Evolutionary Ecology

Animal colouration evolves under multiple, often conflicting, selective pressures. Conspicuous, non-aposematic colour-patterns that enhance conspecific communication may simultaneously increase detectability by predators. Such trade-offs can be resolved by optimising colour-patterns to match the perceptual abilities of different receivers. We tested whether dorsal colour-patterns of the Lusitanian wall lizard (Podarcis lusitanicus) are optimised for ecologically relevant receivers across relevant viewing distances, while accounting for the visual acuity of conspecifics and predators. Conspecifics and snakes detected chromatic information at shorter distances, whereas achromatic and luminance information were detected at longer distances. Birds showed a uniform decline in detectability across the colour-pattern components with increasing viewing distance. Larger males retained high chromatic detectability across all receivers despite the general distance-related decline, whereas females and smaller individuals exhibited less salient colour patterns, consistent with predator avoidance strategy. Our results show that lizards resolve the trade-off between conspecific communication and predator detection through distance-dependent colour-pattern perceptibility across receivers. This resolution breaks down in large males, for whom the benefits of salient chromatic patterns for intraspecific communication may outweigh increased detectability to predators.

The evolutionary patterns of trait diversification provide insights into the function of the trait. Early burst of trait evolution is often associated with adaptive radiation, rapidly diversifying the trait in response to vacant niches followed by the slowdown of the diversification with niche filling, whereas late burst is more likely to be associated with sexual selection, possibly contributing to reproductive barriers between closely related species. Here, we studied the diversification of tail fork depth through time in hirundines to infer its function, which remains unclear due to the competing two alternative hypotheses: the sexual selection hypothesis, which is a classic explanation of deeply forked tails, proposed that this trait has evolved via sexual selection, which was then challenged by the viability selection hypothesis, which proposed that deeply forked tails have mainly evolved via viability selection for enhancing aerodynamic performance during aerial foraging on large prey. We found a late burst of tail fork depth, but not of bill length, i.e., an index of prey size. The observed pattern is consistent with the sexual selection hypothesis but not with the viability selection hypothesis.

Animal personality is the expression of consistent among-individual variation in a behavioural trait across time and context. The application of this theory to behavioural research provides a valuable framework to investigate the among- and within-individual variation in behaviour. The animal personality theory is particularly relevant to understand and diagnostic fish welfare. It can be integrated within the nature-based welfare framework, which emphasizes the expression of species-specific behaviours and the maintenance of consistent behavioural patterns over time. Because behavioural trait such as boldness may be closely linked to other functional phenotypes, such associations reflect the broader concept of animal personality, whereby a behavioural trait can covary with another phenotypic trait to support an adaptive responses to environmental conditions. Although these relationships are both species and context dependent, they are consistently shaped by environmental conditions and environmental complexity tend to promote species specific behaviours and reduce maladaptive traits. Here we examined how structural environmental complexity shapes personality in Arctic charr and their covarying functional phenotypes, specifically growth rate and brain size. We propose that environmental complexity promotes alternative behavioural and functional phenotypes through multivariate phenotypic plasticity. We found that environmental complexity did not influence mean boldness between both treatments, but repeatability of boldness in the complex environment was remarkably consistent over a longer-term period, while estimates collapse after seven days in the plain treatment. Our findings are a clear evidence that environmental complexity foster stable behavioural trait expression and that a plain environment may suppress personality. Our results provide compelling evidence that behavioural structure and dynamics are embedded within patterns of behavioural variance. Although we found no support for behavioural covariation or associations with growth rate and brain size, we suggest that the animal personality framework may offer a valuable approach for diagnosing fish welfare issues through the partitioning of behavioural variance.

An animal's musculature must support its specific biomechanical needs, so muscle morphology and volume allocation may adapt when locomotor strategies diversify. We examined muscle size and morphology in two sister families of bombycoid moths, wild silkmoths (Saturniidae) and hawkmoths (Sphingidae), that have diverged in wingbeat frequency, wing morphology, and behavior. Although both families rely on the same muscles to power and steer flight, they may distribute muscle volume differently to prioritize distinct functions. We hypothesized that flight power muscle proportions are larger in hawkmoths and increase with wingbeat frequency, helping meet inertial power demands of high-frequency maneuverable flight. We also hypothesized that some individual muscles diverge in proportional volume and area to support distinct wing control strategies. To test our hypotheses, we took CT scans of twenty bombycoid species and quantified volumes and geometries of six flight muscle pairs. As expected, flight power muscle proportions positively correlate with wingbeat frequency and are generally greater in hawkmoths. Two of three steering muscles diverge substantially in relative volume and area between families. Most muscles exhibit greater length in silkmoths and greater cross-sectional area in hawkmoths. Finally, the dorsal oblique(DO) muscle diverges exceptionally in size and morphology, being highly developed in hawkmoths and smaller or absent in silkmoths. This unexpected difference supports the DO having an underappreciated role in flight control, possibly via shaping indirect strain propagation in the elastic thorax. We show that muscle volume distribution parallels bombycoids' divergent flight strategies, demonstrating how muscle allocation can adapt for specialized functional goals.

Phenotypic differences among populations can arise through heritable genetic divergence, phenotypic plasticity, or both, making it difficult to determine whether trait-environment correlations observed in nature reflect adaptive evolution. Within threespine stickleback (Gasterosteus aculeatus) studies, numerous document morphological differences among allopatric-, parapatric-, and even sympatric populations. These phenotypic differences among populations are often correlated with diet and lake habitat (e.g., lake size), suggesting an adaptive value to the population differences. However, many studies of ecomorphological divergence in stickleback use wild-caught stickleback, which may differ due to evolution or plasticity. Although common garden experiments have confirmed that population differences can be heritable, such experiments typically entail small numbers of populations. Consequently, we still do not know to what extent well-known trait-environment correlations in stickleback are a result of evolution. To address this gap, we reared stickleback embryos from 27 lake populations on Vancouver Island, in a laboratory environment. Morphological differences among populations persist in common-garden fish, confirming a large role for divergent evolution. These heritable differences were associated with environmental variation among lakes, implying an adaptive value. However, some well-known trait-environment relationships in stickleback did not persist in common-garden fish and may be primarily plastic.

For organisms with biparental care, successful reproduction hinges on coordination between partners. Seabirds face an extreme coordination challenge because parents must schedule nest attendance on land with long-distance foraging trips at sea. We present a computational model of incubation schedules for a vulnerable seabird, the Leachs Storm-Petrel (Hydrobates leucorhous). Using only simple energetic rules and parameters, the model recapitulates natural incubation rhythms, exposes a tradeoff between parent energy and egg attendance, and predicts severe reproductive failure in harsh environments. Incubation primarily fails through "schedule breakdown" -- a single point in the season when both parents spend too long foraging and the egg dies from cold. The resilience of the developing offspring to neglect is thus a fundamental adaptation to the uncertainties of biparental care. These results raise new alarms about the indirect causes of reproductive failure in sensitive marine species and provide theoretical foundations for the evolutionary ecology of scheduling behaviors.

Population dynamics and their component vital rates may be driven by weather, climate teleconnections between sea and air (e.g. ENSO), or biotic interactions. These drivers operate directly or indirectly and on different temporal scales. We used a Bayesian structural equation model to characterize effects among weather, climate, and incidental intraguild predation (IGP) on the butterfly Euphydryas gillettii's vital rate of pre-diapause survival, using an 18 year dataset. IGP was a major determinant of pre-diapause survival, along with direct and indirect effects of weather and spring climate teleconnections. The direction of climate effects was reversed when mediated through IGP. Our analysis illustrates the need for sequential hypotheses to capture the cascading effects of abiotic factors via biotic interactions. Using sequential hypotheses addresses the debate on weather -- climate teleconnection roles by disentangling their contributions from one another. Finally, vital rates must be decomposed to component rates in order to detect their drivers.

Animals often attempt to resolve the trade-off between foraging and predation by regulating their activity timings and patterns. Driven by individual energetic requirements and the local environment, onset of activity in a species varies across space and time. These differences are particularly enhanced on a latitudinal gradient, influenced by varying lengths of daylight, temperature and seasonality. For a nocturnal mammal like the bat, such patterns translate to shorter activity windows at higher latitudes, both on a nightly and a seasonal basis. This constructs the timing of activity onset as a crucial variable for a successful night of foraging. While roost exit timings and influence of local conditions on bat activity have been extensively studied across species inhabiting a variety of locations around the world, our understanding of bat emergence behaviour on a global scale remains limited. To investigate emergence patterns in bats across a latitudinal gradient, we conducted a meta-analysis spanning 91 species from across 13 Chiropteran families. We evaluated how timing and luminosity (i.e., sun altitude) at exit varied across latitudes and species. Results revealed that bats across the globe tended to emerge under conserved thresholds of brightness, a pattern that was facilitated by a temporal delay in roost exits at higher latitudes. By maintaining emergence within the confines of nautical twilight (sun altitude between 0{degrees} to -12{degrees}), bats across the phylogeny thus seemed to balance the dilemma of predation versus foraging. This pattern was mirrored across the two broad dietary types (frugivores and insectivores) as well as different social structures (maternal v. non-maternal colonies). Furthermore, our models indicated that while local conditions dictate final exit decisions, shared ancestry was potentially influencing the extent of plasticity seen in emergence patterns. Taken together, these results highlight how broad-scale latitudinal gradients of light can influence the foraging strategies in a globally distributed nocturnal mammal.

Rapid evolution allows populations to persist in environments where they would otherwise go extinct. This phenomenon, known as evolutionary rescue, is typically studied in the framework of biological evolution, yet adaptive traits can also arise and spread through cultural evolution. The present study developed a stochastic eco-evolutionary model to compare rescue probabilities through biological and cultural evolution. Transmission bias governed the rescue probability under cultural evolution by setting how readily a rare adaptive trait was copied. Conformity bias suppressed population persistence because a rare trait was the least likely to be copied. Content bias toward the adaptive trait enabled evolutionary rescue when social learning was rapid, but it typically yielded a lower rescue probability than biological evolution. Only anticonformity bias, together with a high social learning rate, exceeded the rescue probability of biological evolution by enabling the adaptive trait to be established more rapidly. These results demonstrate that transmission bias alters the demographic consequences of cultural evolution and highlight the importance of transmission processes in evolutionary rescue theory. Understanding how adaptive behaviours are socially transmitted may also improve predictions of animal population persistence and inform conservation efforts in rapidly changing environments.

Mixed-species groups (MSGs) pose a particular challenge for our understanding of sociality in animals. Though MSGs are widespread social assemblages that form to enhance foraging success and reduce predation risk of participants, the role of traits in mediating grouping has received less attention. In particular, the role of body colour has not been tested quantitatively, despite the fact that visual similarity can reduce individual predation risk. Here, we examine whether plumage colour structures mixed-species bird flocks (MSFs) at a global scale. Using data spanning four continents, we developed a new metric that quantifies colour similarity among flock participants and compared observed flocks to null assemblages constructed from all flocking species at each site. We further examined whether MSF participants represented a colour subset of the available colours in the regional species pool. We found striking evidence that birds in MSFs were more similar in colour than expected by chance across all sites, indicating that plumage colour is a non-random structuring trait that shapes assembly of flocks globally. The strength and prevalence of colour structuring varied across geographies, but not flock size. Within communities, MSF participants differed systematically in colour composition from the regional species pool, occupying a restricted region of colour space dominated by yellow and brown plumage. Thus, plumage colour affects MSFs influencing both overall flock participation as well as species co-occurrence within flocks. Our findings illustrate the importance of visual traits in structuring interspecific social systems, by highlighting that birds of a feather do indeed flock together.

Allee effects are positive relationships between components of individual fitness and the number or density of individuals in a population. Negative density effects are well documented in Drosophila melanogaster across life stages, while Allee effects are rare and largely confined to the larval stages. However, despite the costs of high density, adult flies are found to exhibit attraction to same-sex conspecifics, suggesting some fitness value to the presence of conspecifics. We measured fitness related traits of singly mated-females housed at same-sex densities of 1, 2, or 10 and found clear reductions in lifetime reproductive output at low densities. Additionally, these females concentrated reproductive effort within early adulthood, albeit without improving estimates of fitness. When housed at variable densities, females altered their reproductive output in response to immediate densities, but were unable to improve it unless remating was possible, indicating an interaction between mating and density. Overall, our findings suggest that reproductive plasticity in response to the presence of conspecifics mediates positive effects of density on fitness in female Drosophila melanogaster. Understanding the physiological and ecological bases of such plasticity may help explain the evolution of social tendency in the fly.

Cryptic female choice - female-mediated bias in fertilization after mating - is well established in animals and can also occur in plants when multiple pollens compete on the same pistil. However, whether interactions between pollen and pistil tissues after pollen deposition contribute to this process remains unknown. Here, we experimentally test whether such interactions mediate cryptic female choice in the angiosperm Brassica rapa. We quantified fertilization success of pollen donors competing on the same pistil using paternity analyses, and in parallel, made semi-in vivo assays to measure pollen tubes trajectories emerging from the excised styles and growing toward unfertilized ovules for each donor-recipient pair. We show that pollen tube growth towards ovules predicts higher fertilization success under pollen competition. Thus, we document a previously unobserved mechanism of cryptic female choice based on physical interactions between male and female components of reproduction. In addition, different recipient plants favour different pollen donors, consistent with non-directional female choice. Plants with longer styles bias paternities more strongly towards the most successful pollen donor. Overall, our study demonstrates that interactions between pollen tubes and pistil tissues after pollen germination enable plants to bias paternity toward particular donors.

Sensory systems mediate the interaction between organisms and their environment, but how complex sensory pathways evolve and relate to variation in perception and behavior across ecological contexts, remains poorly understood, especially for terrestrial taxa. Here, we investigate whole-visual-system adaptation in Heliconius erato butterflies. Using continent-wide sampling, we demonstrate that within H. erato, facet count significantly decreased with increasing elevation. Common-garden rearing of low-elevation H. erato populations from Ecuador and their high-elevation sister species, H. himera, showed that eye and brain morphology are heritable, and comparisons to genomic measures of divergence indicates that this variation is due to divergent selection. Parallel comparisons from Colombia involving H. chestertonii (high elevation) and H. erato venus (low elevation) further revealed that eye and brain morphology can evolve as independent, decoupled traits. For both locations, differences in visual acuity correlated with variation in facet count. We also observed parallel evolution of spectral sensitivity, with independent high-elevation populations having fewer red-reflecting lateral filtering pigments. To experimentally link visual system morphology to behavior, we assessed visual acuity in second-generation H. erato cyrbia-H. himera hybrids. Overall, acuity was influenced by facet count, and when analyzed together with brain morphology, by a positive interaction between facet count and optic lobe volume, demonstrating that structural investment in the eye and neural expansion combine to maximize visual perception. This work shows that visual adaptation is a multi-layered process whereby sensory traits can evolve independently under localized ecological pressures, but evolution across the visual pathway contributes to refinements in behavioral performance.

Machine learning models can be used to analyze large bioacoustics datasets and explore variation due to geography or habitat. We find that in the monotypic Lark Sparrow (Chondestes grammacus), both environmental variables and geographic distance influence song variation in this species. Bird song is an important method of communication within avian species. The variation in bird song within a species can be due to a variety of factors, including genetic drift and isolation by distance. However, it remains unclear in species with wide ranges how environmental factors in particular can cause changes to the song. In this study, the song C. grammacus was analyzed via machine learning to determine if it had significant variation based on multiple geographical metrics. We trained a convolutional neural network to segment individual syllables of 91 C. grammacus recordings, then extracted song characteristics. We found that ecoregion and state explain variation in C. grammacus songs. Our results demonstrate the efficacy of using machine learning models to analyze large datasets, as well as the impact that ecogeographic variation has on song variance.

Sexually selected traits often impose fitness costs on their bearers. Yet, the relative costs and benefits of conspicuous traits can vary through space and time, driving variation in selection acting on those traits. For insects, an important but overlooked source of such variation is seasonal shifts in the local abundance of migratory insectivorous birds. Smoky rubyspot damselflies (Hetaerina titia) exhibit a marked seasonal polyphenism in wing pigmentation throughout much of North America, with individuals emerging in the summer exhibiting conspicuous dark wings. Here, we test the hypothesis that this variation is an adaptive response to seasonal and geographical variation in predation risk. First, we find evidence for strong constraints acting on wing phenotypes outside of the summer season, consistent with a seasonal shift in the relative costs and benefits of pigmentation. Second, using a continentally distributed predation experiment, we find that predation risk covaries with spatiotemporal variation in wing pigmentation and is linked to shifts in the local abundance of migratory birds. Overall, our analyses establish an eco-evolutionary link between tropical and temperate regions, underscoring the importance of considering both the evolutionary and ecological consequences of spatiotemporal variation in biotic interactions as species assemblages shift in response to global change.

Understanding how populations persist in gradually deteriorating environments through evolution is a central question in ecology and evolutionary biology. Previous studies have primarily focused on identifying the critical rate of environmental change beyond which extinction is certain. However, the existence of a viable equilibrium when the rate is below the threshold does not guarantee that a population can survive the transient dynamics to reach it. Using a quantitative genetic model that explicitly incorporates feedback among population size, genetic variance, and mean trait evolution, we show that population persistence can exhibit bistability when the rate of environmental change is below the extinction threshold. Specifically, extinction still occurs if the initial population size and genetic variance fall below a critical level. The initial state also influences the eco-evolutionary dynamics, such that a temporary increase or decline in population size and/or genetic variance does not necessarily predict the ultimate fate of the population. Therefore, in addition to estimating the critical rate of environmental change for extinction, characterizing current population size, genetic variation, and the degree of maladaptation may improve predictions of extinction risk in deteriorating environments.

1. Plants produce a great chemodiversity, which is the diversity of specialized metabolites (SMs). These SMs are produced in complex metabolic pathways and play an important role in inter-species interactions. There are numerous hypotheses about the evolutionary processes which brought about and maintain chemodiversity. Some have been partially tested in lab and field studies. However, some of their assumptions and predictions are better tested by quantitative modeling, and so far no quantitative model has investigated the role of metabolic pathways. 2. To close this gap, we developed an individual-based model for metabolic pathway evolution. It models enzymes creating metabolites with various modifications. Enzymes undergo inheritance and mutation. We used the model to compare the screening and interaction diversity hypotheses. 3. The screening hypothesis predicts promiscuous enzymes, genetic drift, the presence of many non-beneficial metabolites, and high metabolite richness. The interaction diversity hypothesis predicts specialized enzymes, selection, the almost exclusive presence of beneficial metabolites, and situation- dependent metabolite richness. We found that the patterns predicted by the screening hypothesis did not occur, while those predicted by the interaction diversity hypothesis did. 4. This provides reason to favor the interaction diversity hypothesis over the screening hypothesis when connecting empirical results to their evolutionary context

The performance of any natural population in variable environments depends on contemporaneous changes in its vital rates (e.g., survival, reproduction) as well as legacies carried by its population structure. Yet whether the relative contribution of these two pathways can be predicted from life history remains unknown. Here, we use stochastic simulations of 1,986 matrix population models from 137 species to quantify the contribution of transient dynamics to variation in population growth rate, and test its associations with key life history traits. Longer generation times were associated with reductions in transient contributions, contrary to theoretical expectations. Greater stage-specific survival heterogeneities were associated with increases in transient contributions, whereas greater iteroparity was associated with decreases in plants but increases in animals. These associations were robust to body size, phylogenetic relationships, and vital-rate variability. Life history traits therefore provide a strong predictor for when population structure shapes population responses to environmental variability.

Transgenerational plasticity (TGP)- when parental environments influence offspring phenotypes - is ubiquitous across taxonomic groups and can have benefits for offspring beyond what is possible with developmental plasticity, particularly when selective pressures are high early in life. However, patterns of TGP vary widely across populations and species, and the evolutionary processes shaping this variation remain poorly understood. Here, we tested whether repeated evolutionary transitions result in parallel or population-specific evolutionary divergence in TGP relative to ancestral conditions. We examined sperm-mediated paternal effects across two ancestral marine and three derived freshwater populations of threespined stickleback fish (Gasterosteus aculeatus). We exposed fathers to dragonfly larvae (endemic to freshwater) or sculpin (endemic to all populations) predators and measured both paternal response to predators as well as antipredator behavior and growth in larval offspring. Fathers behaviorally responded to the presence of sculpin predators, but not dragonfly larvae. However, we found strong paternal effects in response to both predators in all populations. Further, the magnitude of TGP did not differ between marine and freshwater populations, suggesting that TGP does not become genetically accommodated as marine populations move into freshwater habitats. We found some evidence consistent with parallelism in both within and trans-generational plasticity: 1) personal exposure of larval stickleback to dragonfly larvae elicited strong antipredator responses in freshwater populations that were absent in marine populations, and 2) paternal predation exposure consistently increased offspring growth in marine populations while slowing growth in freshwater populations. In contrast, paternal effects altered offspring behavior in population-specific ways, with strong sex-specific effects of paternal exposure emerging in response to endemic predators. Adaptive evolution is a two-step process, in which heritable genotypic and phenotypic variation must first be present and then selected on. Therefore, high population-level variation in TGP suggests the capacity for rapid evolution of parental effects, while signatures of parallelism and sex-specific patterns suggest that TGP may evolve in targeted ways in response to ecological stressors.

Dominance is a widespread feature of genetic variants which affects life-history traits and fitness. Although dominance is generally thought to be an intrinsic property of genetic variants, it can sometimes evolve, as in the classic case of melanism in the peppered moth. The broader question of how likely dominance is to evolve is, however, controversial, because conditions favouring dominance evolution are often restrictive. Here, we revisit Haldanes classic hypothesis that dominance might evolve during the spread of beneficial mutations to fixation (i.e., during selective sweeps). We first confirm results of earlier models that sweeps of unconditionally beneficial mutations generate little potential for dominance to evolve, even in cases where modifier alleles segregate prior to selective sweeps. However, when sweeping beneficial alleles trade off between different environments -- which we explore with the illustrative case of sexually antagonistic selection -- the scope for dominance evolution expands. This occurs because modifier alleles can alter dominance separately in each environment, increasing the mean fitness of heterozygotes, prolonging the sojourn time of the sweep, and generating more heterozygosity upon which the modifier can act. In extreme cases, beneficial mutations that were initially destined for fixation can undergo a "dominance reversal" as a result of dominance evolution, converting them to balanced polymorphisms. We quantify how regularly dominance reversals of sweeping sexually antagonistic alleles can be expected to evolve. Overall, our results highlight conditions that allow the dominance of beneficial mutations to evolve, which we discuss in light of data on the frequency of selective sweeps, standing genetic variation for modifiers, and plasticity of modifier effects.