on body size - direct, arising from size-selective harvesting within species individuals, and indirect, emerging from fishing-induced changes in community structure - and investigate how their interplay shapes evolutionary trajectories. Using an adaptive dynamics framework within a predator-prey model, we show that (i) community destructuring can either amplify or dampen the effects of intraspecific size-selectivity on body-size evolution, (ii) predator evolution is primarily driven by direct selection, whereas prey evolution is mostly constrained indirectly by community structure. We then extend our analysis using a stochastic framework and show that (iii) prey evolution allows the evolutionary rescue of predators, underscoring the importance of community context. Our results demonstrate that eco-evolutionary feedbacks can profoundly alter both community structure and fishery yields, strengthening calls to incorporate evolution into ecosystem-based fisheries management.

Revealing the genetic basis of local adaptation is a common goal of evolutionary biology, but despite theoretical progress, general expectations for the genetic architecture of local adaptation are still unclear. Theoretical analyses usually model simplified ecologies or simplified genetic architectures of adaptive traits, so the interplay of these factors is missing from our understanding. In this study, we use simulations to explore how the interplay of ecological and genetic parameters influences the evolution and genetic architecture of local adaptation. With these simulations, we ask: i) What are the features of alleles that made the largest contribution to local adaptation, and how are they affected by polygenicity of adaptive traits, migration rates, demographic history, and the spatial pattern of the environment? And ii) does allele age moderate the confounding effect from population structure in genotype-environmental associations (GEA)? We find that the frequency, number, and phenotypic effect size of locally adaptive alleles are sensitive to trait polygenicity and demographic history, and that these factors shape the evolutionary dynamics of local adaptation. We find that population expansions can leave legacies in the genetic architecture of local adaptation, reducing the expected number of adaptive alleles relative to models with constant population size, and this effect is long-lasting. Compared to range expansion, other ecological variables known to affect the genetic basis of local adaptation had limited effects. Finally, allele age moderated the confounding effect of population structure and modified the causal effect of environmental variables on genotypes. Alleles that arose around the time of environmental changes often made large contributions to local adaptation, but young alleles often had the highest false positive rates and were the most common age category. We describe how incorporating allele age and its interactions with population structure and environmental variables may increase the sensitivity and specificity of GEA analysis. Overall, this work demonstrates the critical importance that a species demographic history can have on its genetic architecture of local adaptation.

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.

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.

Parasite prevalence varies in time and space. Thus, hosts may escape infection by dispersing out of habitats where parasites are present. However, it is not clear if the advantage of avoiding parasites outweighs the cost of dispersing. Juvenile hosts are expected to be relatively protected from environmentally-transmitted parasites, and we hypothesize that this age bias in transmission could magnify the benefits of juvenile (i.e., natal) dispersal. We tested these ideas in the model nematode Caenorhabditis elegans, a host with discrete life stages and natal dispersal, and its environmentally transmitted microsporidian parasite Nematocida parisii. We found that under standardized exposure conditions, larger C. elegans individuals (corresponding to older life stages) acquired many more parasites than smaller (younger) individuals. We found this same bias during multigeneration epidemics, especially during early stages of the epidemics. We also found that C. elegans dispersal larvae were less likely to be infected and harbored less severe infections than the population mean. We conclude that the early stages of an epidemic can provide young hosts with a window of opportunity to escape infection by dispersing.

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

Many demographic models assume that only females matter for population dynamics. However, theory and evidence of sexual conflict suggest that males can affect female fitness through mating competition between and within the sexes, yet it is unclear how such effects may influence population dynamics. We used experimental population demography to understand how sexual conflict affects offspring recruitment in Drosophila melanogaster, a model species for studying the evolution of sexual conflict. By manipulating sex ratio and male/female density independently in a response surface design we found that increasing male density, and thereby the intensity of sexual conflict, led to fewer offspring per female, but that effect was nearly half the strength of female density dependence. Consistent with this, our best fitting birth function showed female dominance of births with sex-specific density dependence, indicating that males have a demographic effect even if females have demographic dominance. Our results confirm that females have a larger influence than males on offspring recruitment, however, more importantly our result increases our understanding about the demographic effects males have through sexual conflict.

Species introductions and transplants offer powerful contexts to understand evolutionary patterns and processes, and they are increasingly critical for conservation. However, introduction success varies widely, and predicting outcomes remains challenging. Introducing multiple source populations should increase the chance of success, while also providing an opportunity to explore the factors that predict success of individual source populations in the same environment. We used replicated, mixed-population introductions of >12,000 threespine stickleback (Gasterosteus aculeatus) to test whether source population success could be predicted by environmental matching between source and recipient environments and/or by intrinsic source population characteristics. We introduced four to eight source populations of stickleback into each of nine natural lakes and tracked their relative success over the following two years (up to two generations). Source population success was largely consistent across lakes, despite divergent environmental conditions. These results point to the importance of intrinsic source population characteristics rather than environmental matching in predicting introduction success in natural settings. Source populations that were consistently successful tended to have greater stress tolerance (mortality rate during translocation) and higher genetic diversity, though these relationships were not conclusive. Our study highlights the value of considering factors that generate fitness differences independent of environmental contexts in predicting ecological and evolutionary dynamics and planning conservation programs. Significance StatementPredicting which populations will succeed when introduced to new environments is a central challenge in ecology, evolution, and conservation. Environmental conditions are often assumed to be crucial in determining which populations succeed, given the expectation that populations preadapted to local conditions should perform best. We test this assumption by introducing >12,000 threespine stickleback fish from up to eight source populations into nine natural lakes spanning diverse environmental conditions. We show that the relative success of individual source populations was remarkably consistent across lakes and environmental conditions, indicating that some populations are intrinsically better suited to introductions. Our findings underscore the importance of considering intrinsic population characteristics alongside environmental conditions when predicting ecological and evolutionary outcomes and guiding conservation efforts.

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.

An organisms life history strategy is an attempt to optimize fitness, given environmental constraints and inherent demographic tradeoffs. As such, life history helps to shape an organisms ecological and evolutionary responses to environmental change. However, life history can also be shaped by the environment, as the organisms demographic rates respond--directly or through tradeoffs--to the new conditions. This feedback between life history and environment remains poorly understood, limiting our ability to predict the outcomes of environmental change. Here, we studied the effects of environmental change - specifically altered pollination services - on four perennial plant species. We conducted a field-based demography experiment that subjected naturally occurring populations of Delphinium nuttallianum, Hydrophyllum fendleri, Potentilla pulcherrima and Erigeron speciosus to three pollination treatments: ambient (control), reduced, or increased pollination. We estimated population growth rate ({lambda}) and 11 metrics describing life history strategy and demographic resilience from an Integral Projection Model we constructed for each species and parameterized with 4-5 years of census data. Although most life history metrics responded idiosyncratically to pollination treatment, we found consistent effects of pollination on generation time, longevity and, in three of four species, recovery time. Specifically, reduced pollination led to increased longevity, generation time, and recovery time, and increased pollination led to the opposite. These changes in life history resemble shifts along the slow-fast continuum; reduced pollination led to slower lives and increased pollination led to faster lives. This is consequential because generation time and longevity influence short- and long-term population dynamics - for example, by affecting demographic stochasticity and sensitivity to environmental stochasticity, or rates of adaptation to novel conditions. Notably, these changes occurred largely independent from changes in population growth. Altogether, our results highlight changes in life history as an important but underappreciated consequence of environmental change.

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.

Understanding ecological drivers of reproductive success is crucial to predict whether natural populations can cope with the pace of anthropogenically driven environmental change. In marine ecosystems, this knowledge is difficult to acquire due to the lack of tractable field systems. Here, we took advantage of the nest-brooding behavior of the two-spotted goby Pomatoschistus flavescens, an important planktivorous fish in Scandinavian coastal ecosystems, to study its reproduction across the steep climatic gradient of its natural range. We deployed 360 artificial nests in the field, covering six populations during the breeding season of 2022. We found that climate explained differences among populations in the phenotypes of nest-holding males, and in the impact of both marine growth and parental cannibalism on the broods. In addition, climate affected egg density and diameter. Despite these ecological effects, and although populations differed in average male reproductive success, reproductive success was not influenced by climate. Instead, it was largely determined by competition occurring at the local scale, in particular through the acquisition of high-quality nests, which was itself affected by the relative size of males within the local pool. We propose that the frequency-dependent nature of mating competition may buffer reproductive success against climatic influence in P. flavescens, and discuss the potential generality of such mechanisms and implications for population resilience.

The Allee effect is a phenomenon where individual fitness is reduced in small populations, for example because of mate-finding difficulties or increased predation. Allee effects matter in conservation biology because they can drive small populations to extinction. The severity of Allee effects can depend on traits such as mate-search rate and defense against predators. Many natural populations exhibit considerable intraspecific trait variation (ITV) in such traits, but most studies so far assume these traits to be constant. Thus the impact of ITV on populations with Allee effect is largely unknown. Here we create two individual-based stochastic models that simulate a small population experiencing either a mate-finding Allee effect or a predator-driven Allee effect. We analyze how ITV, trait inheritance, and mutation affect the proportion of surviving populations. Under the mate-finding Allee effect, higher ITV hindered population survival and increased Allee thresholds. This can be explained by Jensens inequality and the negative curvature of the mate-finding function. Under the predator-driven Allee effect, ITV effects were weak, but higher mutation standard deviations were beneficial, likely because they provided more substrate for selection to act on. We thus recommend to take into account ITV when dealing with threatened populations with an Allee effect.

Repeated divergence across contrasting habitats is widely used to infer natural selection and local adaptation. However, such inferences remain inherently correlative and capture only adaptation shared within habitat types, thereby missing site-specific adaptation among populations from the same habitat type. Field transplant experiments test adaptation more directly by measuring fitness in nature, but they are typically limited to pairwise reciprocal exchanges between populations and therefore cannot separate the contributions of shared habitat-level and site-specific adaptation to fitness. Here, we overcome these limitations by extending the typical transplant framework to include multiple populations transplanted both within and across habitat types. We apply this framework to lake-stream stickleback, a classic system for studying local adaptation via repeated divergence. Specifically, we transplanted laboratory-reared fish from a panmictic lake population and four independently evolving stream populations into one lake and two stream sites. Stream fish outperformed lake fish in streams and vice versa, providing evidence for adaptive lake-stream divergence. Strikingly, local stream fish also outperformed foreign stream fish at both stream sites. This site-specific advantage was twice as large as the advantage of foreign stream fish over lake fish, which reflects the fitness benefit of shared stream adaptation. These results show that in this system, the majority of fitness-relevant evolutionary variation is site-specific and therefore missed by approaches that rely on repeated divergence to infer adaptation. More broadly, this underscores the importance of ecological scale for understanding adaptation and evolutionary predictability.

We provide a general theoretical explanation for a longstanding result in spatial ecology: weak dispersal among habitat patches promotes local biodiversity. Using analytical approximations of spatial Lotka-Volterra competition models, we show that species persistence in heterogeneous landscapes can be expressed as a function of regional abundance and local invasion growth rates. We further demonstrate that local multispecies coexistence is governed by the feasibility domain, linking spatial coexistence to a structural property of nonspatial competitive systems. Together, these results explain why weak dispersal increases local species richness and why this effect strengthens with landscape size. We test these predictions using numerical simulations and find that the theory breaks down only when both dispersal and competitive interactions are very strong, in which case dispersal has a unimodal effect on coexistence. In contrast, landscape size retains a positive effect on coexistence whenever an effect is detectable. We then apply the theory to long-term data from a natural Daphnia metacommunity. We detect strong preemptive competition among species and find no detectable effect of dispersal rate on local coexistence, whereas species co-occurrence increases with local landscape size, as predicted by theory. Together, our results identify how dispersal, interaction strength, and landscape size jointly regulate biodiversity in competitive systems.