An individual's relatedness to its group may change with age due to demographic processes, and such kinship dynamics can shape age-linked social behaviors. Existing models, however, have focused almost exclusively on dispersal and mating, leaving the consequences of group size local variation unexplored. Here, we extend these models to incorporate such variation within a single, genetically connected meta-population. We then contrast predicted kinship dynamics and age-linked selection for helping/harming in coexisting smaller and larger groups in three typical social mammal systems characterized by distinct patterns of dispersal and mating, followed by exploring how group size local variation impacts female and male kinship dynamics across broader demographic contexts to clarify the population-genetic mechanisms. We show that, within the adult reproductive lifespans of these social systems, an individual's age-specific relatedness to others is higher, and changes faster (especially when younger), in smaller groups; consequently, smaller groups favor more extreme helping/harming (especially when younger)-in social system with bisexual philopatry with nonlocal mating (e.g., whales) that favors female shifts from harming to helping with age (which explains the evolution of menopause and postreproductive helping), such shifts are earlier in smaller groups. Further explorations suggest that, in a genetically connected population with group size local variation, group size effects on local relatedness are shaped by the relative strengths of ancestry dilution versus lineage coalescence, and kinship dynamics in a group reflect not only its local demographic conditions, but also those in coexisting groups of different size. Collectively, our study generates new insights into how female and male kinship dynamics emerge and vary under within-population group-size heterogeneity, and how such locally dynamic, varying kinship environments may help to explain variation in age-linked trends in social traits, such as the timing of menopause in social mammals.
Abstract Urbanisation profoundly alters natural habitats and reshapes many traits in wild species, including their reproduction. In birds, urban populations typically breed earlier and lay smaller clutches than their rural conspecifics, patterns usually attributed to warmer temperatures and lower food availability in cities. Yet, whether these differences reflect phenotypic plasticity or genetic change remains unclear. To disentangle environmental from genetic contributions, we conducted a common garden experiment with great tits (Parus major) originating from unincubated eggs collected in urban and forest habitats. Nestlings were hand-reared under identical conditions and, the following spring, paired by origin in breeding aviaries. We recorded laying date, clutch size, egg volume, and fertilisation success, and compared them with wild phenotypic distributions. Contrary to patterns in the wild, laying dates did not differ between urban- and forest-origin females, revealing a plastic adjustment of the onset of breeding to the environment. Egg size remained consistently smaller in urban-origin females across both conditions, pointing to a genetic divergence. No difference in fertilisation rate was found between individuals of urban and forest origin in the common garden. Finally, clutch size differences showed striking opposite patterns between experimental and wild birds: in the common garden urban-origin females laid larger, and not smaller, clutches than forest-origin females, suggesting a counter-gradient variation where genetic and environmental effects act in opposing directions on the phenotype. Overall, our study showcases how integrating experimental designs with field monitoring can uncover the hidden dynamics of urban adaptation, including cryptic evolution masked by environmental constraints in cities.
Understanding reproductive isolation (RI) between lineages is a central goal of speciation research. While the strength of RI has been estimated across a broad range of taxa, synthesizing these data remains challenging, partially because we lack a common language for classifying and reporting RI estimates. Here, we present the Reproductive Isolation Ontology (RIO), a structured framework designed to standardize the classification of RI estimates across most sexually reproducing organisms. The RIO comprises 3 interrelated domains, each organized into a nested hierarchy of classification terms. We demonstrate the utility of this approach and call for researchers to adopt and expand the RIO to facilitate the integration of speciation research.
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.
Facing geographical barriers, phenotypic responses of migratory landbirds may differ even between closely related taxa: some may bypass barriers while others cross them. Such phenotypic variation can arise from different genetic backgrounds and lead to different adaptive processes. A classic example is migratory divide, i.e., breeding ranges where different migration-route phenotypes co-exist or meet. Such variation can facilitate an understanding of the evolutionary background of migration and responses to barriers. In Asia, a migratory divide has been suggested in response to the major landscape, the Qinghai-Tibet Plateau (QTP) for 2 stonechat taxa (Siberian stonechat Saxicola maurus maurus and Amur stonechat S. stejnegeri). Detouring along either side of the QTP, these taxa are believed to disfavor crossing over the highland. However, the Tibetan stonechat (S. m. przewalskii), breeding on the QTP, may differ in its barrier response due to possible adaptation to high elevation. To investigate migration patterns and potentially associated genetic differences, we studied migration routes and population genetics of populations around the assumed migratory divide in Russia and Mongolia and of a Chinese population from the QTP. Our results confirmed the existence of a migratory divide between maurus and stejnegeri, albeit with extensive hybridization over generations. Of the 3 genotyped individuals employing intermediate routes across the QTP, 2 were clear hybrids. Meanwhile, przewalskii consistently followed a highland-crossing route and was genetically differentiated from maurus and stejnegeri. The diverse migration routes indicate that Asian stonechats respond differently to the geographical barrier. The partly viable intermediate route may be associated with hybridization and potentially facilitating gene flow between maurus and stejnegeri. The Asian stonechat complex thus offers great opportunities for research, with its specific evolutionary background associated with inhabiting and crossing the QTP, offering novel perspectives on the genetics and evolution of migration.
At the species level, the evolution of traits is driven by a combination of selective and neutral forces. To disentangle these processes, different scenarios of evolution are modeled and compared. For quantitative traits under selection, the species is usually considered to track a trait optimum, and such an optimum can change along the branches of the species tree. On the other hand, neutral evolution is modeled with a trait changing randomly around the ancestral trait value along the different branches of the species tree. Regardless of the intricacy of modeling trait changes, the species tree is assumed to be known and obtained independently of the trait data analysed. Branch lengths are usually assumed to be in units proportional to time, and the tree is represented by a chronogram. The rationale is that time correlates with trait changes because of its direct connection with the number of generations that have occurred. However, since the generation time of species can also vary along the phylogenetic tree, we argue that their use introduces biases. In contrast, if the phylogenetic tree is represented by a phylogram with branch lengths in units of sequence divergence, this will account for the effect of changing generation time. In this study, we show using simulations that, for a trait evolving neutrally, the fit of a random evolution model has more support on a phylogram than on a chronogram. However, comparing models and testing different scenarios of selection using a phylogram leads to incorrect predictions. Given these results, we argue that we should use phylograms instead of chronograms when claiming that a trait is evolving under drift. Nevertheless, we support the generally accepted use of chronograms to model selection acting on a quantitative trait.
While developmental plasticity helps organisms to maintain fitness as environments change, such plasticity has limits. When novel environments exceed these limits and mean fitness declines, the extent of decline is expected to vary among genotypes, which could increase adaptive potential. We lack fundamental insights into whether genetic variation in early development is linked to adaptive potential in novel environments, which limits our ability to predict how natural populations will respond to global change. Using a breeding design, we generated c. 20,000 seeds of 2 ecologically contrasting Sicilian species of daisies (Senecio, Asteraceae) adapted to high and low elevations on Mount Etna. We planted the seeds across 4 elevations that included elevations within the native range of each species, the edge of their range, and a novel elevation. We tracked seedling mortality and measured development time as the number of days it took seedlings to establish. As predicted, genetic variance in survival increased at novel elevations, suggesting that adaptive potential consistently increases for contrasting species facing different novel environments. However, genetic variance in development time showed the opposite trend, decreasing at novel elevations. A strong negative genetic correlation between development time in the native range and survival at novel elevations suggested that genotypes with faster development in native environments survived better in novel environments. These results were consistent across the two ecologically contrasting species, suggesting that genetic variance in early development in native environments could be used to predict genotypes that increase adaptive potential in novel environments.
Inbreeding depression (ID)-the reduction in fitness with increasing parental relatedness-is classically attributed to the expression of recessive deleterious mutations in homozygous individuals. Yet, the assumption that ID can only arise from changes in genetic heterozygosity has rarely, if ever, been directly tested. To test this, we produced highly inbred lines (F = 0.99999997) of the freshwater snail Physa acuta and generated offspring that differed in parental relatedness (self-fertilization, sib or cousin matings) while their parents, produced by crossing two inbred lines, all shared an identical genome. Several fitness traits showed significant declines with increasing parental relatedness. These traits included juvenile survival, body size, and self-fertility, and the magnitude of their decline was equivalent to a substantial fraction of the ID observed in natural, genetically polymorphic populations of P. acuta. Individual-based simulations demonstrated that spontaneous mutation rates compatible with natural levels of ID are far too low to account for the magnitude of ID observed here. These findings suggest that non-genetic mechanisms, most plausibly involving heritable epigenetic changes, can generate ID even in genetically uniform populations. This challenges the long-standing view that ID arises exclusively from genetic homozygosity and highlights the need to investigate epigenetic contributions to ID.
The spectacular diversity of flowers is largely driven by pollinator-mediated selection that favors attractive flowers and effective pollen transfer. Urbanization has the potential to affect floral trait evolution by altering pollinator communities through environmental changes. Additionally, abiotic changes in urban habitats can induce phenotypic plasticity, further shaping evolutionary trajectories. We investigated how urbanization affects the genetic and plastic components of flower morphology of Impatiens capensis (Balsaminaceae) across four Canadian cities. We found that urbanization influenced the pollinator community composition and the body size of bumblebees, the species' main pollinator, although the magnitude of the size effect varied among cities. Using a combination of field surveys and a common garden experiment, our results suggest that urbanization affects sepal size-a tubular floral organ in which pollinators enter to access the nectar-through both genetic and plastic responses. While plasticity sometimes masked the genetic determination of sepal size in the field, we observed a positive correlation between the genetic component of the sepal size and bumblebee body size. These results suggest that urban habitats may drive evolutionary changes in floral traits by modifying pollinator communities.
The rapid pace of environmental change has prompted pressing concerns about the persistence of wild populations. For plants, because they move from one place to another only passively between generations, their persistence is especially likely to depend on their capacity for ongoing adaptive evolution. There are numerous examples of rapid adaptation in the recent past, but evidence about rates of adaptation in the wild is limited. Previously, to assess the capacity for genetic adaptation of three wild plant populations growing in their source locations, we have estimated their additive genetic variance for fitness in three successive years. Here, we present the actual difference between successive generations in their average absolute fitness. We partition this change into components resulting from genetic change and due to environmental difference, as well as a residual component. In each of six cases of intergenerational change, we have detected evolutionary adaptation as genetic increase in average fitness during the first generation, while also finding generally greater effects of differences in environment between years. Nevertheless, we show that when environmental change reduces a population's average fitness, these adaptive genetic responses often substantively ameliorate its deleterious impact.
The spontaneous mutation rate (μ) is shaped by two distinct forces: the passage of chronological time, inevitably associated with mutation accumulation, and the speed of development, where rapid replication contributes to error rates. Disentangling these forces has been a major challenge, particularly in ectotherms. Testing the distinct predictions of the classic replication-dependent generation length hypothesis and the time-dependent accumulation model, we experimentally assessed individuals with naturally short (15 days) and long (38 days) generation time (GT), which is mainly determined by differences in developmental speed in the midge Chironomus riparius. To overcome the challenges of swarm-mating, we employed a parent-offspring pedigree reconstruction approach using pooled sequencing of siblings to infer parental allelic composition. We estimated the de novo mutation rates by whole genome sequencing. We found that Long-GT groups accumulated 1.2-fold more total mutations per generation (μ/gen), consistent with time-dependent mutagenic processes. Conversely, Short-GT groups exhibited a nearly two-fold higher mutation rate per day (μ/day) and a trend toward a transition-biased mutational spectrum (Ts/Tv ratio = 1.14 vs. 0.89), a pattern consistent with a replication-dependent errors in DNA. These results suggest that the overall mutation load is the product of these two interacting processes. Integrating our data with previous studies and life-history data, we show that the daily mutation rate followed a non-linear relationship with respect to developmental speed, and that the species' generation time mode coincides with its minimum. This suggests that the developmental speed is, amongst other factors, selected to optimize the mutational load by balancing between replication accuracy and developmental speed.
As large-scale genomic datasets are becoming abundant, new questions can now be posed in evolutionary biology. Although innovative methodological approaches are constantly developed to test these new hypotheses, their application to the study of nonmodel species is hampered by technical challenges associated with such systems. In recent years, artificial intelligence (AI) solutions, mostly in the form of deep neural networks, have been successfully introduced to analyse genomic data from nonmodel species. Here, we highlight the latest trends in deep learning to infer demographic history and signals of natural selection, and offer novel research directions to develop AI algorithms for the study of nonmodel organisms. Specifically, we identify strategies to process data missingness and uncertainty, to infer selective events in the face of unknown genomic and demographic parameters, and to generate interpretable and explainable predictions. We demonstrate our arguments by showcasing an original implementation to detect selective sweeps from an experimental setting with low sample size, uncertain sequencing data, and unknown demographic model, as typical in studies of nonmodel species. We argue that the study of nonmodel organisms is an opportunity to develop general-purpose data-driven methodologies for evolutionary inferences. Fair sharing of resources and inclusive frameworks are key to enabling researchers to benefit the most from this new wave of technologies.
Sensory traits shape animal lifestyles due to the central role they play in retrieving and processing environmental information. However, being some of the most energetically expensive tissues to build and maintain, ecological demands often modulate investment in these organs. Evidence that ecology shapes the evolution of sensory traits is plenty, but is heavily biased towards vertebrates and has only recently begun to emerge in invertebrates. Here, we elucidate the macroevolution of a key sensory organ-eye size-using temperate butterflies as models. Using micro-CT X-ray imaging of pinned museum specimens, we quantified the eye size of 443 individuals comprising 59 species. Further, using 12 years of long-term monitoring data to quantify species habitat, we tested the hypothesis that forest-associated species, likely experiencing dimmer light conditions, should have larger eyes than those from open habitats. Our comparative analyses revealed tight allometric scaling between eye and wing size, and phylogeny alone explained 74% of eye size variation, with low heterogeneity in the evolutionary rates. Further, we found that habitat structure had no association with eye size. Overall, our findings indicate that allometry and shared ancestry, not ecology, shape the macroevolution of 3D eye size in temperate butterflies. We also demonstrate how non-invasive microCT imaging can be used on pinned museum specimens for studying phenotypic evolution on a macroevolutionary scale.
Bony fishes (Osteichthyes) occupy a diverse range of aquatic habitats, yet the ecological transitions underlying their early evolution remain debated. Extant "living fossil" lineages-such as lungfishes and basal ray-finned fishes-are primarily restricted to benthic freshwater habitats, raising questions about the ancestral ecology of bony fishes. To investigate this, we reconstructed and expressed visual pigments from both extant and inferred ancestral taxa in vitro, enabling characterization of their spectral sensitivities. The results reveal that the ancestral visual phenotype is most consistent with adaptation to shallow-water light conditions. Furthermore, parallel shifts in the spectral tuning of visual pigments across both lobe-finned and ray-finned fish lineages were observed, with consistent patterns of shorter wavelength tuning in middle/long-wavelength-sensitive pigments, paired with longer wavelength shifts in others. The shifts of spectral tuning support an ecological transition from marine to freshwater habitats. Additionally, changes in rhodopsin retinal release rates and signatures of positive selection on opsin genes further point to independent visual adaptations to freshwater environments in both lineages. These findings suggest that early bony fish evolution involved ecological expansion from shallow marine habitats into deeper or more turbid freshwater environments, as reflected in parallel adaptations of visual systems to benthic photic conditions.
Theories on the evolutionary origins of human aggression have often implicitly assumed that conspecific aggression is a single behavioral trait. However, different types of aggression can be described, based upon their intensity, frequency, as well as the age and sex of the opponents. The phylogenetic relationships between different types of aggression remain poorly understood. We tested the strength of correlated evolution between five distinct types of aggression in primates, namely, between- and within-group mild (i.e., not life-threatening) aggression, between- and within-group adulticide, and infanticide. We collected data on 100 free-ranging, non-provisioned and group-living species, including humans. Phylogeny had a weaker effect on mild than on lethal aggression; the effect of phylogeny was greater for adulticide, especially when we partitioned our analyses by the sex of the attacker. Furthermore, we found a positive correlation between within- and between-group adulticide, and with infanticide; these results were mostly confirmed when we considered the sex of the attacker. Conversely, the two types of mild aggression were weakly related with lethal aggression. Our study highlights the importance of treating aggression as a complex set of interrelated traits in comparative analyses. Our findings indicate that mild aggression is not closely linked to killing; thus, the escalation of aggression may follow more complex patterns that what predicted by current socio-ecological models.
Strong disparity in species richness among organisms is well documented, but heterogeneity in the underlying diversification process is less understood. Using novel probabilistic methods, we investigate clade-specific diversification rate shifts in several species-rich phylogenies, together representing over 300,000 species across the Tree of Life. We find that diversification rate shifts are extremely prevalent across all clades, with more frequent changes in younger clades and an overall excess of upshifts, resulting in an apparent acceleration of net diversification rates. We also reveal that heterogeneity in diversification rates is related to the tempo of diversification itself. While we find support for more prevalent shifts in speciation rates than extinction rates and more upshifts than downshifts, this is partially due to data insufficiency and inference challenges. Our insights are fundamentally enabled by studying numerous large phylogenies with rigorous statistical methods, showing widespread prevalence of diversification rate shifts across the Tree of Life.
The formation of habits, whereby learnt actions come to be performed automatically with repetition and practice, is a well-established focus for studies in psychology. This contrasts with evolutionarily motivated studies of learning, which typically view behavior as either learnt or fixed, to elucidate the ecological conditions where each predominates. Here, we envisage habit formation functioning to free up limited mental resources (e.g., attention), potentially improving an individual’s ability to multitask. As an ecologically relevant case, we investigate exploration-exploitation in foraging under predation risk. In our model, a forager does not know the quality of feeding options, but can learn from the rewards they give. When the environment occasionally changes, individuals can attend to exploration of feeding options in the new conditions. The options can then become habitually exploited, freeing attention for antipredatory vigilance. Via evolutionary simulations, we show that evolutionarily stable forming and breaking of foraging habits can substantially reduce mortality from predation, without drastically reducing foraging success, when environmental conditions remain stable enough between changes. We identify factors promoting habit formation, such as the repetition of actions that yield predictable rewards, and also discuss the role of habits more generally, including their relation to ideas about bounded rationality in theories of decision making. In conclusion, we argue that exploration-exploitation strategies involving the forming and breaking of habits are a type of behavioral flexibility that is likely to be selected for under a range of ecological conditions. The forming and breaking of habits has long been a focus of study in psychology, as well as appearing in many discussions about human behavior. Surprisingly, the topic has been virtually absent from evolutionary studies of learning in non-human animals, despite featuring prominently in Darwin’s discussion of the evolution of species-specific behaviors. Our aim is to change this, by theoretically investigating a possible evolutionary explanation for habits, namely that habits enhance an individual’s ability to multitask. We model the combination of foraging and antipredator vigilance, which is important for many animal species in their natural environments. We conclude that the forming and breaking of habits can promote behavioral flexibility, helping animals to achieve important tasks in different environments.
Longevity, a major fitness component, is heritable in multiple species including both captive and wild populations, and often varies widely between the sexes. The sex-specific genetic architecture of longevity however has rarely been estimated in wild populations, despite its potentially large implication for the evolutionary dynamic of a species. Using a long-term study of wild yellow-bellied marmots, a hibernating rodent, we estimated sex-specific additive genetic variance VA and the cross-sex genetic correlation rfm of longevity. Given the challenges associated with accurately measuring longevity in the wild, we used a new analytical approach based on a Censored Poisson distribution allowing us to integrate measurement errors on longevity in the model. Our approach revealed moderate and comparable VA in both sexes and a strongly negative rfm, albeit with large credible intervals. This contrasts with the results from a classic model with a restricted dataset for which VA in males was estimated as zero, rendering the rfm inestimable and uninterpretable. Our results suggest that studying selection and evolution while focusing on only one sex can lead to erroneous predictions given that, in marmots, selection pressures increasing longevity in one sex would inherently select for the reverse effect in the other sex. Taken together, this suggests the possible presence of a self-reinforcing feedback loop for the development of different life-history strategies among sexes in marmots, with long-lived females producing short-lived males who must maximize early life reproductive success (“live-fast die-young” strategy) and vice-versa. Our study provides rare evidence of heritable longevity in a wild population and highlights how genetic conflicts between the sexes may constrain evolution and help maintain sex-specific genetic variance in fitness.
Analysis often splits change into components. For example, how much of the observed variance is caused by genes or environment? In many cases, the split is ultimately made by the logic of the chain rule, which divides the difference of a product into two terms. Each term quantifies the partial difference associated with change in one component while holding the other component constant. The chain rule is of course widely known. However, this article argues that its deep fundamental role often goes unrecognized. The article shows how simply the basic chain rule unifies Fisher's fundamental theorem of natural selection, the Price equation description of evolutionary change, the Oaxaca-Blinder decomposition of wage differences in economics, the Kitagawa decomposition of mortality differences in demography, many expressions of thermodynamics, and most strikingly back propagation, the core optimization method of modern machine learning and artificial intelligence. The success in creating good designs and finding good solutions in both natural selection and artificial intelligence depends on how the chain rule propagates causes from instances of success or failure back to the underlying genes or parameters of the system. The mathematical analysis presented here shows that, for finite differences, the product rule form of the chain rule yields a basic decomposition of change into two components of a regression equation. That regression decomposition is purely a description of change with no explicit causal meaning. However, simple additional assumptions lead naturally to the modern counterfactual analysis of causality. From that perspective, we can easily understand the causal interpretation that Fisher gave to his fundamental theorem, and we can see the same causal structure in the Oaxaca-Blinder decomposition of economics and in causal analyses across many disciplines.
Sexual selection can be an engine of divergent evolution between closely related lineages, as a result of idiosyncratic coevolution of male and female reproductive traits. The possibility that this can contribute to speciation has ample support from comparative studies but very few experimental evolution studies have addressed the role of sexual selection in very early stages of divergent evolution. Here, we use experimental evolution to study divergent evolution between replicate lines of the seed beetle Acanthoscelides obtectus evolving under strong or weak sexual selection for >190 generations. We first confirm that the experimental regimes employed resulted in marked differences in the strength of sexual selection. We then indirectly assess the degree of divergent evolution of those male and female traits that affect postmating sexual selection, by crossing replicate lines. We find that lines evolving under strong sexual selection are more divergent in reproductive traits, as evidenced by a stronger male × female interaction for male sperm competition success. Finally, we assess the degree of divergent evolution in the expression of candidate genes for male seminal fluid proteins and female reproductive proteins. We find that lines evolving under strong sexual selection are more divergent in the expression of reproductive proteins, providing a possible causal mechanism contributing to the results seen in the reproductive phenotype. Our findings provide evidence for more divergent evolution of reproductive traits under stronger sexual selection, in line with the tenet that sexual selection may promote divergence even in the absence of environmental differences between populations.
