Phylogeny and historical biogeography of the swallow family (Hirundinidae) inferred from comparisons of thousands of UCE loci.

Swallows (Hirundinidae) are a globally distributed family of passerine birds that exhibit remarkable similarity in body shape but tremendous variation in plumage, sociality, nesting behavior, and migratory strategies. As a result, swallow species have become models for empirical behavioral ecology and evolutionary studies, and variation across the Hirundinidae presents an excellent opportunity for comparative analyses of trait evolution. Exploiting this potential requires a comprehensive and well-resolved phylogenetic tree of the family. To address this need, we estimated swallow phylogeny using genetic data from thousands of ultraconserved element (UCE) loci sampled from nearly all recognized swallow species. Maximum likelihood, coalescent-based, and Bayesian approaches yielded a well-resolved phylogenetic tree to the generic level, with minor disagreement among inferences at the species level, which likely reflect ongoing population genetic processes. The UCE data were particularly useful in helping to resolve deep nodes, which previously confounded phylogenetic reconstruction efforts. Divergence time estimates from the improved swallow tree support a Miocene origin of the family, roughly 13 million years ago, with subsequent diversification of major groups in the late Miocene and Pliocene. Our estimates of historical biogeography support the hypothesis that swallows originated in the Afrotropics and have subsequently expanded across the globe, with major in situ diversification in Africa and a secondary major radiation following colonization of the Neotropics. Initial examination of nesting and sociality indicates that the origin of mud nesting - a relatively rare nest construction phenotype in birds - was a major innovation coincident with the origin of a clade giving rise to over 40% of extant swallow diversity. In contrast, transitions between social and solitary nesting appear less important for explaining patterns of diversification among swallows.

Colonial breeding impacts potentially fitness-relevant cognitive processes in barn swallows.

Many animals breed colonially, often in dense clusters, representing a complex social environment with cognitive demands that could ultimately impact individual fitness. However, the effects of social breeding on the evolution of cognitive processes remain largely unknown. We tested the hypothesis that facultative colonial breeding influences attention and decision-making. Barn swallows (Hirundo rustica) breed in solitary pairs or in a range of colony sizes, up to dozens of pairs. We tested for selective attention to social information with playbacks of conspecific alarm calls and for decision-making with simulated predator intrusions, across a range of colony sizes from 1 to 33 pairs. We also evaluated the adaptive value of both processes by measuring seasonal reproductive success. Swallows breeding in larger colonies were more selective in their attention to social information. Birds breeding in larger colonies were also less risk averse, deciding to return more quickly to their nests after a predator approach paradigm. Finally, birds that showed higher selective attention hatched more eggs and birds that returned to their nests more quickly after a predator intrusion had more nestlings. Although we cannot fully attribute these fitness outcomes to the cognitive measures considered in this study, our results suggest that social breeding plays a role in adaptively shaping both the acquisition of social information and decision-making.

Estimating phylogenies from genomes: A beginners review of commonly used genomic data in vertebrate phylogenomics.

Despite the increasing feasibility of sequencing whole genomes from diverse taxa, a persistent problem in phylogenomics is the selection of appropriate genetic markers or loci for a given taxonomic group or research question. In this review, we aim to streamline the decision-making process when selecting specific markers to use in phylogenomic studies by introducing commonly used types of genomic markers, their evolutionary characteristics, and their associated uses in phylogenomics. Specifically, we review the utilities of ultraconserved elements (including flanking regions), anchored hybrid enrichment loci, conserved nonexonic elements, untranslated regions, introns, exons, mitochondrial DNA, single nucleotide polymorphisms, and anonymous regions (nonspecific regions that are evenly or randomly distributed across the genome). These various genomic elements and regions differ in their substitution rates, likelihood of neutrality or of being strongly linked to loci under selection, and mode of inheritance, each of which are important considerations in phylogenomic reconstruction. These features may give each type of marker important advantages and disadvantages depending on the biological question, number of taxa sampled, evolutionary timescale, cost effectiveness, and analytical methods used. We provide a concise outline as a resource to efficiently consider key aspects of each type of genetic marker. There are many factors to consider when designing phylogenomic studies, and this review may serve as a primer when weighing options between multiple potential phylogenomic markers.

A biologist's guide to model selection and causal inference.

A goal of many research programmes in biology is to extract meaningful insights from large, complex datasets. Researchers in ecology, evolution and behavior (EEB) often grapple with long-term, observational datasets from which they construct models to test causal hypotheses about biological processes. Similarly, epidemiologists analyse large, complex observational datasets to understand the distribution and determinants of human health. A key difference in the analytical workflows for these two distinct areas of biology is the delineation of data analysis tasks and explicit use of causal directed acyclic graphs (DAGs), widely adopted by epidemiologists. Here, we review the most recent causal inference literature and describe an analytical workflow that has direct applications for EEB. We start this commentary by defining four distinct analytical tasks (description, prediction, association, causal inference). The remainder of the text is dedicated to causal inference, specifically focusing on the use of DAGs to inform the modelling strategy. Given the increasing interest in causal inference and misperceptions regarding this task, we seek to facilitate an exchange of ideas between disciplinary silos and provide an analytical framework that is particularly relevant for making causal inference from observational data.

Sex-linked genetic diversity and differentiation in a globally distributed avian species complex.

Sex chromosomes often bear distinct patterns of genetic variation due to unique patterns of inheritance and demography. The processes of mutation, recombination, genetic drift and selection also influence rates of evolution on sex chromosomes differently than autosomes. Measuring such differences provides information about how these processes shape genomic variation and their roles in the origin of species. To test hypotheses and predictions about patterns of autosomal and sex-linked genomic diversity and differentiation, we measured population genetic statistics within and between populations and subspecies of the barn swallow (Hirundo rustica) and performed explicit comparisons between autosomal and Z-linked genomic regions. We first tested for evidence of low Z-linked genetic diversity and high Z-linked population differentiation relative to autosomes, then for evidence that the Z chromosome bears greater ancestry information due to faster lineage sorting. Finally, we investigated geographical clines across hybrid zones for evidence that the Z chromosome is resistant to introgression due to selection against hybrids. We found evidence that the barn swallow mating system, demographic history and linked selection each contribute to low Z-linked diversity and high Z-linked differentiation. While incomplete lineage sorting is rampant across the genome, our results indicate faster sorting of ancestral polymorphism on the Z. Finally, hybrid zone analyses indicate barriers to introgression on the Z chromosome, suggesting that sex-linked traits are important in reproductive isolation, especially in migratory divide regions. Our study highlights how selection, gene flow and demography shape sex-linked genetic diversity and underlines the relevance of the Z chromosome in speciation.

Migratory divides coincide with reproductive barriers across replicated avian hybrid zones above the Tibetan Plateau.

Migratory divides are proposed to be catalysts for speciation across a diversity of taxa. However, it is difficult to test the relative contributions of migratory behaviour vs. other divergent traits to reproductive isolation. Comparing hybrid zones with and without migratory divides offers a rare opportunity to directly examine the contribution of divergent migratory behaviour to reproductive barriers. We show that across replicate sampling transects of two pairs of barn swallow (Hirundo rustica) subspecies, strong reproductive isolation coincided with a migratory divide spanning 20 degrees of latitude. A third subspecies pair exhibited no evidence for a migratory divide and hybridised extensively. Within migratory divides, overwintering habitats were associated with assortative mating, implicating a central contribution of divergent migratory behaviour to reproductive barriers. The remarkable geographic coincidence between migratory divides and genetic breaks supports a long-standing hypothesis that the Tibetan Plateau is a substantial barrier contributing to the diversity of Siberian avifauna.

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.

Demographic inference in barn swallows using whole-genome data shows signal for bottleneck and subspecies differentiation during the Holocene.

Accounting for historical demographic features is vital for many types of evolutionary inferences, including the estimation of divergence times between closely related populations. In barn swallow, Hirundo rustica, inferring historical population sizes and subspecies divergence times can shed light on the recent co-evolution of this species with humans. Pairwise sequentially Markovian coalescent uncovered population growth beginning on the order of one million years ago-which may reflect the radiation of the broader Hirundo genus-and a more recent population decline. Additionally, we used approximate Bayesian computation to evaluate hypotheses about recent timescale barn swallow demography, including population growth due to human commensalism, and a potential founder event associated with the onset of nesting on human structures. We found signal for a bottleneck event approximately 7,700 years ago, near the time that humans began building substantial structures, although there was considerable uncertainty associated with this estimate. Subspecies differentiation and subsequent growth occurred after the bottleneck in the best-supported model, an order of magnitude more recently than previous estimates in this system. We also compared results obtained from whole-genome sequencing versus reduced representation sequencing, finding many similar results despite substantial allelic dropout in the reduced representation data, which may have affected estimates of some parameters. This study presents the first genetic evidence of a potential barn swallow founder effect and subspecies divergence coinciding with the Holocene, which is an important step in analysing the biogeographical history of a well-known human commensal species.

Theory Meets Empiry: A Citation Network Analysis.

According to a recent survey, ecologists and evolutionary biologists feel that theoretical and empirical research should coexist in a tight feedback loop but believe that the two domains actually interact very little. We evaluate this perception using a citation network analysis for two data sets, representing the literature on sexual selection and speciation. Overall, 54%-60% of citations come from a paper's own category, whereas 17%-23% are citations across categories. These cross-citations tend to focus on highly cited papers, and we observe a positive correlation between the numbers of citations a study receives within and across categories. We find evidence that reviews can function as integrators between the two literatures, argue that theoretical models are analogous to specific empirical study systems, and complement our analyses by studying a cocitation network. We conclude that theoretical and empirical research are more tightly connected than generally thought but that avenues exist to further increase this integration.

Genomic variation across two barn swallow hybrid zones reveals traits associated with divergence in sympatry and allopatry.

Hybrid zones are geographic regions where isolating barriers between divergent populations are challenged by admixture. Identifying factors that facilitate or inhibit hybridization in sympatry can illuminate the processes that maintain those reproductive barriers. We analysed patterns of hybridization and phenotypic variation across two newly discovered hybrid zones between three subspecies of barn swallow (Hirundo rustica). These subspecies differ in ventral coloration and wing length, traits that are targets of sexual and natural selection, respectively, and are associated with genome-wide differentiation in allopatry. We tested the hypothesis that the degree of divergence in these traits is associated with the extent of hybridization in secondary contact. We applied measures of population structure based on >23,000 SNPs to confirm that named subspecies correspond to distinct genomic clusters, and assessed coincidence between geographic clines for ancestry and phenotype. Although gene flow was ongoing across both hybrid zones and pairwise FST between subspecies was extremely low, we found striking differences in the extent of hybridization. In the more phenotypically differentiated subspecies pair, clines for ancestry, wing length and ventral coloration were steep and coincident, suggestive of strong isolation and, potentially, selection associated with phenotype. In the less phenotypically differentiated pair, gene flow and phenotypic variation occurred over a wide geographic span, indicative of weaker isolation. Traits associated with genome-wide differentiation in allopatry may thus also contribute to isolation in sympatry. We discuss potentially important additional roles for evolutionary history and ecology in shaping variation in the extent hybridization between closely related pairs of subspecies.

Effects of assortative mate choice on the genomic and morphological structure of a hybrid zone between two bird subspecies.

Phenotypic differentiation plays an important role in the formation and maintenance of reproductive barriers. In some cases, variation in a few key aspects of phenotype can promote and maintain divergence; hence, the identification of these traits and their associations with patterns of genomic divergence is crucial for understanding the patterns and processes of population differentiation. We studied hybridization between the alba and personata subspecies of the white wagtail (Motacilla alba), and quantified divergence and introgression of multiple morphological traits and 19,437 SNP loci on a 3,000 km transect. Our goal was to identify traits that may contribute to reproductive barriers and to assess how variation in these traits corresponds to patterns of genome-wide divergence. Variation in only one trait-head plumage patterning-was consistent with reproductive isolation. Transitions in head plumage were steep and occurred over otherwise morphologically and genetically homogeneous populations, whereas cline centres for other traits and genomic ancestry were displaced over 100 km from the head cline. Field observational data show that social pairs mated assortatively by head plumage, suggesting that these phenotypes are maintained by divergent mating preferences. In contrast, variation in all other traits and genetic markers could be explained by neutral diffusion, although weak ecological selection cannot be ruled out. Our results emphasize that assortative mating may maintain phenotypic differences independent of other processes shaping genome-wide variation, consistent with other recent findings that raise questions about the relative importance of mate choice, ecological selection and selectively neutral processes for divergent evolution.

An experimental test of the effect of brood size on glucocorticoid responses, parental investment, and offspring phenotype.

Because elevated glucocorticoid levels can impair reproduction, populations or species that engage in particularly valuable reproductive attempts may down-regulate the glucocorticoid stress response during reproduction (the brood value hypothesis). It is not clear, however, whether individuals rapidly modulate glucocorticoid responses based on shifting cues about the likelihood of reproductive success. By manipulating brood size to create broods that differed in potential value, we tested whether female barn swallows (Hirundo rustica) rapidly modulated the glucocorticoid stress response to promote investment in high-value broods, and whether nestling phenotype was influenced by treatment. Within-individual changes in female corticosterone, body mass, and measures of oxidative stress were unrelated to brood size treatment. Standard offspring provisioning rate did not differ across treatments; however, in the presence of a model predator, females raising enlarged broods maintained higher offspring feeding rates relative to control broods. Brood size did influence nestling phenotype. Nestlings from enlarged broods had lower body mass and higher baseline corticosterone than those from reduced broods. Finally, in adult females both baseline and stress-induced corticosterone were individually repeatable. Thus, while under moderately challenging environmental conditions brood size manipulations had context-dependent effects on parental investment, and influenced nestling phenotype, maternal glucocorticoid levels were not modulated based on brood value but were individually consistent features of phenotype during breeding.

Piecing together female extra-pair mate choice: females really do prefer more ornamented males.

Evolutionary biologists have long been fascinated by extravagant male traits that abound across the animal kingdom and yet convey no apparent benefits to survival. From isopods to elephants, from armaments to ornaments, researchers have spent decades studying male-male competition and female mate choice in an effort to understand the significance of these secondary sexual characteristics. Among socially monogamous species, a frequently proposed explanation for the existence of male ornaments is that they are indicators of male genetic quality subject to female extra-pair mate choice. However, despite over two decades of extensive research into extra-pair paternity (EPP), the evidence that females actually choose more ornamented extra-pair sires is surprisingly scant. Consequently, whether EPP and female choice have contributed to the evolution of male ornaments in socially monogamous species, and what fitness benefits (if any) they signal to females, remains unclear. Progress in this field has been hampered by the challenge of dissociating clear female choice for ornamentation from confounding factors. In this issue of Molecular Ecology, Whittingham & Dunn (2016) use an experimental approach in a bird species with very high rates of EPP to tease apart these correlative effects. In doing so, they demonstrate clearly that male ornamentation is subject to female extra-pair mate choice. Their findings further suggest that EPP can be adaptive for females, and represent an important step forward in validating the role of EPP as an evolutionary driver of ornamental elaboration in socially monogamous species.

Stress response, gut microbial diversity and sexual signals correlate with social interactions.

Theory predicts that social interactions are dynamically linked to phenotype. Yet because social interactions are difficult to quantify, little is known about the precise details on how interactivity is linked to phenotype. Here, we deployed proximity loggers on North American barn swallows (Hirundo rustica erythrogaster) to examine intercorrelations among social interactions, morphology and features of the phenotype that are sensitive to the social context: stress-induced corticosterone (CORT) and gut microbial diversity. We analysed relationships at two spatial scales of interaction: (i) body contact and (ii) social interactions occurring between 0.1 and 5 m. Network analysis revealed that relationships between social interactions, morphology, CORT and gut microbial diversity varied depending on the sexes of the individuals interacting and the spatial scale of interaction proximity. We found evidence that body contact interactions were related to diversity of socially transmitted microbes and that looser social interactions were related to signalling traits and CORT.

Multimodal signalling in the North American barn swallow: a phenotype network approach.

Complex signals, involving multiple components within and across modalities, are common in animal communication. However, decomposing complex signals into traits and their interactions remains a fundamental challenge for studies of phenotype evolution. We apply a novel phenotype network approach for studying complex signal evolution in the North American barn swallow (Hirundo rustica erythrogaster). We integrate model testing with correlation-based phenotype networks to infer the contributions of female mate choice and male-male competition to the evolution of barn swallow communication. Overall, the best predictors of mate choice were distinct from those for competition, while moderate functional overlap suggests males and females use some of the same traits to assess potential mates and rivals. We interpret model results in the context of a network of traits, and suggest this approach allows researchers a more nuanced view of trait clustering patterns that informs new hypotheses about the evolution of communication systems.

An experimental analysis of the heritability of variation in glucocorticoid concentrations in a wild avian population.

Glucocorticoid hormones (CORT) are predicted to promote adaptation to variable environments, yet little is known about the potential for CORT secretion patterns to respond to selection in free-living populations. We assessed the heritable variation underlying differences in hormonal phenotypes using a cross-foster experimental design with nestling North American barn swallows (Hirundo rustica erythrogaster). Using a bivariate animal model, we partitioned variance in baseline and stress-induced CORT concentrations into their additive genetic and rearing environment components and estimated their genetic correlation. Both baseline and stress-induced CORT were heritable with heritability of 0.152 and 0.343, respectively. We found that the variation in baseline CORT was best explained by rearing environment, whereas the variation in stress-induced CORT was contributed to by a combination of genetic and environmental factors. Further, we did not detect a genetic correlation between these two hormonal traits. Although rearing environment appears to play an important role in the secretion of both types of CORT, our results suggest that stress-induced CORT levels are underlain by greater additive genetic variance compared with baseline CORT levels. Accordingly, we infer that the glucocorticoid response to stress has a greater potential for evolutionary change in response to selection compared with baseline glucocorticoid secretion patterns.

Environmental harshness is positively correlated with intraspecific divergence in mammals and birds.

Life on Earth is conspicuously more diverse in the tropics. Although this intriguing geographical pattern has been linked to many biotic and abiotic factors, their relative importance and potential interactions are still poorly understood. The way in which latitudinal changes in ecological conditions influence evolutionary processes is particularly controversial, as there is evidence for both a positive and a negative latitudinal gradient in speciation rates. Here, we identify and address some methodological issues (how patterns are analysed and how latitude is quantified) that could lead to such conflicting results. To address these issues, we assemble a comprehensive data set of the environmental correlates of latitude (including climate, net primary productivity and habitat heterogeneity) and combine it with biological, historical and molecular data to explore global patterns in recent divergence events (subspeciation). Surprisingly, we find that the harsher conditions that typify temperate habitats (lower primary productivity, decreased rainfall and more variable and unpredictable temperatures) are positively correlated with greater subspecies richness in terrestrial mammals and birds. Thus, our findings indicate that intraspecific divergence is greater in regions with lower biodiversity, a pattern that is robust to both sampling variation and latitudinal biases in taxonomic knowledge. We discuss possible causal mechanisms for the link between environmental harshness and subspecies richness (faster rates of evolution, greater likelihood of range discontinuities and more opportunities for divergence) and conclude that this pattern supports recent indications that latitudinal gradients of diversity are maintained by simultaneously higher potentials for both speciation and extinction in temperate than tropical regions.

Stress and success: individual differences in the glucocorticoid stress response predict behavior and reproductive success under high predation risk.

A fundamental element of how vertebrates respond to stressors is by rapidly elevating circulating glucocorticoid hormones. Individual variation in the magnitude of the glucocorticoid stress response has been linked with reproductive success and survival. But while the adaptive value of this response is believed to stem in part from changes in the expression of hormone-mediated behaviors, it is not clear how the behavior of stronger and weaker glucocorticoid responders differs during reproduction, or during exposure to ecologically relevant stressors. Here we report that in a population of barn swallows (Hirundo rustica erythrogaster) experiencing high rates of nest predation, circulating levels of corticosterone (the primary avian glucocorticoid) during exposure to a standardized stressor predict aspects of subsequent behavior and fitness. Individuals that mounted a stronger corticosterone stress response during the early reproductive period did not differ in clutch size, but fledged fewer offspring. Parents with higher stress-induced corticosterone during the early reproductive period later provisioned their nestlings at lower rates. Additionally, in the presence of a model predator stress-induced corticosterone was positively associated with the latency to return to the nest, but only among birds that were observed to return. Model comparisons revealed that stress-induced hormones were better predictors of the behavioral and fitness effects of exposure to transient, ecologically relevant stressors than baseline corticosterone. These findings are consistent with functional links between individual variation in the hormonal and behavioral response to stressors. If such links occur, then selection on the heritable components of the corticosterone stress response could promote adaptation to novel environments or predation regimes.

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.

Speciation.

What drives the emergence of new species has fascinated biologists since Darwin. Reproductive barriers to gene flow are a key step in the formation of species, and recent advances have shed new light on how these are established. Genetic, genomic, and comparative techniques, together with improved theoretical frameworks, are increasing our understanding of the underlying mechanisms. They are also helping us forecast speciation and reveal the impact of human activity.