Major population splits coincide with episodes of rapid climate change in a forest-dependent bird

Climate change influences population demography by altering patterns of gene flow and reproductive isolation. Direct mutation rates offer the possibility for accurate dating on the within-species level but are currently only available for a handful of vertebrate species. Here, we use the first directly estimated mutation rate in birds to study the evolutionary history of pied flycatchers (Ficedula hypoleuca). Using a combination of demographic inference and species distribution modelling, we show that all major population splits in this forest-dependent system occurred during periods of increased climate instability and rapid global temperature change. We show that the divergent Spanish subspecies originated during the Eemian-Weichselian transition 115-104 thousand years ago (kya), and not during the last glacial maximum (26.5-19 kya), as previously suggested. The magnitude and rates of climate change during the glacial-interglacial transitions that preceded population splits in pied flycatchers were similar to, or exceeded, those predicted to occur in the course of the current, human-induced climate crisis. As such, our results provide a timely reminder of the strong impact that episodes of climate instability and rapid temperature changes can have on species' evolutionary trajectories, with important implications for the natural world in the Anthropocene

Contrasting Patterns of Polymorphism and Divergence on the Z Chromosome and Autosomes in Two Ficedula Flycatcher Species

In geographic areas where pied and collared flycatchers (Ficedula hypoleuca and F. albicollis) breed in sympatry, hybridization occurs, leading to gene flow (introgression) between the two recently diverged species. Notably, while such introgression is observable at autosomal loci it is apparently absent at the Z chromosome, suggesting an important role for genes on the Z chromosome in creating reproductive isolation during speciation. To further understand the role of Z-linked loci in the formation of new species, we studied genetic variation of the two species from regions where they live in allopatry. We analyzed patterns of polymorphism and divergence in introns from 9 Z-linked and 23 autosomal genes in pied and collared flycatcher males. Average variation on the Z chromosome is greatly reduced compared to neutral expectations based on autosomal diversity in both species. We also observe significant heterogeneity between patterns of polymorphism and divergence at Z-linked loci and a relative absence of polymorphisms that are shared by the two species on the Z chromosome compared to the autosomes. We suggest that these observations may indicate the action of recurrent selective sweeps on the Z chromosome during the evolution of the two species, which may be caused by sexual selection acting on Z-linked genes. Alternatively, reduced variation on the Z chromosome could result from substantially higher levels of introgression at autosomal than at Z-linked loci or from a complex demographic history, such as a population bottleneck

Data from: The evolution of sexual imprinting through reinforcement

Reinforcement is the process whereby assortative mating evolves due to selection against costly hybridization. Sexual imprinting could evolve as a mechanism of reinforcement, decreasing hybridization, or it could potentially increase hybridization in genetically purebred offspring of heterospecific social pairs. We use deterministic population genetic simulations to explore conditions under which sexual imprinting can evolve through reinforcement. We demonstrate that a sexual imprinting component of female preference can evolve as a one-allele assortative mating mechanism by reducing the risk of hybridization, and is generally effective at causing trait divergence. However, imprinting often evolve to be a component rather than the sole determinant of female preference. The evolution of imprinting has the unexpected side effect of homogenizing existing innate preferences, because the imprinted preference neutralizes any innate preference. We also find that the weight of the imprinting component may evolve to a lower value when migration and divergent selection are strong and the cost of hybridization is low; these conditions render hybridization adaptive for immigrant females because they can acquire locally adaptive genes by mating with local males. Together, these results suggest that sexual imprinting can itself evolve as part of the speciation process, and in doing so has the capacity to promote or retard divergence through complex interactions

Data from: Hybrid speciation by sorting of parental incompatibilities in Italian sparrows

Speciation by hybridization is emerging as a significant contributor to biological diversification. Yet, little is known about the relative contributions of (i) evolutionary novelty and (ii) sorting of preexisting parental incompatibilities to the build-up of reproductive isolation under this mode of speciation. Few studies have addressed empirically whether hybrid animal taxa are intrinsically isolated from their parents, and no study has so far investigated by which of the two aforementioned routes intrinsic barriers evolve. Here, we show that sorting of preexisting parental incompatibilities contributes to intrinsic isolation of a hybrid animal taxon. Using a genomic cline framework, we demonstrate that the sex-linked and mito-nuclear incompatibilities isolating the homoploid hybrid Italian sparrow at its two geographically separated hybrid-parent boundaries represent a subset of those contributing to reproductive isolation between its parent species, house and Spanish sparrows. Should such a sorting mechanism prove to be pervasive, the circumstances promoting homoploid hybrid speciation may be broader than currently thought, and indeed there may be many cryptic hybrid taxa separated from their parent species by sorted, inherited incompatibilities

Major population splits coincide with episodes of rapid climate change in a forest-dependent bird

Climate change influences population demography by altering patterns of gene flow and reproductive isolation. Direct mutation rates offer the possibility for accurate dating on the within-species level but are currently only available for a handful of vertebrate species. Here, we use the first directly estimated mutation rate in birds to study the evolutionary history of pied flycatchers (Ficedula hypoleuca). Using a combination of demographic inference and species distribution modelling, we show that all major population splits in this forest-dependent system occurred during periods of increased climate instability and rapid global temperature change. We show that the divergent Spanish subspecies originated during the Eemian-Weichselian transition 115-104 thousand years ago (kya), and not during the last glacial maximum (26.5-19 kya), as previously suggested. The magnitude and rates of climate change during the glacial-interglacial transitions that preceded population splits in pied flycatchers were similar to, or exceeded, those predicted to occur in the course of the current, human-induced climate crisis. As such, our results provide a timely reminder of the strong impact that episodes of climate instability and rapid temperature changes can have on species' evolutionary trajectories, with important implications for the natural world in the Anthropocene.Peer reviewe

Simulation codes

The codes to run the simulation described in the paper. It is written in C. A makefile and a readme file are included

Sex chromosome evolution and speciation in Ficedula flycatchers.

Speciation is the combination of evolutionary processes that leads to the reproductive isolation of different populations. We investigate the significance of sex-chromosome evolution on the development of post- and prezygotic isolation in two naturally hybridizing Ficedula flycatcher species. Applying a tag-array-based mini-sequencing assay to genotype single nucleotide polymorphisms (SNPs) and interspecific substitutions, we demonstrate rather extensive hybridization and backcrossing in sympatry. However, gene flow across the partial postzygotic barrier (introgression) is almost exclusively restricted to autosomal loci, suggesting strong selection against introgression of sex-linked genes. In addition to this partial postzygotic barrier, character displacement of male plumage characteristics has previously been shown to reinforce prezygotic isolation in these birds. We show that male plumage traits involved in reinforcing prezygotic isolation are sex linked. These results suggest a major role of sex-chromosome evolution in mediating post- and prezygotic barriers to gene flow and point to a causal link in the development of the two forms of reproductive isolation

Beak and skull shapes of human commensal and non-commensal house sparrows Passer domesticus

Background: the granivorous house sparrow Passer domesticus is thought to have developed its commensal relationship with humans with the rise of agriculture in the Middle East some 10,000 years ago, and to have expanded with the spread of agriculture in Eurasia during the last few thousand years. One subspecies, P. d. bactrianus, residing in Central Asia, has apparently maintained the ancestral ecology, however. This subspecies is not associated with human settlements; it is migratory and lives in natural grass- and wetland habitats feeding on wild grass seeds. It is well documented that the agricultural revolution was associated with an increase in grain size and changes in seed structure in cultivated cereals, the preferred food source of commensal house sparrow. Accordingly, we hypothesize that correlated changes may have occurred in beak and skull morphology as adaptive responses to the change in diet. Here, we test this hypothesis by comparing the skull shapes of 101 house sparrows from Iran, belonging to five different subspecies, including the non-commensal P. d. bactrianus, using geometric morphometrics. - Results: the various commensal house sparrow subspecies share subtle but consistent skeletal features that differ significantly from those of the non-commensal P. d. bactrianus. Although there is a marked overall size allometry in the data set, the shape difference between the ecologically differentiated sparrows cannot be explained by differences in size alone. Relative to the size allometry commensal house sparrows exhibit a skull shape consistent with accelerated development (heterochrony), resulting in a more robust facial cranium and a larger, more pointed beak. - Conclusion: the difference in skull shape and robustness of the beak between commensal and non-commensal house sparrows is consistent with adaptations to process the larger and rachis encapsulated seeds of domesticated cereals among human associated populations