Abstract Neo-sex chromosomes have proven powerful for studying the early stages of sex chromosome evolution and differentiation, yet if these dynamic processes could contribute to the emergence of new species remains unclear. The mountain pine beetle (Dendroctonus ponderosae), a major forest pest, is suspected of harboring neo-Y diversity that contributes to cryptic species boundaries. Here, we generated six chromosome-level assemblies (male and female from the three neo-Y populations) to examine the evolutionary processes contributing to differences between, and within, the neo-X and neo-Y chromosomes. Using comparative genomics approaches, we find the large sex chromosomes formed through sequential fusions with three large autosomes, with recombination cessation occurring between the neo-X and neo-Y at multiple distinct time points (∼4.3 to ∼8.6 MYA). Comparative analyses reveal that while the neo-X chromosomes remain largely collinear across populations, only ∼65% of the highly rearranged neo-Y can be aligned to the neo-X. We find dramatic structural divergence between the three neo-Ys which likely contributes to the extensive degeneration despite only moderate accumulation of repeats. All populations retain a single pseudoautosomal region (PAR), though PAR size and gene content also vary due to neo-Y specific rearrangements. We document a pattern of rapid, ongoing, and variable gene loss across neo-Y chromosomes in the mountain pine beetle. Some genes undergoing degeneration are associated with early-stage reproductive isolation phenotypes previously characterized in crossing experiments. Together, these results highlight how rapid genome restructuring through chromosomal fusions and Y chromosome degeneration can occur at evolutionary time scales relevant to the evolution of new species.
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.
