AbstractGradient variation evolves when environmental and genotypic effects on a phenotype covary positively (cogradient variation) or negatively (countergradient variation) across locations, whereas gene-by-environment interactions (G × E) reflect nonadditive genetic and environmental influences on phenotypes. Spatial covariance in environmental and genotypic effects (Cov) shapes variation in quantitative traits, facilitates local adaptation, and provides insights into eco-evolutionary dynamics. Yet several debates regarding gradient variation remain unresolved, including whether qualitative patterns of reaction norms accurately reflect Cov, whether cogradient or countergradient variation occurs more frequently than G × E, and whether general patterns emerge according to taxonomic groups, forms of environmental gradient, or trait types. We conducted a quantitative survey of 556 phenotypes and measured Cov and G × E across various phenotypes, taxa, and environmental gradients. We found that the qualitative assessment of reaction norms was unreliable for identifying Cov and that Cov occurred as frequently as G × E. No distinct patterns in Cov emerged across environmental, taxonomic, or trait-based groups. Our results challenge prevailing views regarding Cov and suggest that gradient variation can evolve under any environmental condition, taxonomic grouping, or trait type. We suggest that broader application of quantitative methods for Cov across diverse systems will enhance our understanding of Cov in nature.

AbstractNatural selection is widely considered responsible for the fit between organisms and their environment. Lizard limb length variation is a paradigmatic example: studies have shown that limb length differences tightly correlate with habitat use among species, while small differences in limb length between individuals can affect biomechanical function, fitness, and survival within populations. It has therefore been surprising for many field biologists to find otherwise-healthy wild lizards with damaged or missing limbs, appearing to challenge associated expectations of substantial fitness costs. We document limb loss (from a foot to an entire limb) in 58 lizard species, with all cases showing healed limbs and many lizards appearing robust and healthy. Data indicate that limb-deficient lizards typically comprise less than 1% of populations and often exhibit body condition, sprint speed performance, and survival comparable to limb-intact individuals. We discuss the implications of these findings for how evolutionary adaptation is studied and understood in natural populations and provide a perspective on conventional assumptions about the strength and ubiquity of selection pressures on seemingly critical traits. Is natural selection always as omnipresent as Darwin envisioned it to be?

AbstractSince the late 1890s up until today, how phenotypic plasticity interacts with genetic adaptation has been a debated issue. Proponents of a positive causal role of phenotypic plasticity-James M. Baldwin in the first place-supported the view that in altered environmental conditions, phenotypic plasticity is a key factor allowing a population to avoid extinction and then genetic evolution to catch up ("original Baldwin effect" [OBE]). Opponents, such as Ernst Mayr, regularly pointed out that phenotypic plasticity, by masking genetic variation, slows gene-level evolution ("Mayr effect" [ME]). For decades, this opposition remained only verbal and qualitative. To resolve it, we propose here a stochastic model that, following Baldwin's intuitive take, combines the minimal number of ingredients to account for extinction, selection, mutation, and plasticity. We study evolutionary rescue of the population (arrival and invasion of an adaptive genetic mutant) in the altered environment for different values of phenotypic plasticity, here quantified as the probability that the maladapted genotype develops into the adapted phenotype. Our claim is that OBE can be a genuine evolutionary mechanism, depending on the level of phenotypic plasticity with respect to a threshold value . When , increasing promotes evolutionary rescue by delaying extinction ("strong" OBE); when , plasticity sustains population survival and increasing has two antagonistic effects: to accelerate adaptation by increasing the supply of adaptive mutants ("weak" OBE, intermediate values of ) and to slow down adaptation by decreasing their fitness advantage (ME, high values of ).

AbstractEukaryogenesis is the prototypical example of an egalitarian evolutionary transition in individuality, and endosymbiosis, more generally, is central to the origins of many complex biological systems. Why do only some symbioses undergo such a transition, and how does the host-symbiont relationship change during this process? Here, we characterize endosymbiosis by two emergent collective-level properties: host and symbiont survival as a collective ("mutual dependence") and the level of synchronized reproduction ("reproductive cohesion"). Using adaptive dynamics, we study the evolution of the traits underlying these properties. First, by adding a carrying capacity for the collective population-a realism omitted in previous models-we find novel reasons why complete dependence or cohesion might not evolve, thus providing further theoretical support for the rarity of transitions in individuality. Second, our model suggests that asymmetries in evolutionary outcomes of hosts and symbionts can be explained by a difference in their population growth parameters, coupled with their shared fate when in a collective. Last, we show that during the early stages of an endosymbiosis, even if investments in dependence and cohesion are uncorrelated, mutual dependence arises faster than reproductive cohesion. Our results hence shed light on three aspects of endosymbiosis: coevolution between the host and symbiont, coevolution between dependence and cohesion, and ultimately the opportunity to undergo an evolutionary transition. Connecting to ecological factors, this work uncovers fundamental properties of endosymbioses, providing a clear way forward for theoretical and empirical investigations.

AbstractAnimals employ various mechanisms for camouflage, including color change, that may facilitate habitat use. However, the extent to which these mechanisms operate under nocturnal conditions is unclear. To investigate this, we combined a background-induced color change experiment with visual modeling to test whether altering backgrounds for a tropical tree frog () could induce short-term color change under nocturnal conditions to match the viewing background, as perceived by three predator classes: snakes, mammals, and birds. We demonstrated that frogs can change color multiple times from green to brown and back across grass and leaf litter backgrounds in dim conditions. Frog visual contrast varied by predator and background. Brown frogs matched against leaf litter across all predators, whereas green frogs were more variable and comparatively less well matched against grass. Notably, frogs achieved near-optimal color matching against both backgrounds for avian predators, with green frogs matching into grass and brown frogs matching into leaf litter. Our study provides evidence that undergoes rapid background-induced color changes at night maintaining effective camouflage, at least against avian predators. We emphasize the need to assess rapid color change against visually guided predators in natural conditions and the importance of understanding viewing conditions for illuminating the ecology and evolution of camouflage.

AbstractIn simultaneous hermaphrodites, resource availability and the temporal distribution of mates determine male and female fitness and optimal sex allocation. In insect-pollinated plants, we expect individuals to allocate more to their female function when they are large and more to their male function when other individuals have many ovules available to be fertilized. Here, we studied the dependence of sex allocation and male and female components of reproductive success on both the size and the timing of reproduction in the plant (Ranunculaceae), accounting for inbreeding depression and variation in the mating system. Female reproductive success depended positively on size, whereas male reproductive success depended on mate availability and the timing of flowering, as predicted. Moreover, male reproductive success trended to a saturating function of allocation to stamens, whereas female reproductive success was a slightly accelerating function of pistil production. These results provide new insights into the reproductive strategies of perennial plants and help to explain the joint strategy in of andromonoecy (the production of both male and bisexual flowers by individuals over the course of their lives) and gender diphasy (a shift between a male and a hermaphrodite phase among seasons).

AbstractMany ecological models treat exploitative competition in isolation from interference competition. Corresponding theory centers around the * rule, according to which consumers that share a single limiting resource cannot coexist. Here we model motile consumers that directly interfere while handling resources, mechanistically capturing both exploitative and interference competition. Our analytical coexistence conditions show that interference competition readily promotes coexistence. In contrast to previous theory, coexistence does not require intraspecific interference propensities to exceed interspecific interference propensities or for interference behaviors to carry a direct (rather than merely an opportunity) cost. The underlying mechanism of coexistence can resemble the hawk-dove game, the dominance-discovery trade-off (akin to the competition-colonization trade-off), or a novel trade-off we call the "dove-discovery trade-off," depending on parameter values. Competitive exclusion via the * rule occurs only when differences in exploitative abilities swamp other differences between species, and it occurs more easily when differences in * reflect different search speeds than when they reflect different handling times. Our model provides a mathematically tractable framework that integrates exploitative and interference competition and synthesizes previous disparate models.

AbstractEcologists differ in the degree to which they consider the linear type I functional response to be an unrealistic versus sufficient representation of predator feeding rates. Empiricists tend to consider it unsuitably nonmechanistic, and theoreticians tend to consider it necessarily simple. Holling's original rectilinear type I response is dismissed by satisfying neither desire, with most compromising on the smoothly saturating type II response for which searching and handling are assumed to be mutually exclusive activities. We derive a "multiple-prey-at-a-time" response and a generalization that includes the type III to reflect predators that can continue to search when handling an arbitrary number of already-captured prey. The multiprey model clarifies the empirical relevance of the linear and rectilinear models and the conditions under which linearity can be a mechanistically reasoned description of predator feeding rates, even when handling times are long. We find evidence for the presence of linearity in 35% of 2,591 compiled empirical datasets and support for the hypothesis that larger predator-prey body mass ratios permit predators to search while handling greater numbers of prey. Incorporating the multiprey response into the Rosenzweig-MacArthur population dynamic model reveals that a nonexclusivity of searching and handling can lead to coexistence states and dynamics that are not anticipated by theory built on the linear type I, type II, and type III models. In particular, it can lead to bistable fixed point and limit cycle dynamics with long-term crawl-by transients between them under conditions where abundance ratios reflect top-heavy food webs and the functional response is linear despite having an inherent upper limit. We conclude that functional response linearity should not be considered empirically unrealistic but also that more cautious inferences should be drawn in theory presuming the linear type I to be appropriate.

AbstractWarming induces metabolic changes in microbial organisms, including increased respiration. Empirical studies have shown that evolution can compensate for thermal sensitivity and reduce respiration rate at high temperatures. Evolutionary adaptation may mitigate the effects of warming, but it remains unclear to what extent organisms can overcome thermodynamic constraints through evolution. Furthermore, evolutionary adaptations are modulated by interactions with plastic changes to respiration and other metabolic traits. We develop a mechanistic model including both evolution and metabolic plasticity to explore how adaptation to temperature affects variability in metabolic traits in mixotrophic marine microorganisms under thermal stress. By combining modeling with empirical data, we show that variability in metabolic activity between mixotrophs with different temperature histories can be explained by changes to the carbon budget facilitated by evolved reductions in respiration. The model suggests that evolution enhances thermal resilience over evolutionary timescales. Evolving mixotrophs exhibit less metabolic variability in response to temperature changes. In contrast, over shorter timescales plastic responses dominate over evolutionary adaptations, producing transient changes to metabolic activity following a temperature change. These results highlight the interplay between different biological adaptive mechanisms and provide a modeling framework for representing variability in microbial metabolism in the context of climate change.

AbstractThe evolution of sexual dimorphism is predicted to resolve conflict that can arise from divergent evolutionary interests between sexes, enabling each sex to reach its fitness optimum. However, most of the genome is shared between sexes, which can lead to a genetic constraint for dimorphism evolution. Most studies of intersexual genetic constraints have focused on the effect of genetic correlations, , for single traits. However, multivariate studies of the matrix of intersexual genetic covariances suggest that sexual dimorphism may be more evolvable than inferred from because of the potential for indirect responses to selection from correlated traits. To comprehensively address this question, we collected and reanalyzed published estimates of using a recently developed approach to quantify the evolvability of sexual monomorphism and dimorphism. We find that across the traits and species we study, the evolvability of dimorphism is lower than that of monomorphism, but also that sexually concordant and antagonistic selection are almost equally capable of producing dimorphism. We also find that asymmetry in would affect the response to selection more in females than in males. Our results show that sexual dimorphism is more evolvable than studies of suggest and underscore that sexually antagonistic selection is not required for the evolution of sexual dimorphism.

AbstractUnderstanding and identifying factors influencing the likelihood of sudden transitions in ecological systems is a significant area of scientific research. Environmental fluctuations are particularly important, as they can trigger these transitions before reaching the system's condition to a deterministic tipping point. While there has been much focus on noise-induced tipping due to uncorrelated environmental noise, the impact of correlated noise on multispecies systems has been relatively overlooked. Specifically, studies have neglected the impact of correlations between species responses to environmental changes and a system's susceptibility to tipping. This study examines various two-species ecological models representing different interaction types in noisy environments. We reaffirm that elevated positive temporal autocorrelations in environmental fluctuations aggravate the chance of tipping. Conversely, our key findings suggest that elevated positive correlations in species responses generally delay the onset of tipping, except when the system dynamics is solely driven by positive interspecific interactions. The correlation of species responses is also critical in determining the reliability of early warning signals for predicting sudden ecological changes. Our findings highlight the importance of considering the similarity between species' responses to environmental variability, which significantly influences the likelihood and detectability of dramatic ecological transitions.

AbstractElevational distributions have long fascinated scientists, an interest that has burgeoned with studies of predicted upslope range shifts under climate change. However, this body of work has yielded conflicting results, perhaps due to varied conceptual and statistical approaches. Here I explore how ecological processes and researcher decisions shape the patterns characterized by elevational ranges. I use community science data to illustrate (1) that elevational ranges include variation in abundance; (2) that elevational ranges are usually estimated, not observed directly; (3) that elevational ranges are dynamic across short distances and time intervals; and (4) that how we describe elevational ranges has consequences for inference of range shifts. I present a conceptual framework for understanding elevational ranges across multiple spatial scales and propose that elevational distributions are governed by scale-dependent processes. This framework implies that accurately quantifying elevational ranges and learning how they are formed or maintained requires matching questions to their appropriate scale domain. I provide a list of best practices for studying elevational ranges and highlight promising directions for future research into these complex phenomena.

AbstractWarming climate has led to significant phenological advances in many plant and animal populations. Whether these advances represent evolutionary responses or phenotypic plasticity remain typically unknown. Using a 53-year-long time series of individually marked Great Tits () and Willow Tits (), we investigated whether the significant breeding time advances in these species could be explained as resulting from evolutionary responses, phenotypic plasticity, or both. In the case of both species, we did not find any evidence for changes in breeding values for timing of breeding, suggesting that the observed changes do not have a genetic and, hence, evolutionary basis. In contrast, we found that annually fluctuating environmental effects explained most of the variation in first egg-laying dates, suggesting that advances in breeding time were attributable to phenotypic plasticity. We further inferred that phenotypic plasticity in response to spring temperatures can fully explain the observed advancement of Great Tit phenology over time, whereas Willow Tits have advanced their phenology much beyond what would be expected from phenotypic plasticity in response to spring temperatures. The latter observation suggests that some other yet unidentified environmental factor, uncorrelated with spring temperatures, likely explains about half of the advancement in their breeding time.

AbstractMetapopulations span environmental gradients and experience variable rates of environmental change, with populations differing in their tolerance and evolutionary capacity. Our study aimed to quantify the extent to which interactions between population-specific traits and spatial environmental heterogeneity affect metapopulation persistence under climate change. Using an eco-evolutionary model, we simulated 25 population types with varying thermal tolerance breadths and genetic variance, impacting the strength of selection and rate of evolutionary response, respectively. We applied this framework to marine ecosystems, which face significant threats from climate change, with many habitat-forming organisms such as coral, oysters, and kelp existing as metapopulations connected through propagule dispersal via ocean currents. We tracked the response of different populations under sea surface temperature spatial ranges and projected warming rates to 2100 that are specific to 49 large marine ecosystems. We found that the rate of warming was the strongest predictor of the number of persistent metapopulations, where faster warming reduced the population types that a region could support. We also found that cooler subpopulations outperformed warmer ones, likely due to immigration from warmer sites, suggesting that cooler sites may act as climate refugia.

AbstractSeveral metrics have been proposed to measure phenotypic parallel evolution. All of these metrics stem from a geometric definition of parallel evolution in which two evolutionary trajectories are, literally, parallel or nonparallel to each other. Two metrics fit this definition: the interaction term between population and habitat in a two-factor ANOVA and a measure of the angle between two multivariate trajectories of evolution. A third metric is derived from the general direction of multivariate trajectories; although this might fit our intuition about parallel evolution, it does not fit the geometric definition. A fourth metric is based on the amount of variation explained by the habitat variable in a one-factor ANOVA (i.e., the ). We show here that the metric does not reliably measure any aspect of parallelism and should be avoided. We also discuss the importance of establishing proper ancestor-descendent relationships in attempting to use any of the valid metrics to quantify parallel evolution. Finally, because different metrics measure different aspects of evolutionary trajectories, we recommend being explicit about what one is trying to measure (angle, direction, or length of trajectories).

AbstractThermal preference (Tp) prevents ectotherms from encountering sublethal temperatures. Its plasticity likely modulates the importance of behavioral thermoregulation under changing conditions. While it has been widely recognized that Tp varies across ontogeny, the plasticity level of this trait across life stages is poorly understood. We propose a novel conceptual framework relating two plastic components of Tp: its mean, which indicates temperature affinity, and its variance, which informs on the precision of behavioral thermoregulation. We tested this framework at the population scale by measuring Tp variations across life stages of an insect model after several generations under contrasting developmental temperatures. Tp plastic responses differed among life stages. Generally, we obtained a bell-shaped relationship between temperature affinity and precision of thermoregulation, indicating a strategy to avoid suboptimal and supraoptimal temperatures in , but not in all life stages. We highlight the need to change the paradigm underlying the study of Tp plasticity beyond the use of a single metric (median or range) to better comprehend thermoregulatory strategies.

AbstractEvolution requires both robustness of adaptive states and transitions between them. Understanding the mechanisms that reconcile these seemingly opposing properties is limited by the transient nature of evolutionary processes, where past pathways and contexts are often lost. Here, we overcome this limitation by tracing the biochemical evolution of avian carotenoid networks on the global carotenoid biochemical network, which is unmodified in avian evolution. By mapping enzymatic interactomes of 260 extant bird species and their reconstructed ancestral states onto this global network, we reveal that stepping stones between them are evolutionarily stable degenerate carotenoids-compounds that can be synthesized interchangeably by different dietary carotenoid-specific pathways. We find that ecological specialization across taxonomic groups is consistently associated with an uneven biochemical reach of individual dietary carotenoids, leading to increased fragmentation and reduced resilience of enzymatic networks to failure. However, the robustness of enzymatic networks of specialized groups is restored by the accumulation of degenerate carotenoids. This accumulation enables direct transitions between ecological specializations and sustains evolutionary explorations. Thus, the same feature of network structure-its degeneracy-increases the robustness of specialized enzymatic networks as enables evolutionary transitions between them. These findings provide an insight into the mechanistic basis for the interplay between natural selection and historical contingency, highlighting their fundamental interdependence.

AbstractMost species distributions are dynamic, and as species distributions change they often encounter novel environments and resident species. To establish new populations, ecologically similar species compete with residents for resources while adapting to the environment. Yet local adaptation in residents can allow them to outcompete maladapted invaders and prevent their establishment. Indeed, local adaptation often improves male condition but also intensifies sexual conflict, a process where males increase their fitness while decreasing female fitness. Using an eco-evolutionary model, we show that sexual conflict can prevent adapted residents from monopolizing resources. This cost of adaptation in the residents opens a window of opportunity for the establishment of maladapted invaders. Female resistance to male harm can, however, prevent the invader from establishing. Sexual conflict can therefore reduce differences in competitive ability, facilitating establishment, but does not affect niche differences. However, when sexual conflict is density dependent, it can facilitate resident and invader coexistence, even when interspecific competition is stronger than intraspecific competition. Our results show that reproductive interactions may critically shape the dynamics of species invasions and species coexistence.

AbstractFamily groups, ranging from simple to complexly structured, are widespread in the animal kingdom, with parent-offspring interactions in the form of parental care traditionally considered the primary driver of family life. However, recent considerations suggest that sibling cooperation might have facilitated the early evolution of social and family life. While the effects of isolated family interactions have been extensively studied, the intricate dynamics between different family interactions and their reciprocal impacts have gained little attention. Using a full-factorial social isolation experiment in the subsocial burying beetle , where we isolated offspring from siblings and/or parents, we showed that offspring benefited from the presence of both parents as well as siblings. The positive effects of siblings were evident in the absence and presence of parents, although they manifested differently. Without parents, growing alongside siblings resulted in higher larval mass at dispersal, perhaps due to advantages of collective feeding. With parents, having siblings accelerated early growth and increased survival, possibly due to higher begging activity, which may have influenced parental investment. Our results support the notion that beneficial sibling interactions are an important part of facultative family systems and may encourage offspring to stay in a family group.

AbstractMultitrait analyses can be used to measure the differential performance of phenotypic traits in species complexes. Hybridization within these complexes can result in a mismatch between mitochondrial and nuclear DNA that may lead to reduced performance and acclimation capacity in hybrids. To test the effect of this mismatch on physiology, we compared physiological performance and acclimation capacity of metabolic rate () and total resistance to water loss () between two sexual species and a closely related unisexual lineage. We also separated unisexuals by their unique biotypes to determine how physiology varies with subgenomic composition. We found that unisexual biotypes exhibited phenotypes more like their related sexual species than other unisexuals. We also found a trade-off between and , with increasing resulting in a decrease in . Although we did not find evidence for mitonuclear mismatch, our results indicate that the genomic composition of hybrids may be a suitable predictor of hybrid trait performance. Multitrait analyses are imperative for understanding variation in phenotypic diversity, providing insight into how this diversity affects species responses to environmental change.

AbstractSynthetic gene drives are being investigated as tools to suppress pest populations, and it is important to understand how natural selection will act on variant drivers that may either arise by de novo mutation or be intentionally released. In this study, we extend previous spatially implicit stochastic models to examine the evolutionary dynamics of synthetic driving Y chromosomes in patchy environments when population size is responding dynamically to the spread of the driver and derive conditions for the existence of an evolutionarily stable strategy (ESS) for drive strength. Under broad conditions, an intermediate drive strength emerges as the ESS, capable of outcompeting both stronger and weaker variants. Additionally, we show how the intentional release of two drivers straddling the ESS can help stabilize population dynamics. Finally, inbreeding depression has the effect of expanding the range of conditions under which no intermediate ESS exists, with ever stronger drive being selected until the population is eliminated. These results provide insights into the expected evolutionary trajectories of gene drive systems, with important implications for the design and release of gene drives for pest and vector control.