AbstractLife has evolved different strategies to take advantage of seasonal changes in the environment that are emblematic of boreal and arctic biomes. However, ecological theories often ignore seasonal changes for tractability or simplicity. Understanding the effect of seasonality may prove crucial as the changing climate puts more pressure on ecosystems. Hybrid dynamical models are an efficient way to represent seasonal adaptations where switches in food web compositions account for species migrations and predator movements. We use the highly seasonal and cyclic dynamics of an Arctic food web to showcase the utility of hybrid models. The simplified representation of community dynamics provided by the hybrid framework eases the study of conditions leading to lemming cycles and facilitates parameterization with empirical data. We corroborate that seasonal switches, accounting for the onset of reproduction of resident predators and the migration of mobile predators, likely drive cyclic fluctuations in lemming abundance. Our empirical investigation reveals that each predator alone does not reduce lemming growth rate enough to generate population cycles, which reinforces the idea that the predator community as a whole is responsible for the cyclic dynamics. This situation arises because each predator has unique adaptations to seasonality and impacts the dynamics in different but complementary ways. Our results have implications for community ecology, as they show how hybrid models can help understand complex dynamics in highly seasonal ecosystems. This is especially relevant in the Arctic, considering that rapid warming has the potential to disrupt lemming population cycles and negatively affect their predators.
AbstractReproductive division of labor (DOL) is key to the ecological success of eusocial insects such as ants, termites, and honeybees, in which queens reproduce while workers perform nonreproductive tasks. DOL is often associated with a shift in the fecundity-longevity trade-off, with queens outliving nonreproductive workers. In most species, reproductive and nonreproductive individuals differ significantly (e.g., in ontogeny or morphology), which may contribute to this phenomenon. In contrast, in the ant Platythyrea punctata, females are clonally identical, and socially dominant workers produce female offspring from unfertilized eggs by thelytokous parthenogenesis. We investigated whether all workers-that is, dominants and subordinates-reproduce when given the opportunity. We formed dyads of workers of the same age and allowed them to establish rank orders. We then investigated their reproductive performance in isolation. We found that nearly 88% of workers regardless of social rank activated their ovaries in isolation. However, of the 12% that never laid eggs, a higher proportion were previously classified as subordinates than as dominants. This suggests that reproductive ability may differ among workers. Isolated subordinates that were reproductively active matched isolated dominants in their egg-laying rate, with no apparent trade-off between fecundity and longevity. Reproductive costs, likely related to the use of physiological or energetic resources, were evident for both workers in isolation, as egg-laying rates declined over time in the absence of supportive workers. These results highlight the complex interplay between reproduction, longevity, and social status in eusocial insects and provide insights into how eusociality has shaped aging and life history evolution.
AbstractNest material kleptoparasitism, the theft of nesting materials by birds from other nests, is likely more widespread in passerines than currently documented. Yet no studies examine the hypotheses underlying when nest material theft will likely occur. Here we investigate nest material kleptoparasitism during the monitoring of 216 nests of passerines on the island of Hawai'i. Native Hawaiian forest birds were victims of nest material theft at a frequency correlated to their relative nesting abundance in the landscape. We provide the first evidence consistent with the height overlap hypothesis, demonstrating that Hawaiian forest birds stole material from nests in the same strata where they foraged for prey. Because 2 out of 39 (5%) of these events shortly preceded nest failure, we suggest that nest material theft, albeit small and previously overlooked, may be a contributing factor to nest failure. Future research should quantify key factors influencing this behavior, including types and relative abundance of materials stolen, timing, nest height, and impact on nest success.
AbstractAdaptive evolution is a key means for populations to persist under environmental change, yet whether populations across a species' range can adapt quickly enough to keep pace with climate change remains unknown. The breeder's equation predicts the evolutionary change in a trait from one generation to the next as the product of the selection differential and the narrow-sense heritability in that trait. Incorporating these aspects of the breeder's equation, we performed a resurrection study with the scarlet monkeyflower (Mimulus cardinalis) to evaluate whether traits associated with drought adaptation have evolved in populations across a species' range in response to extreme drought. We compared trait and fitness differences of predrought ancestors and postdrought descendants from six populations transplanted into three latitudinally arrayed common gardens and quantified phenotypic selection and trait heritabilities. The strength, direction, and mode of selection varied among traits and gardens. Trait heritabilities were relatively low and did not differ dramatically among populations or gardens. Overall, instances of evolutionary responses between ancestors and descendants were few and small in magnitude, but the magnitude of these evolutionary differences varied among gardens. These results suggest that evolutionary responses to climate change vary among populations in unpredictable ways and that the expression of these responses depend on environmental conditions, hindering our ability to predict evolutionary rescue under changing climate.
AbstractThe extent of contemporary evolution, which is mediated by interactions with plasticity, will be an important determinant of biological responses to climate change. We synthesize two functional resurvey projects that, coupled with mechanistic models, evaluate the interplay of plasticity and evolution of pierid butterfly larval (thermal sensitivity of feeding) and adult (wing melanization) traits over recent decades. We characterize thermal environments over the resurvey periods, which we interface with developmental and (historical, current, and hypothetical) thermal sensitivity traits to examine the implications of evolutionary changes. We find that the evolution of photoperiod-cued plasticity of wing melanization in California Colias is consistent with avoiding thermal stress during warming springs. Plasticity has not evolved for Colorado Colias populations, which have experienced stronger increases in climate means relative to extremes in recent decades. Evolution in Colorado Colias larvae has improved tolerance to warm extremes, whereas evolution in California Colias larvae has broadened thermal sensitivity, consistent with capitalizing on expanded seasonal thermal opportunity. Our models predict that Washington Pieris larvae have experienced shifts in the direction of selection to increase performance at warm temperatures. The research highlights the importance of evaluating changes in climate change exposure and sensitivity to understand interacting organismal responses.
AbstractAbrupt ecosystem shifts during the Late Quaternary coincided with major climatic changes and intensified human activities, but the precise causes of these shifts remain debated. Here, building on previous hypotheses and work, we propose a new hypothesis that both plant beneficial and antagonistic soil microorganisms were the proximate drivers of Late Quaternary change. We synthesized evidence from paleoecological studies and contemporary ecosystems to understand how microbes and their interactions with plants shift ecosystem function. Because relevant paleoecological data are nonexistent, we reanalyzed a contemporary survey from grasslands and woodlands across Europe to test the general role of microbial diversity versus climate in controlling ecosystem function. Our models found that the richness of different microbial groups, including Proteobacteria, mycorrhizas, and plant fungal pathogens, were more strongly associated with the magnitude of direct effects on net primary productivity than temperature and precipitation. The richness of most of these groups was also influenced by climate, supporting our hypothesis that climate change may have indirectly caused past ecosystem shifts by changing microbial composition and function. We end by highlighting the potential of environmental DNA to reconstruct the biota and conditions of past ecosystems. Ultimately, improving our understanding of how microbes drove past ecosystem shifts may improve our ability to respond to future environmental changes.
AbstractFisher's fundamental theorem states that the rate of change in mean fitness due to natural selection equals the additive genetic variance in fitness, suggesting that selection generally drives populations toward higher average fitness. Yet in real populations, this increase can be altered or reversed by mutation, frequency-dependent selection, or environmental fluctuations, underscoring the need for complementary measures of adaptation. We analyze stochastic game dynamics of phenotypic frequency in large finite populations under weak frequency-dependent selection and genetic drift. Using the Fokker-Planck equation for the probability density of phenotypic frequency and a path integral formulation, we characterize the feature of possible evolutionary paths over finite timescales. Within this framework, we define the "evolutionary path characteristic" as the likelihood ratio between the probability densities of paths reaching a given endpoint under selection plus drift versus under neutrality. This ratio is time invariant and captures the cumulative effect of directional selection relative to drift. Importantly, its expected value, which equals 1 plus the χ2 divergence between evolutionary paths under selection and drift versus those under drift alone, is nondecreasing. In the presence of fitness variance, the effect of directional selection on phenotypic frequency accumulates over time, resulting in a divergence from paths shaped solely by drift. This framework complements Fisher's theorem by providing a robust measure of accumulating adaptation in stochastic evolutionary dynamics.
AbstractA prevailing problem in evolutionary biology is elucidating the genotype-to-phenotype map that characterizes how genomic activities regulate different aspects of organismal morphology and their variability in both space and time. Here, we explore potential causality between genome content and both morphological complexity and disparity by compiling the regulatory components (i.e., transcription factors, RNA-binding proteins, and microRNA families) as well as a representative set of nonregulatory housekeeping genes in 32 species belonging to a wide variety of animal phyla spanning a range of morphological, ecological, and genomic characteristics. A principal component analysis of these four nonoverlapping genomic components from each of these 32 species in relation to their last common ancestor revealed that no relationship exists between genome space and disparity, as changes to animal body plans appear to be largely the result of changes to the regulatory networks that govern animal development rather than gaining or losing specific sets of regulatory genes. However, using both phylogenetically correlated and phylogenetically uncorrelated statistical tests, we find a strong relationship between the loss of all considered gene types in some parasitic taxa, an exacerbation of a trend that characterizes animal genomes in general. We also find a strong correlation, and a likely causal relationship, between microRNA innovations and organismal complexity. While this analysis of genomic features suggests how complexity and disparity are each encoded in the genome, further analysis of the regulatory networks in which they participate should provide a more comprehensive description of how organisms diversify their morphologies through time.
AbstractEvaluating the evolutionary impacts of anthropogenic activity on populations is key to understanding species resiliency and to designing effective conservation strategies. Sequencing DNA from historical specimens provides the opportunity to establish a historical baseline and empirically assess changes in genetic diversity, changes in effective population size, and selection over time. Here, we sequenced historical and contemporary samples of the cardinalfish Taeniamia zosterophora collected in 1908 and in 2021-2022 across two sites with differing human impact in the Philippines. At both sites, genetic diversity increased over time, with contemporary samples having significantly higher Watterson's θ than historical samples. This diversity increase was primarily attributable to positive selection on low-frequency alleles such that they increased toward intermediate frequencies through time. For the putatively neutral fraction of the genome, in contrast, there was a slight but significant decline in Watterson's θ at both low and high human impact sites, suggesting that drift strengthened and effective population sizes declined through time. There was more evidence for selection and greater loss of neutral diversity at the site with higher human impact. Our results provide empirical evidence for the surprising preservation of genetic diversity through the action of natural selection in the face of anthropogenic impacts.
AbstractAfter a fitful start, the conceptual study of mutualism (mutually beneficial interspecific interactions) is now flourishing. In 1994, I reviewed the status of the field as reflected in the peer-reviewed literature; I also laid out directions for future research. Here, I look back on that assessment and offer an updated perspective on our understanding of mutualism. Most of the open questions I identified now have significant literatures of their own. New questions have sprung from each of these, and methodological innovations have made it more possible than ever before to obtain answers. I identify one astonishing gap from 1994: the absence of attention, either in journals or in my own synthesis, to the fate of mutualisms in a changing world. I offer a brief assessment of the now-massive literature on this topic. Finally, I suggest some directions in which the field as a whole might profitably move in the future.
AbstractNavigation to and from a familiar site is a common animal behavior called homing. Many species use olfactory environmental landmarks or scents deposited in the environment by themselves or their conspecifics for homing. Birds regularly commute to and from their nest, and olfaction, an underappreciated sense in birds, may facilitate this behavior. Burrow-nesting seabirds, for example, rely on olfaction to locate their breeding colony and to identify their burrow, but the specific chemical information they use is unclear. We examined the chemical profiles of the colony landscape and its avian occupants at a breeding island of Leach's storm petrels (Hydrobates leucorhous) to determine whether place-specific chemicals, bird-produced chemicals, or both enable homeward navigation in this burrow-nesting species. We found that the colony contains spatial gradients of chemicals that may facilitate multiple stages of homing. We also show that burrows possess unique odors owing to chemicals deposited by their occupants. Moreover, the burrow shapes the odor of the birds such that individuals carry the scent of their nest and mated pairs possess similar chemical profiles. The bidirectional transfer of compounds between burrows and birds may enable burrow recognition in this species and potentially functions as a means of communication between conspecifics.
AbstractThe last 30 years have seen major advances in our understanding of the evolution of cooperation-traits that have evolved because of the benefit they provide other individuals. In contrast, we have been much less successful in determining the consequences of cooperation for long-term ecological and evolutionary change. Studies of birds, insects, and bacteria suggest that cooperation has major consequences for fundamental features of life, such as ecological niche range, genetic variation within species, and rates of species diversification. However, the role of cooperation in driving these changes is largely limited to hypotheses, as we lack both data and a general theoretical framework. We synthesize the progress that has been made and highlight the major gaps in our understanding for future study.
AbstractSexual selection theory focuses on variation in mating success caused by a shortage of mates relative to same-sex competitors, but variation in mating success can also arise if mates are limited in an absolute sense (e.g., due to low encounter rates). To assess the potential for absolute mate limitation to contribute to sexual trait evolution, we develop a quantitative genetic model of a costly trait that increases mate encounter rates but is expressed solely in the operationally limiting sex. We show that sexual selection favors the elaboration of such a trait provided the marginal increase in offspring production exceeds the marginal increase in mortality. The conditions in which this occurs depends on population dynamic variables that change as the trait evolves. The resulting eco-evolutionary dynamics generally cause the sexual trait to converge on a single eco-evolutionary equilibrium value that, once established, cannot be replaced. These findings suggest a broader set of ecological contexts in which sexual selection can in principle occur and highlight promising directions for future research on the eco-evolutionary dynamics of sexual selection, sexual coevolution, and causes of variation in mating success in the limiting sex.
AbstractMilk is not cheap. The energetic cost for mammalian mothers to provide and sustain milk production makes it a finite resource. Offspring are therefore expected to wean before sexual maturity and reproductive activity, whether on their own or through termination by their mothers. Weaning delays should result in a reproductive trade-off for the mother: the possibility of begetting a fitter pup at the cost of a longer interbirth interval. Using 20 years of data, we show the occurrence of repeated suckling events between female Galápagos sea lions (GSLs; Zalophus wollebaeki) and their adult (≥5 years) biological offspring well beyond the average age of independence and when the offspring are themselves already reproductively active. This behavior, "supersuckling," suggests that GSL mother-offspring relationships are more complex and longer lasting than previously thought. To our knowledge, this is the first long-term documentation of known mother-offspring pairs repeatedly performing this behavior in any marine mammal species.
AbstractAccording to optimal foraging theory, mesopredators should forage in areas where their prey is abundant while avoiding high predation risk. Here, we investigate how environmental factors influence mesopredators' abilities to minimize spatiotemporal overlap with predators while increasing spatiotemporal overlap with prey. We paired 30 western diamond-backed rattlesnake (Crotalus atrox) 3D printed replicas with game cameras in West Texas for 2 years to quantify several spatiotemporal factors affecting prey availability and predation risk. Concurrently, 25 C. atrox were radiotracked at the same site to gather activity and microhabitat selection data regarding free-ranging individuals. Random forest algorithms were trained using data obtained from the game camera and applied to predict the probability of predation and the probability of prey encounter for each radiotracking event. Time of day, month, vegetation structure, and concealment percentage all had a significant association with the probability of predation and the probability of prey encounter. Our results suggest that rattlesnakes choose to be active when and where the probability of prey encounter was significantly higher than the probability of predator encounter, thus following optimal foraging theory. Our results demonstrate that mesopredators increase chances of prey capture while reducing predator detection in natural settings.
AbstractBird species with high demand for efficient flight (e.g., migrants) tend to have more pointed wing tips than sedentary birds, and indices describing wing tip pointedness, such as the hand-wing index (HWI), are often used as proxies for dispersal propensity in comparative studies. Wing pointedness also varies among closely related populations of the same species that experience different selection pressures on flight, but we know surprisingly little about how variation in bone versus feather lengths contributes to wing pointedness. Here, we compare wing tip shape (HWI) of migratory versus sedentary populations of a widespread songbird, the Yellow Warbler (Setophaga petechia), to deconstruct variation in the individual skeletal and feather components of the hand-wing. Our results reveal that the relatively pointed wing shape of migrants is a consequence of shorter secondary feathers (i.e., a narrower wing) compared with nonmigrants, rather than longer wings. Indeed, despite having more pointed wings, migratory populations have similar wing length (i.e., wing chord) as sedentary continental populations. These populations show similar trunk size, but migrants have significantly shorter limb bones. Our results reveal the morphological underpinnings of a wing shape metric that has been widely used in macroevolutionary and macroecological studies of avian dispersal.
AbstractGenomic offset metrics are increasingly used to predict population maladaptation under changing climates, based on the assumption of a negative statistical relationship between offset measures and local relative fitness. Recent theoretical advances have confirmed this relationship by relating genomic offset to phenotypic trait distances along selection gradients. However, these metrics typically rely on the assumption that stabilizing selection, which maintains local adaptive optima, operates on fitness-related traits through Gaussian-shaped selection gradients. In this study, we extend the theory to accommodate more diverse forms of selection gradients and introduce more general genomic offset measures that preserve the fitness-offset relationship. We validate this generalization through simulations and demonstrate the utility of these new measures in predicting relative fitness in common garden experiments involving three plant species: pearl millet, a vital staple cereal grown in arid soils, and two emblematic North American tree species, balsam poplar and red spruce. Our findings indicate that assuming a local Gaussian-shaped selection gradient for climate adaptation is a robust approximation for these species. These results have important implications for validating genomic offset predictions using fitness proxies and for studies that aim to predict fitness loss based on genomic offset metrics.
AbstractSexual size dimorphism (varying body sizes between males and females) and the operational sex ratio (ratio of sexually active males to receptive females) are key demographic traits influenced by complex selective pressures. Two hypotheses explain their relationship: the mating competition hypothesis posits that male-biased sexual size dimorphism intensifies with increasingly male-skewed adult sex ratios, while the mating opportunity hypothesis proposes that female-biased sexual size dimorphism escalates with greater male-biased adult sex ratios. We tested these hypotheses across 101 Chinese anuran species. Our results support the mating opportunity hypothesis, with enhanced female-biased sexual size dimorphism at more male-skewed operational sex ratios, particularly in monogamous species. We further explored the role of ecological factors and life history traits in shaping sexual size dimorphism and operational sex ratio. We found predation pressure to covary negatively with the male bias in operational sex ratios, while temperature variation, likely reflecting seasonal differences, negatively influenced both sexual size dimorphism and operational sex ratio. Our findings highlight the interplay between sexual selection, ecology, and life history in driving the evolution of sexual size dimorphism and operational sex ratio in anurans. Understanding these mechanisms is crucial for predicting how species may respond to future environmental changes.
AbstractDeciding which offspring to feed is one of the most critical decisions parents make for both parental and offspring fitness. Despite knowing much about what choices parents make, we know little about how parents choose. What we do know about how the brain integrates sensory evidence when choosing between options comes from laboratory studies and models. However, such studies may not adequately reflect decisions made in nature-with real-world complexity and consequences. Our naturalistic experiment on decision-making in 62 wild Parus major parents addresses this issue. Decision speed was impacted by whether parents chose to feed a typically preferred chick, offspring starvation risk, decision complexity, and parental sex. Parents regularly moved food between chicks before committing, suggesting that parents perhaps were not confident in their initial decision, had made a mistake, were continuing to collect evidence, or could not execute their initial decision. Such decision changes were predicted by similar factors as speed. After moving food, parents were more likely to continue gathering evidence after their decision, and their next decision was slower. These results demonstrate several factors impacting cognition, and perhaps metacognition, in wild birds. More broadly, our study demonstrates how crucial evolutionarily relevant experiments in natural settings are.
AbstractUnderstanding how thermal tolerance determines species distributions is key to predicting species persistence in changing climates. However, thermal tolerance evolution is likely associated with multiple interacting abiotic and biotic factors, which are rarely explored in combination. Using an integrative framework, we examine how thermal tolerance breadth (TTB) relates to environmental variability, life history traits, and geography in a diverse lizard radiation (family: Phrynosomatidae). We test whether TTB evolution is primarily associated with shifts in cold tolerance (CTmin) or heat tolerance (CTmax) and assess its relationship with temperature variability, vegetation cover, range size, elevational range, reproduction mode, thermal preference, and body size. We found that, contrary to expectations, CTmax exhibits more macroevolutionary shifts than CTmin. Moreover, TTB shows no association with intrinsic traits such as body size and parity mode, suggesting that the evolution of TTB is primarily relevant in the context of environmental pressures rather than intrinsic biological constraints. Finally, causal models revealed that species with broader TTB tend to occupy more thermally heterogeneous regions, which in turn facilitates range expansion. A broader TTB may facilitate species persistence under changing climates, and incorporating physiological traits into conservation assessments could help identify species most vulnerable to climate change, particularly when thermal limits are evaluated in relation to environmental temperatures.