Elizabeth S. C. Scordato

Contributions of natural and sexual selection to the evolution of premating reproductive isolation: a research agenda.

Speciation by divergent natural selection is well supported. However, the role of sexual selection in speciation is less well understood due to disagreement about whether sexual selection is a mechanism of evolution separate from natural selection, as well as confusion about various models and tests of sexual selection. Here, we outline how sexual selection and natural selection are different mechanisms of evolutionary change, and suggest that this distinction is critical when analyzing the role of sexual selection in speciation. Furthermore, we clarify models of sexual selection with respect to their interaction with ecology and natural selection. In doing so, we outline a research agenda for testing hypotheses about the relative significance of divergent sexual and natural selection in the evolution of reproductive isolation.

Genomic divergence in a ring species complex

Ring species provide particularly clear demonstrations of how one species can gradually evolve into two, but are rare in nature. In the greenish warbler (Phylloscopus trochiloides) species complex, a ring of populations wraps around Tibet. Two reproductively isolated forms co-exist in central Siberia, with a gradient of genetic and phenotypic characteristics through the southern chain of populations connecting them. Previous genetic evidence has proven inconclusive, however, regarding whether species divergence took place in the face of continuous gene flow and whether hybridization between the terminal forms of the ring ever occurred. Here we use genome-wide analyses to show that, although spatial patterns of genetic variation are currently mostly as expected of a ring species, historical breaks in gene flow have existed at more than one location around the ring, and the two Siberian forms have occasionally interbred. Substantial periods of geographical isolation occurred not only in the north but also in the western Himalayas, where there is now an extensive hybrid zone between genetically divergent forms. Limited asymmetric introgression has occurred directly between the Siberian forms, although it has not caused a blending of those forms, suggesting selection against introgressed genes in the novel genetic background. Levels of reproductive isolation and genetic introgression are consistent with levels of phenotypic divergence around the ring, with phenotypic similarity and extensive interbreeding across the southwestern contact zone and strong phenotypic divergence and nearly complete reproductive isolation across the northern contact zone. These results cast doubt on the hypothesis that the greenish warbler should be viewed as a rare example of speciation by distance, but demonstrate that the greenish warbler displays a continuum from slightly divergent neighbouring populations to almost fully reproductively isolated species.

Genomic approaches to understanding population divergence and speciation in birds

ABSTRACT The widespread application of high-throughput sequencing in studying evolutionary processes and patterns of diversification has led to many important discoveries. However, the barriers to utilizing these technologies and interpreting the resulting data can be daunting for first-time users. We provide an overview and a brief primer of relevant methods (e.g., whole-genome sequencing, reduced-representation sequencing, sequence-capture methods, and RNA sequencing), as well as important steps in the analysis pipelines (e.g., loci clustering, variant calling, whole-genome and transcriptome assembly). We also review a number of applications in which researchers have used these technologies to address questions related to avian systems. We highlight how genomic tools are advancing research by discussing their contributions to 3 important facets of avian evolutionary history. We focus on (1) general inferences about biogeography and biogeographic history, (2) patterns of gene flow and isolation upon secondary contact and hybridization, and (3) quantifying levels of genomic divergence between closely related taxa. We find that in many cases, high-throughput sequencing data confirms previous work from traditional molecular markers, although there are examples in which genome-wide genetic markers provide a different biological interpretation. We also discuss how these new data allow researchers to address entirely novel questions, and conclude by outlining a number of intellectual and methodological challenges as the genomics era moves forward.

The Role of Ecology in Speciation by Sexual Selection: A Systematic Empirical Review

Theoretical and empirical research indicates that sexual selection interacts with the ecological context in which mate choice occurs, suggesting that sexual and natural selection act together during the evolution of premating reproductive isolation. However, the relative importance of natural and sexual selection to speciation remains poorly understood. Here, we applied a recent conceptual framework for examining interactions between mate choice divergence and ecological context to a review of the empirical literature on speciation by sexual selection. This framework defines two types of interactions between mate choice and ecology: internal interactions, wherein natural and sexual selection jointly influence divergence in sexual signal traits and preferences, and external interactions, wherein sexual selection alone acts on traits and preferences but ecological context shapes the transmission efficacy of sexual signals. The objectives of this synthesis were 3-fold: to summarize the traits, ecological factors, taxa, and geographic contexts involved in studies of mate choice divergence; to analyze patterns of association between these variables; and to identify the most common types of interactions between mate choice and ecological factors. Our analysis revealed that certain traits are consistently associated with certain ecological factors. Moreover, among studies that examined a divergent sexually selected trait and an ecological factor, internal interactions were more common than external interactions. Trait–preference associations may thus frequently be subject to both sexual and natural selection in cases of divergent mate choice. Our results highlight the importance of interactions between sexual selection and ecology in mate choice divergence and suggest areas for future research. Subject areas: Reproductive strategies and kinship analysisTheoretical and empirical research indicates that sexual selection interacts with the ecological context in which mate choice occurs, suggesting that sexual and natural selection act together during the evolution of premating reproductive isolation. However, the relative importance of natural and sexual selection to speciation remains poorly understood. Here, we applied a recent conceptual framework for examining interactions between mate choice divergence and ecological context to a review of the empirical literature on speciation by sexual selection. This framework defines two types of interactions between mate choice and ecology: internal interactions, wherein natural and sexual selection jointly influence divergence in sexual signal traits and preferences, and external interactions, wherein sexual selection alone acts on traits and preferences but ecological context shapes the transmission efficacy of sexual signals. The objectives of this synthesis were 3-fold: to summarize the traits, ecological factors, taxa, and geographic contexts involved in studies of mate choice divergence; to analyze patterns of association between these variables; and to identify the most common types of interactions between mate choice and ecological factors. Our analysis revealed that certain traits are consistently associated with certain ecological factors. Moreover, among studies that examined a divergent sexually selected trait and an ecological factor, internal interactions were more common than external interactions. Trait-preference associations may thus frequently be subject to both sexual and natural selection in cases of divergent mate choice. Our results highlight the importance of interactions between sexual selection and ecology in mate choice divergence and suggest areas for future research.

Prevalence and beta diversity in avian malaria communities: host species is a better predictor than geography

Patterns of diversity and turnover in macroorganism communities can often be predicted from differences in habitat, phylogenetic relationships among species and the geographical scale of comparisons. In this study, we asked whether these factors also predict diversity and turnover in parasite communities. We studied communities of avian malaria in two sympatric, ecologically similar, congeneric host species at three different sites. We asked whether parasite prevalence and community structure varied with host population, host phylogeography or geographical distance. We used PCR to screen birds for infections and then used Bayesian methods to determine phylogenetic relationships among malaria strains. Metrics of both community and phylogenetic beta diversity were used to examine patterns of malaria strain turnover between host populations, and partial Mantel tests were used determine the correlation between malaria beta diversity and geographical distance. Finally, we developed microsatellite markers to describe the genetic structure of host populations and assess the relationship between host phylogeography and parasite beta diversity. We found that different genera of malaria parasites infect the two hosts at different rates. Within hosts, parasite communities in one population were phylogenetically clustered, but there was otherwise no correlation between metrics of parasite beta diversity and geographical or genetic distance between host populations. Patterns of parasite turnover among host populations are consistent with malaria transmission occurring in the winter rather than on the breeding grounds. Our results indicate greater turnover in parasite communities between different hosts than between different study sites. Differences in host species, as well as transmission location and vector ecology, seem to be more important in structuring malaria communities than the distance-decay relationships frequently found in macroorganisms. Determining the factors affecting parasite community diversity and turnover has wide-ranging implications for understanding the selective pressures shaping host ecology and ecosystem structure. This study shows that metrics of community and phylogenetic beta diversity can be useful tools for disentangling the ecological and evolutionary processes that underlie geographical variation in parasite communities.

Cross-generational effects of climate change on expression of a sexually selected trait.

Sexually selected traits and early breeding are often correlated with quality in birds: individuals that breed earlier in the season have more elaborate traits and raise more surviving offspring [1, 2]. As global climate warms, breeding date for many temperate birds is advancing [3, 4], but we lack corresponding information on climate-induced variation in sexual selection. Here, we investigated influences of climate on a sexually selected plumage trait in a Himalayan warbler (Phylloscopus humei). We found that when spring is warm, birds breed early. Subsequent to an early-breeding year, adults express relatively large sexually selected traits and rear offspring that also develop large traits. The positive effects of early breeding, plus the across-year correlation between parent and offspring cohorts, predict that warmer climates should lead to increases in trait size. However, trait size has not increased over the past 25 years, even though mean breeding date has advanced. We show that whereas warm springs have positive effects on trait size, warm summers have negative effects due to increased feather wear. Apparent stasis in the size of a sexually selected trait thus masks large, conflicting influences of climate change. Continued climate warming has the potential to affect the honesty of sexual signals, as trait expression and condition become increasingly disassociated.

Genome-wide differentiation in closely related populations: the roles of selection and geographic isolation.

Population divergence in geographic isolation is due to a combination of factors. Natural and sexual selection may be important in shaping patterns of population differentiation, a pattern referred to as ‘isolation by adaptation’ (IBA). IBA can be complementary to the well‐known pattern of ‘isolation by distance’ (IBD), in which the divergence of closely related populations (via any evolutionary process) is associated with geographic isolation. The barn swallow Hirundo rustica complex comprises six closely related subspecies, where divergent sexual selection is associated with phenotypic differentiation among allopatric populations. To investigate the relative contributions of selection and geographic distance to genome‐wide differentiation, we compared genotypic and phenotypic variation from 350 barn swallows sampled across eight populations (28 pairwise comparisons) from four different subspecies. We report a draft whole‐genome sequence for H. rustica, to which we aligned a set of 9493 single nucleotide polymorphisms (SNPs). Using statistical approaches to control for spatial autocorrelation of phenotypic variables and geographic distance, we find that divergence in traits related to migratory behaviour and sexual signalling, as well as geographic distance, together explain over 70% of genome‐wide divergence among populations. Controlling for IBD, we find 42% of genomewide divergence is attributable to IBA through pairwise differences in traits related to migratory behaviour and sexual signalling alone. By (i) combining these results with prior studies of how selection shapes morphological differentiation and (ii) accounting for spatial autocorrelation, we infer that morphological adaptation plays a large role in shaping population‐level differentiation in this group of closely related populations.

Mechanisms of Assortative Mating in Speciation with Gene Flow: Connecting Theory and Empirical Research

The large body of theory on speciation with gene flow has brought to light fundamental differences in the effects of two types of mating rules on speciation: preference/trait rules, in which divergence in both (female) preferences and (male) mating traits is necessary for assortment, and matching rules, in which individuals mate with like individuals on the basis of the presence of traits or alleles that they have in common. These rules can emerge from a variety of behavioral or other mechanisms in ways that are not always obvious. We discuss the theoretical properties of both types of rules and explain why speciation is generally thought to be more likely under matching rather than preference/trait rules. We furthermore discuss whether specific assortative mating mechanisms fall under a preference/trait or matching rule, present empirical evidence for these mechanisms, and propose empirical tests that could distinguish between them. The synthesis of the theoretical literature on these assortative mating rules with empirical studies of the mechanisms by which they act can provide important insights into the occurrence of speciation with gene flow. Finally, by providing a clear framework we hope to inspire greater alignment in the ways that both theoreticians and empiricists study mating rules and how these rules affect speciation through maintaining or eroding barriers to gene flow among closely related species or populations.

On the role of male competition in speciation: a review and research agenda

Little attention has been given to how males competing for mates can facilitate the evolution and persistence of new species. We expand the current framework for how new species evolve (speciation) to include male competition, drawing on recent research to show how male competition contributes to divergence between co-occurring or spatially isolated populations. We also identify interactions with female mate choice and environmental variation, and formulate a research program that will move this field forward.

Geographical variation in male territory defence strategies in an avian ring species

Interactions between sexual selection and ecology can drive phenotypic divergence between populations. Geographical variation in female preferences has been linked to ecology in several studies, but much less is known about patterns of geographical variation in male competition. I asked whether male aggressive territorial behaviour varied among three breeding populations of a ring species, the greenish warbler, Phylloscopus trochiloides. I measured aggressive response to playbacks of conspecific song at multiple time points to determine how territorial behaviour varied throughout the breeding season both within and between populations. Differences in the abundance and timing of resources necessary for raising offspring can shape male competitive strategies, and competition may consequently vary as a function of resource availability. I therefore combined assays of temporal variation in aggressive behaviour with season-long measures of food abundance, population density and parental provisioning rates. I found that the populations differed in intensity of aggressive response, the seasonal pattern of territoriality and the traits used in territorial responses. Overall intensity of aggression was lowest but most prolonged in the population with the lowest food abundance and highest population density, and males responded to playback primarily by singing. By contrast, birds in the two populations that experienced high food abundance and low population density exhibited a burst of aggressive display behaviour only when females were fertile. The results suggest that territorial strategies vary geographically and respond to limited resources, switching in function from season-long food defence where food is scarce to mate guarding where mates are scarce. Interactions between sexual selection and ecology across large geographical scales may ultimately lead to population divergence. The geographical variation in territorial behaviour observed in the greenish warbler implies that male competition may be an important diversifying force in this system.