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Weyna, A.

Publications and source records attributed to Weyna, A..

8 recordsLinked to original sources

Directional and disruptive selection in populations structured by class and continuous ontogeny under incomplete plasticity

Many organisms undergo ontogeny, whereby individuals change in state (e.g. in size, morphology, or condition) as they age. Understanding the evolution of traits influencing ontogeny is challenging because their fitness effects unfold across an individuals lifetime and may differ between classes such as sexes. Here, we analyse selection on non-plastic traits (e.g., fixed resource allocation strategies) that determine the development of dynamical states throughout life (e.g., body size), with consequences for fecundity and survival in age- and class-structured populations. Using invasion analysis, we derive expressions for directional and quadratic selection that decompose into age- and class-specific components. This allows us to identify convergence stable trait values, assess whether they are uninvadable or potentially experience evolutionary branching, and pinpoint the age and class pathways through which correlational and disruptive selection act. Applying our results to a model of growth under size-mediated sexual selection, we show how selection on growth rates distributes across ages and sexes, and how its relative strength depends on genetic correlations, individual ploidy and life-history. We also show how sex-specific developmental trade-offs and constraints can generate disruptive selection on male growth and favour the evolution of alternative male life histories. More broadly, our results highlight how adaptation is mediated by the interaction of development and demography, and provide tools to investigate how conflicts across ages and classes may influence senescence, sexual dimorphism, and the diversification of ontogenetic strategies. Author SummaryHow does natural selection shape traits that influence how organisms develop through their lifetime? This question is difficult because the effects of such traits unfold dynamically as individuals change in states such as size or condition, which in turn influence survival and reproduction throughout life. We formulate a mathematical model that follows these causal links and characterises the gradual evolution of non-plastic traits affecting development. Our results apply to populations with different classes, such as males and females, that follow distinct developmental and demographic paths. Our model reveals when selection is stabilizing, holding populations fixed for an optimal trait value, and when it is disruptive, favouring trait diversification and the emergence of alternative life-history strategies. As an illustration, we analyse the evolution of sex-specific growth under size-based sexual selection. We show how the evolution of male and female growth rates depends on genetics, such as individual ploidy or genetic correlation between traits, but also on life history, which determines the relative strength of selection acting on trait expression at different ages. We further show how developmental trade-offs and demographic differences can generate disruptive selection on male growth, leading to the coexistence of fast-growing short-lived males and slow-growing long-lived ones. More broadly, our results link development, demography, and adaptation, and show how their interplay shapes biological diversity both within and between populations.

evolutionary biology↗

Phylogenomics of Messor harvester ants (Hymenoptera: Formicidae: Stenammini) unravels their biogeographical origin and diversification patterns

As a major abiotic factor, climate change is expected to profoundly alter biological communities. On this basis, identifying how past temperature variations affected species diversification and distribution can help to predict the effects of the ongoing climate change. In this study, we focused on the harvester ant genus Messor which is mostly adapted to dry environments dominated by seed-producing plants. The phylogenetic analysis of 2,524 markers obtained from 58 Messor species/subspecies, supports their emergence in the Irano-Indian area approximately 20 Mya. Phylogenetic relationships uncovered in this study enabled us to redefine historical taxonomic groups, providing a solid basis for future revisions that encompass the entire genus diversity. Their diversification appears to be affected by temperature, with a higher speciation rate during warmer periods. This confirms that the ecological specialization of Messor makes them strongly dependent on thermal conditions. Our results highlight the importance of abiotic factors on diversification processes, especially for highly specialized species that may exhibit predictable evolutionary responses to climate changes.

evolutionary biology↗

Social evolution in termites reduces natural selection efficacy

In eusocial species, reproduction is monopolized by a few reproductive individuals. From the perspective of population genetics, this implies that the effective population size (Ne) of these organisms is likely to be smaller compared to solitary species, as has been proposed in the literature for eusocial hymenoptera. In this study, we investigate the genomic consequences of eusociality in termites (Isoptera) on two different timescales. First, by analyzing transcriptome data from 66 Blattodea species, we focus on the ratio of non-synonymous to synonymous mutations (dN/dS) as a marker of natural selection efficiency and effective population size. Our results demonstrate an elevated dN/dS ratio in termites compared to other members of Blattodea, further generalizing the idea that convergent evolution toward eusociality strongly reduces the effective population size and the genome-wide efficiency of natural selection. Then, by comparing 68 termite transcriptomes, we show that this decrease in natural selection efficiency is even more pronounced in termites displaying high levels of social complexity. This study contributes to understanding the complex interplay between social structures and natural selection patterns, highlighting the genetic footprint of eusociality in shaping the evolution of termites.

evolutionary biology↗

Detection of F1 hybrids from single-genome data reveals frequent hybridization in Hymenoptera and particularly ants

Hybridization occupies a central role in many fundamental evolutionary processes, such as speciation or adaptation. Yet, despite its pivotal importance in evolution, little is known about the actual prevalence and distribution of hybridization across the tree of life. Here we develop and implement a new statistical method enabling the detection of F1 hybrids from single-individual genome sequencing data. Using simulations and sequencing data from known hybrid systems, we first demonstrate the specificity of the method, and identify its statistical limits. Next, we showcase the method by applying it to available sequencing data from more than 1500 species of Arthropods, including Hymenoptera, Hemiptera, Coleoptera, Diptera and Archnida. Among these taxa, we find Hymenoptera, and especially ants, to display the highest number of candidate F1 hybrids, suggesting higher rates of recent hybridization in these groups. The prevalence of F1 hybrids was heterogeneously distributed across ants, with taxa including many candidates tending to harbor specific ecological and life history traits. This work shows how large-scale genomic comparative studies of recent hybridization can be implemented, uncovering the determinants of hybridization frequency across whole taxa.

evolutionary biology↗

Hybridization enables the fixation of selfish queen genotypes in eusocial colonies

A eusocial colony typically consists of two main castes: queens that reproduce and sterile workers that help them. This division of labour however is vulnerable to genetic elements that favour the development of their carriers into queens. Several factors, such as intra-colonial relatedness, can modulate the spread of such caste-biasing genotypes. Here we investigate the effects of a notable yet understudied ecological setting: where larvae produced by hybridization develop into sterile workers. Using mathematical modelling, we show that the coevolution of hybridization with caste determination readily triggers an evolutionary arms race between non-hybrid larvae that increasingly develop into queens, and queens that increasingly hybridize to produce workers. Even where hybridization reduces worker function and colony fitness, this race can lead to the loss of developmental plasticity and to genetically hard-wired caste determination. Overall, our results may help understand the repeated evolution towards remarkable reproductive systems (e.g. social hybridogenesis) observed in many ant species.

evolutionary biology↗

Relaxation of purifying selection suggests low effective population size in eusocial Hymenoptera and pollinating bees

With one of the highest number of parasitic, eusocial and pollinator species among all insect orders, Hymenoptera features a great diversity of lifestyles. At the population genetic level, such life-history strategies are expected to decrease effective population size and the efficiency of purifying selection. In this study, we tested this hypothesis by estimating the relative rate of non-synonymous substitution in 169 species to investigate the variation in natural selection efficiency throughout the hymenopteran tree of life. We found no effect of parasitism, but we show that relaxed selection is associated with eusociality, suggesting that the division of reproductive labour decreases effective population size in ants, bees and wasps. Unexpectedly, the effect of eusociality is marginal compared to a striking and widespread relaxation of selection in both social and non social bees, which indicates that these keystone pollinator species generally feature low effective population sizes. This widespread pattern suggests specific constraints in pollinating bees potentially linked to limited resource availability and high parental investment. The particularly high load of deleterious mutations we report in the genome of these crucial ecosystem engineer species also raises new concerns about their ongoing population decline. This article has been peer-reviewed and recommended by Peer Community in Evolutionary Biology https://doi.org/10.24072/pci.evolbiol.100120

evolutionary biology↗

Evolutionary history of the porpoises (Phocoenidae) across the speciation continuum: a mitogenome phylogeographic perspective

Historical changes affecting food resources are a major driver of cetacean evolution. Small cetaceans like porpoises (Phocoenidae) are among the most metabolically challenged marine mammals and are particularly sensitive to changes in their food resources. The seven species of this family inhabit mostly temperate waters and constitute a textbook example of antitropical distribution. Yet, their evolutionary history remains poorly known despite major conservation issues threatening the survival of some porpoises (e.g., vaquita and Yangzte finless porpoises). Here, we reconstructed their evolutionary history across the speciation continuum, from intraspecific subdivisions to species divergence. Phylogenetic analyses of 63 mitochondrial genomes suggest that, like other toothed whales, porpoises radiated during the Pliocene in response to deep environmental changes. However, all intra-specific phylogeographic patterns were shaped during the Quaternary Glaciations. We observed analogous evolutionary patterns in both hemispheres associated with convergent adaptations to coastal versus oceanic environments. This result suggests that the mechanism(s) driving species diversification in the relatively well-known species from the northern hemisphere may apply also to the poorly-known southern species. In contrast to previous studies, we showed that the spectacled and Burmeisters porpoises share a more recent common ancestor than with the vaquita that diverged from southern species during the Pliocene. The low genetic diversity observed in the vaquita carried signatures of a very low population size throughout at least the last 5,000 years, leaving one single relict mitochondrial lineage. Finally, we observed unreported subspecies level divergence within Dalls, spectacled and Pacific harbor porpoises, suggesting a richer evolutionary history than previously suspected. These results provide a new perspective on the mechanism driving the adaptation and speciation processes involved in the diversification of cetacean species. This knowledge can illuminate their demographic trends and provide an evolutionary framework for their conservation.

evolutionary biology↗

How do invasion syndromes evolve? An experimental evolution approach using the ladybug Harmonia axyridis

Experiments comparing native to introduced populations or distinct introduced populations to each other show that phenotypic evolution is common and often involves a suit of interacting phenotypic traits. We define such sets of traits that evolve in concert and contribute to the success of invasive populations as an invasion syndrome. The invasive Harlequin ladybird Harmonia axyridis displays such an invasion syndrome with, for instance, females from invasive populations being larger and heavier than individuals from native populations, allocating more resources to reproduction, and spreading reproduction over a longer lifespan. Invasion syndromes could emerge due to selection acting jointly and directly on a multitude of traits, or due to selection on one or a few key traits that drive correlated indirect responses in other traits. Here, we investigated the degree to which the H. axyridis invasion syndrome would emerge in response to artificial selection on either female body mass or on age at first reproduction, two traits involved in their invasion syndrome. To further explore the interaction between environmental context and evolutionary change in molding the phenotypic response, we phenotyped the individuals from the selection experiments in two environments, one with abundant food resources and one with limited resources. The two artificial selection experiments show that the number of traits showing a correlated response depends upon the trait undergoing direct selection. Artificial selection on female body mass resulted in few correlated responses and hence poorly reproduced the invasion syndrome. In contrast, artificial selection on age at first reproduction resulted in more widespread phenotypic changes, which nevertheless corresponded only partly to the invasion syndrome. The artificial selection experiments also revealed a large impact of diet on the traits, with effects dependent on the trait considered and the selection regime. Overall, our results indicate that direct selection on multiple traits was likely necessary in the evolution of the H. axyridis invasion syndrome. Furthermore, they show the strength of using artificial selection to identify the traits that are correlated in different selective contexts, which represents a crucial first step in understanding the evolution of complex phenotypic patterns, including invasion syndromes.

evolutionary biology↗