The American Naturalist

In many animal species, individuals acquire knowledge from others that enhances their survival and reproduction. However, among the many available cultural exemplars, not all provide reliable information. Consequently, individuals tend to choose their exemplars selectively. One widespread pattern is a preference for older individuals, who may have accumulated valuable knowledge through life. Yet empirical studies also show that individuals frequently learn from age peers, suggesting that copying elders is not universally optimal. The ecological and social conditions that favor learning from elders rather than peers, therefore, remain unclear. Here, we investigate the evolutionary drivers of age-biased exemplar choice in age-structured populations where individuals accumulate knowledge over their lifespan. We develop a model that captures the coevolution of exemplar age choice and age-specific investments in social learning, individual learning, and the use of acquired knowledge for energy extraction. We show that selection promotes a progressive shift from social to individual learning and from learning to energy extraction with age. Exemplar age choice, in turn, evolves through a trade-off between targeting knowledgeable individuals and accessible ones. This trade-off leads young learners to learn preferentially from relatively young exemplars, who are common and still able to provide substantial amounts of novel knowledge, given learners limited knowledge at early ages. As individuals age, encountering exemplars with substantially novel knowledge becomes increasingly difficult. Consequently, as they age, individuals are expected to shift toward learning from older individuals, who possess more knowledge. Population, environment, and knowledge characteristics can shift this balance, generating a wide range of strategies from learning primarily from peers to consistently targeting the oldest individuals. In particular, learning from age peers is favored in populations with strong within-cohort interaction structure, high mortality, or high encounter rates, in unstable environments with rapid knowledge loss, and when knowledge is easily acquired or transmitted.

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.

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.

Why do some lineages diversify while others do not? This remains a central question in evolutionary ecology. A long-standing assumption, dating to Darwin and embedded in the Unified Neutral Theory of Biodiversity, holds that abundant species should speciate at higher rates. Conversely, theoretical and empirical work highlights the possibility that rare and dispersal-limited clades might be more prone to speciation. Using a birth-death-immigration model with protracted speciation in a multi-population landscape connected by limited dispersal, we show that abundance has a hump-shaped effect on probability of speciation. Our model reveals that intermediate abundance maximizes speciation probability because larger populations disperse more, swamping regional differentiation and inhibiting speciation completion, while smaller populations lack the persistence and incipient speciation needed to diversify. We find empirical support for this prediction with an analysis of data from arthropods endemic to Hawaii, where genus-level species richness shows a significant hump-shaped relationship with mean genus abundance. These findings provide a mechanistic explanation for a nuanced relationship between abundance and diversification.

Plant economics traits, such as leaf mass per unit leaf area (LMA) and stem specific density (SSD), capture diversity among plant species in how common tissues (leaf, wood, root) are constructed. These traits are key descriptors of plant strategy, yet it has proven difficult to explain this variation with theory and process-based models. Here we reveal a general explanation on why these economics traits vary with environment, through ontogeny, and with other plant traits. This explanation relies on three core assumptions: 1) plants seek to maximise growth rate, 2) growth rate can be decomposed into a product, and 3) there is a tradeoff between the efficiency of tissue construction and tissue turnover rate. Formulation of growth as a product is essential, as it causes the optimal value of an economics trait to vary with the plants biomass production rate, which means economics traits will naturally covary with the abiotic environment, the competitive context, and other strategical features of the plant. Finally, we show how a modification of the trait into plastic and non-plastic components alters the magnitude of intra-specific responses, aligning model responses with empirical trends. Broadly, our results help explain how plant form and function for a wide diversity of species is shaped to suit their environment and, moreover, they reveal insight into a general fast-slow spectrum (Reich 2014) with coordinated shifts among organs (leaf & stem) through tradeoffs between efficient tissue construction and turnover.

Most theory and empirical research on range expansion assumes populations spread into empty landscapes with abundant resources, however expanding populations are likely to compete with residents. In mathematical models, interspecific competition can lead to pushed wave dynamics, where expansions are driven mainly by individuals dispersing from the core, leading to steeper wavefronts and increased genetic diversity at the edge. These predictions are yet to be tested empirically, and the role of interspecific competition in mediating evolution during range expansion is unclear. We used an experimental system with two duckweed species to ask if interspecific competition leads to pushed-like dynamics and to assess how competition alters evolution during range expansion. We found that competition with a resident reduced expansion speed and absolute variance among replicate expansions, suggesting competition makes expansion speed more predictable. Interspecific competition also changed the relative frequencies of genotypes at the leading edge. While competition was associated with some features of pushed waves, genotype diversity did not vary between treatments. Our results demonstrate that demographic and evolutionary patterns associated with pushed waves may not be universal, and that incorporating selective pressures into future research on eco-evolutionary dynamics of range expansion is key to understanding spreading populations in nature.

Despite the ecological importance of ungulate migrations, we lack a complete understanding of why some ungulates migrate and others do not. Though progress has been made towards understanding differences across species and between populations, migratory behavior varies even within populations: in many populations, some individuals remain behind as residents (partial migration). Theoretical population-level work has suggested that these different migratory tactics can coexist, but such approaches stop short of providing insights into how individuals make the decision to stay or go each year. Using long-term data from three ungulate populations, we find that individuals probabilities of migrating are highly variable across years, which points to a non-trivial context-dependent decision-making process, whose underlying mechanisms must be probed via individual-level modeling. Drawing on existing knowledge, we propose a decision-making model of ungulate migration onset wherein individuals probabilistically decide to start migrating based on the local intensity of environmental and/or social cues. Residents arise as a robust collective organization phenomenon in our model. At sufficiently large population sizes, the number of residents is invariant with total population size, consistent with empirical patterns. Instead, resident numbers are influenced by the severity of the bad season, by relevant character differences among individuals, and by how individuals contribute and respond to environmental and/or social cues; for instance, when social cues contribute to decision-making in addition to environmental ones, fewer residents result, and migration is more likely to be complete. Overall, our model provides a potential mechanistic explanation for how residents might emerge within migratory ungulate populations.

Hosts defend themselves against parasites through resistance (reducing parasite burden) and tolerance (reducing the fitness cost of infection without affecting parasites). This distinction has important evolutionary implications: resistance is predicted to maintain polymorphism while tolerance tends to fix, and only resistance is expected to provoke parasite counter-adaptation. The reaction-norm framework, which infers tolerance from the slope of host fitness regressed on parasite burden, assumes that a shallow slope reflects parasite-independent host protection. We test this assumption using a within-host model in two variants: microparasites (Model 1, with within-host replication) and macroparasites (Model 2, without). Sublethal immunity impairs the host-exploitation rate of the parasite, reducing both growth and per-parasite virulence without killing them. We show that this generates systematic slope differences among host genotypes that the framework interprets as variation in tolerance. Furthermore, the ranking of slopes across genotypes reverses between linear and sigmoidal damage functions: under linear damage, the strongest immune responder appears most tolerant; under sigmoidal damage, the weakest responder does. Decomposition of the damage reduction shows that virulence reduction accounts for the majority of the effect across both model variants. Thus, the reaction-norm slope cannot determine whether host fitness is maintained by parasite-independent tissue protection or by sublethal impairment of parasites.

Thermal performance curves (TPCs) are widely used to investigate the effect of changes in body temperature on an organisms performance. Despite empirical evidence that temperature-dependent performance is ubiquitous across taxa, the field lacks models for how thermal performance evolves under realistic timeseries, genetic architectures, and physiological constraints. We address this gap by integrating a mathematical model with individual-based quantitative population genetic simulations. Our model can predict the evolutionary trajectory and shape of TPCs for any given thermal regime. Our model reproduces core properties of TPC evolution from previous studies such as the emergence of generalists in variable environments, but also explains why organisms may evolve TPCs that do not match their historical body temperature range. We uncover novel dynamics of adaptive tracking, the most notable being multi-generation lags between temperature and TPC parameters that can lead to unexpected correlations between the two. Our model predicts empirically observed patterns of adaptive tracking of critical thermal minimum in the invasive pest Drosophila suzukii, including individual-level variability and multi-generation lags with changing temperature. Our results also highlight the limitations of models that ignore factors that influence TPC evolution and individual variability, such as autocorrelation in temperature timeseries, effective population size, evolution of additive genetic correlation in TPC parameters, genetic architecture, and physiological constraints. Our flexible simulation model can incorporate these factors and help generate empirically testable hypotheses of how species will evolve in response to global climate change.

Rapid environmental change and biodiversity loss make it increasingly important to identify factors influencing population extinction risk. Previous studies examining how mating systems can affect persistence of populations under environmental stress generally report higher extinction risks in monogamous than polygynous systems but have largely ignored extra-pair copulations (EPC) and paternity (EPP), despite the prevalence of genetic polyandry in socially monogamous species. Here, using an individual-based model, we study how EPP in socially monogamous systems affects population resilience under directional environmental change. We assume that in socially monogamous species, both sexes carry costly sexual ornaments, the elaboration of which depends on the strength of preference. The effect of EPPs on extinction risk depended on the strength of mate preference, population size, and the degree to which homozygosity affected fitness. Systems with EPCs are not simply intermediate in resilience between strict monogamy and polygyny: the preference strength interacts with mating system, leading to superior resilience of EPC systems compared to strictly monogamous and polygynous systems when choosiness and the negative consequences of heterozygosity loss are low, and EPP rates are high. However, this benefit was reduced in small populations due to faster loss of heterozygosity. At high choosiness, EPC systems exhibited lower resilience than socially polygynous choice systems because the higher reproductive skew of the latter system allowed them to adapt faster while not suffering from the demographic consequences of sexual signaling costs borne by females. Overall, our results suggest that EPCs can enhance population resilience when females obtain fertilizations from higher-condition extra-pair males compared to systems without EPC.

Stable variation in public-good production can generate biological division of labor. Two key drivers are the size of interacting groups and the degree of assortment (relatedness) among individuals with similar investment levels. Here we extend adaptive-dynamic models of continuous public-goods investment by allowing assortment in group formation. We show that increasing group size typically enlarges the range of benefit and cost curvatures that permit evolutionary branching, whereas assortment tends to shrink this range and prevents branching under complete relatedness. For a broad class of models, branching requires diminishing marginal public benefits and diminishing marginal private costs, with costs decreasing faster than benefits. Finally, we analyze post-branching dynamics for one and two public goods, and find that assortment can stabilize the resulting two-type division of labor. Together, these results show how group size, assortment, and payoff curvature jointly determine when heterogeneity in public-goods production can evolve.

Permanent workers in social insects, who forgo reproduction to help others, are a defining feature of superorganisms and a major evolutionary transition. Most theories assume that helping in the natal nests is inherently mutually exclusive from dispersal to found a new colony. This assumption holds for many adult societies whose workers cannot molt and change castes (e.g., Hymenoptera), but not for juvenile societies whose workers may differentiate and disperse after a period of helping (e.g., termites). The evolutionary advantage of permanent workers remains unknown in such juvenile societies with developmental flexibility. Here we develop a demographic model in which individuals can disperse either before or after a period of helping, capturing reversible helpers and permanent workers in termites. We found that permanent workers are favored when colony growth is divided into distinct ergonomic and reproductive phases, even if their performance is the same as that of reversible helpers. Without this phase separation, there is no selective advantage for workers to lose dispersal for colony foundation. After the phase separation, on the other hand, permanent workers increase continuous demographic growth and evolve through kin selection. By mapping diverse termite social systems onto a continuous landscape of ontogeny, the model traces a pathway linking different social forms. These results generalize social evolution theory beyond adult-worker systems by providing a demographic mechanism that favors the loss of the reproductive option.

When encountering a predator, prey must choose between immobility and flight, a decision shaped by predator proximity, habitat structure, body size, and evolutionary history. Despite extensive work on optimal escape theory, few studies have jointly modelled both the decision to flee and the intensity of flight in a phylogenetic comparative framework. Here, we used a Bayesian phylogenetic hurdle log-normal model to analyze the probability of immobility and the conditional jump distance in 534 trials from 89 males across 17 Neotropical frog species (seven families), exposed to a simulated snake predator in three arenas of varying structural complexity. Physical contact with the predator (touch) was the strongest predictor, reducing immobility probability from 94% to 15% and increasing jump distance by 26%. Habitat complexity increased immobility (bush > leaf litter > empty), and frogs in open arenas jumped 31% farther. Larger-bodied species were substantially more likely to remain immobile but did not jump farther, indicating that body size determines strategy choice rather than locomotor magnitude. Phylogenetic signal was strong for both components (Pagels {lambda} = 0.80 for jump distance; {lambda} = 0.71 for immobility), with phylogeny accounting for 69-75% of variance. Species random effects formed a phylomorphospace in which fossorial species showed highest immobility and arboreal/torrent species favored active escape. Substantial individual-level variation in immobility tendency (25% of variance) provides a heritable substrate for ongoing selection. Frog antipredator strategies are jointly shaped by ecological context and evolutionary history; hurdle models offer a powerful framework for decomposing behavioral decisions. LAY SUMMARYWhen a predator approaches, prey must choose between staying still or fleeing -- a decision depending on body size, habitat, and shared evolutionary history. We exposed 17 frog species to a snake in arenas of varying vegetation cover. Frogs fled when touched but mostly stayed still when only approached; larger species and those in dense vegetation were most likely to remain immobile. These antipredator strategies were strongly shaped by frogs shared ancestry.

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.

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

A similar phenotype exhibited by both adults and juveniles is often considered a self-evident default state due to shared genes and similar ecological niches, and thus the function of adult-juvenile resemblance is rarely addressed. An adaptive explanation for adult-juvenile resemblance is that adults mimic juveniles to attract mates by exploiting their parental care behavior and to avoid agonistic intrasexual combat from rivals that tolerate juveniles (i.e., the juvenile-mimicry hypothesis). Using a phylogenetic comparative approach, we tested the juvenile-mimicry hypothesis in aerial foragers, swallows and martins (Aves: Hirundinidae), in which adults and juveniles frequently encounter one another in their open habitat. We predicted that, if adults mimic juveniles, adult-juvenile resemblance should be enhanced in species with many young (i.e., a large number of models in relation to mimics) as well as species with a few young (i.e., a default state with limited intensity of sexual selection). This prediction was confirmed by a quadratic relationship between number of juveniles and adult-juvenile resemblance. In addition, as predicted under the juvenile-mimicry hypothesis, adult-juvenile resemblance was enhanced in species with multiple broods, in which juvenile-mimicry would be particularly effective due to the mating period followed by juvenile production. The observed pattern could not be explained by sexual selection for male ornamentation alone (i.e., with no juvenile-mimicry) even when considering the cost of ornamentation. An alternative explanation that juveniles mimic adults is also unlikely, as the situation favors the opposite pattern. The current study therefore supports the juvenile-mimicry hypothesis, indicating an adaptive function of adult-juvenile resemblance.

Mark-recapture analyses on the delineation of natural populations between areas often assume random sampling, with a between/within (B/W) area resighting ratio that declines towards zero as the population components of two areas become more-and-more isolated from one another, with fewer-and-fewer individuals mixing between areas. I use an individual based population model split in two areas to simulate this result, analysing also for the potential effects of the space-time fidelity of the mark-recapture sampling in the areas. I find that small B/W resighting ratios--that traditionally is taken as evidence of population isolation--can easily be observed within a completely mixing population if a random sampling scheme is restricted in space and/or time. Random sampling within restricted areas and time windows is not sufficient to estimate mixing rates and population isolation between areas, unless the resighting rates are analysed by a method that accounts both for the space-time fidelity of the scientific sampling scheme and the space-time fidelity of the distributional behaviour of the individuals in the population.

Reproductive success requires allocating effort across lifespan in a manner that balances the risk of early mortality against the benefit of higher fecundity or parental expertise that increase with body size or age. Here we report a cross-taxonomic analysis of reproductive schedules in plants, animals, and humans, showing that peak reproductive effort consistently occurs at approximately 1/e (~37%) of species-specific maximum lifespan. The pattern is robust across major phylogenetic groups and independent of absolute lifespan. This convergence is both logically and numerically consistent with the optimal stopping fraction (1/e), which maximizes the probability of selecting a superior option under uncertainty by delaying commitment until 1/e of the available options have been examined. By integrating population dynamics and empirical data with a formal decision-theoretic model, our results suggest a striking previously unrecognized quantitative regularity linking lifespan and reproductive timing. These findings provide a unifying perspective on life-history evolution and suggest that complex biological scheduling strategies are governed by probabilistic principles.

Most plants require animal pollination to reproduce, prompting concern that pollinator declines immediately threaten plant populations. This concern is warranted if pollinator-mediated seed losses cause declines in plant population growth rates ({lambda}). However, demographic trade-offs might reduce the risk of population decline if seed loss improves performance elsewhere in the life cycle. We conducted a multi-year pollination manipulation on four species and measured how demographic vital rates and {lambda} responded. Seed responses did not predict net changes in {lambda}. Reduced pollination decreased seed production, but only caused a net decrease in {lambda} in one species; in the others, improved survival buffered {lambda}. Increased pollination boosted seed production, but at a cost to survival that caused a net reduction in {lambda} in three species. Our results highlight the importance of demographic trade-offs for understanding the impacts of pollinator declines on plant biodiversity and, more broadly, the population-level impacts of changing mutualisms.

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.