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.

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.

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.

Selection on multiple sexual signals in two Central and Eastern European populations of the barn swallow.

Variation in intensity and targets of sexual selection on multiple traits has been suggested to play a major role in promoting phenotypic differentiation between populations, although the divergence in selection may depend on year, local conditions or age. In this study, we quantified sexual selection for two putative sexual signals across two Central and East European barn swallow (Hirundo rustica rustica) populations from Czech Republic and Romania over multiple years. We then related these differences in selection to variation in sexual characters among barn swallow populations. Our results show that tail length and ventral coloration vary between populations, sexes, and age classes (first-time breeders vs. experienced birds). We found that selection on tail length was stronger in first-time breeders than in experienced birds and in males than in females in the Romanian population, while these differences between age groups and sexes were weak in Czech birds. We suggest that the populational difference in selection on tail length might be related to the differences in breeding conditions. Our results show that ventral coloration is darker (i.e., has lower brightness) in the Romanian than in the Czech population, and in experienced birds and males compared with first-time breeders and females, respectively. The sexual difference in ventral coloration may suggest sexual selection on this trait, which is supported by the significant directional selection of ventral coloration in first-time breeding males on laying date. However, after controlling for the confounding effect of wing length and tarsus length, the partial directional selection gradient on this trait turned nonsignificant, suggesting that the advantage of dark ventral coloration in early breeding birds is determined by the correlated traits of body size. These findings show that ventral coloration may be advantageous over the breeding season, but the underlying mechanism of this relationship is not clarified.

Dynamic changes in display architecture and function across environments revealed by a systems approach to animal communication.

Animal communication is often structurally complex and dynamic, with signaler and receiver behavior varying in response to multiple environmental factors. To date, studies assessing signal dynamics have mostly focused on the relationships between select signaling traits and receiver responses in a single environment. We use the wolf spider Schizocosa floridana to explore the relationships between courtship display form and function across two social contexts (female presence vs absence) and two light environments (light vs dark). We use traditional analytical methods to determine predictors of copulation success (i.e., signal function) and examine these predictors in a structural context by overlaying them on signal phenotype networks (Wilkins et al. 2015). This allows us to explore system design principles (degeneracy, redundancy, pluripotentiality), providing insight into hypotheses regarding complex signal evolution. We found that both social context and light environment affect courtship structure, although the predictors of mating success remain similar across light environments, suggesting system degeneracy. Contrastingly, the same display traits may serve different functions across social environments, suggesting pluripotentiality. Ultimately, our network approach uncovers a complexity in display structure and function that is missed by functional analyses alone, highlighting the importance of systems-based methodologies for understanding the dynamic nature of complex signals.

The maintenance of phenotypic divergence through sexual selection: An experimental study in barn swallows Hirundo rustica.

Previous studies have shown that sexual signals can rapidly diverge among closely related species. However, we lack experimental studies to demonstrate that differences in trait-associated reproductive performance maintain sexual trait differences between closely related populations, in support for a role of sexual selection in speciation. Populations of Northern Hemisphere distributed barn swallows Hirundo rustica are closely related, yet differ in two plumage-based traits: ventral color and length of the outermost tail feathers (streamers). Here we provide experimental evidence that manipulations of these traits result in different reproductive consequences in two subspecies of barn swallow: (H. r. erythrogaster in North America and H. r. transitiva in the East Mediterranean). Experimental results in Colorado, USA, demonstrate that males with (1) darkened ventral coloration and (2) shortened streamers gained paternity between two successive reproductive bouts. In contrast, exaggeration of both traits improved reproductive performance within H. r. transitiva in Israel: males with a combination treatment of darkened ventral coloration and elongated streamers gained paternity between two successive reproductive bouts. Collectively, these experimental results fill an important gap in our understanding for how divergent sexual selection maintains phenotype differentiation in closely related populations, an important aspect of the speciation process.

Evolutionary divergence in acoustic signals: causes and consequences.

Acoustic signals mediate mate choice, resource defense, and species recognition in a broad range of taxa. It has been proposed, therefore, that divergence in acoustic signals plays a key role in speciation. Nonetheless, the processes driving divergence of acoustic traits and their consequences in terms of speciation are poorly understood. A review of empirical and comparative studies reveals strong support for a role of sexual selection in acoustic divergence, but the possible concomitant influences of ecological context are rarely examined. We summarize a conceptual framework for testing the relative significance of both adaptive and neutral mechanisms leading to acoustic divergence, predictions for cases where these processes lead to speciation, and how their relative importance plays out over evolutionary time.

Positive carotenoid balance correlates with greater reproductive performance in a wild bird.

BACKGROUND: Carotenoids can confer somatic and reproductive benefits, but most evidence is from captive animal experimentation or single time-point sampling. Another perhaps more informative means by which to assess physiological contributions to animal performance is by tracking an individual's ability to increase or sustain carotenoids or other health-related molecules over time, as these are likely to be temporally variable. METHODOLOGY/PRINCIPAL FINDINGS: In a field study of North American barn swallows (Hirundo rustica erythrogaster), we analyzed within-individual changes in carotenoid concentrations by repeatedly sampling the carotenoid profiles of individuals over the course of the breeding season. Our results demonstrate that carotenoid concentrations of individuals are temporally dynamic and that season-long balance of these molecules, rather than single time-point samples, predict reproductive performance. This was true even when controlling for two important variables associated with reproductive outcomes: (1) timing of breeding and (2) sexually selected plumage coloration, which is itself positively correlated with and concomitantly changes with circulating carotenoid concentrations. CONCLUSIONS/SIGNIFICANCE: While reproduction itself is purported to impose health stress on organisms, these data suggest that free-ranging, high-quality individuals can mitigate such costs, by one or several genetic, environmental (diet), or physiological mechanisms. Moreover, the temporal variations in both health-linked physiological measures and morphological traits we uncover here merit further examination in other species, especially when goals include the estimation of signal information content or the costs of trait expression.