Kristen C. Ruegg

Not as the crow flies: a historical explanation for circuitous migration in Swainson's thrush (Catharus ustulatus)

Many migratory songbirds follow circuitous migratory routes instead of taking the shortest path between overwintering and breeding areas. Here, we study the migration patterns in Swainsons thrush (Catharus ustulatus), a neartic–neotropical migrant songbird, using molecular genetic approaches. This species is presently separated into genetically distinct coastal and continental populations that diverged during the Late Pleistocene (as indicated by molecular dating), yet appear to have retained ancestral patterns of migration. Low nucleotide diversity, a star–like haplotype phylogeny and unimodal mismatch distributions all support the hypothesis that both the coastal and the continental populations have undergone recent demographic expansions. Nearctic–neotropical banding and genetic data show nearly complete segregation of migratory routes and of overwintering locations: coastal populations migrate along the Pacific Coast to overwintering sites in Central America and Mexico, whereas continental populations migrate along an eastern route to overwintering sites in Panama and South America. Nearctic–neotropical banding data also show that continental birds north, northwest and east of this migratory divide fly thousands of miles east before turning south. We conclude that circuitous migration in the Swainsons thrush is an artefact of a Late Pleistocene range expansion.

COMBINING ISOTOPIC AND GENETIC MARKERS TO IDENTIFY BREEDING ORIGINS OF MIGRANT BIRDS

A quantitative method for linking reproductive and nonreproductive phases of migratory life cycles is fundamental to understanding the biology of migratory organisms. Here we combine genetic (mtDNA) and biochemical (stable isotope) information to examine seasonal movements in the Swainsons Thrush (Catharus ustulatus), a Neotropical migrant. We show that when these intrinsic markers are used in concert, they can predict the site-specific origin of thrushes with 76–80% accuracy. Genetic and isotope data needed for these classifications can be obtained from migratory organisms at any phase of the life cycle. We demonstrate how this classification analysis can be used to infer breeding origins of samples gathered during the nonreproductive phases of the life cycle. Based on these results, we argue that further integration of methodologies will refine the scale at which linkages between reproductive and nonreproductive phases of the life cycle can be quantified.

Divergence in mating signals correlates with ecological variation in the migratory songbird, Swainson's thrush ( Catharus ustulatus )

Song divergence among populations of passerine birds is recognized as a potentially important premating isolation mechanism and may represent the first step in speciation. Because song divergence may be influenced by an array of acoustic, ecological, and genetic factors, the study of its origin requires a multifaceted approach. Here we describe the relationship between acoustic, neutral genetic and ecological variation in five populations of the Swainsons thrush: two from coastal temperate rainforest habitat representing the ‘russet‐backed’ subspecies group, two from inland coniferous forest habitat representing the ‘olive‐backed’ subspecies group, and one mixed locality that resides within a contact zone between the two groups. Song in the five populations is analysed using a multivariate analysis of spectral and temporal measurements, population genetic structure is assessed using an analysis of five microsatellite loci and ecological differences between populations are quantified using an analysis of climatic parameters. Matrix correspondence tests are used to distinguish between the potential for drift and selection in driving song divergence. No significant correlation was found between acoustic and genetic distance suggesting that song divergence cannot be explained by drift alone. A significant correlation between ecological and acoustic distance after accounting for genetic distance, suggests a potential role for ecological selection on divergence in spectral and temporal components of Swainsons thrush song.

Mapping migration in a songbird using high-resolution genetic markers

Neotropic migratory birds are declining across the Western Hemisphere, but conservation efforts have been hampered by the inability to assess where migrants are most limited—the breeding grounds, migratory stopover sites or wintering areas. A major challenge has been the lack of an efficient, reliable and broadly applicable method for measuring the strength of migratory connections between populations across the annual cycle. Here, we show how high‐resolution genetic markers can be used to identify genetically distinct groups of a migratory bird, the Wilsons warbler (Cardellina pusilla), at fine enough spatial scales to facilitate assessing regional drivers of demographic trends. By screening 1626 samples using 96 highly divergent single nucleotide polymorphisms selected from a large pool of candidates (~450 000), we identify novel region‐specific migratory routes and timetables of migration along the Pacific Flyway. Our results illustrate that high‐resolution genetic markers are more reliable, precise and amenable to high throughput screening than previously described intrinsic marking techniques, making them broadly applicable to large‐scale monitoring and conservation of migratory organisms.

Novel statistical methods for integrating genetic and stable isotope data to infer individual-level migratory connectivity

Methods for determining patterns of migratory connectivity in animal ecology have historically been limited due to logistical challenges. Recent progress in studying migratory bird connectivity has been made using genetic and stable‐isotope markers to assign migratory individuals to their breeding grounds. Here, we present a novel Bayesian approach to jointly leverage genetic and isotopic markers and we test its utility on two migratory passerine bird species. Our approach represents a principled model‐based combination of genetic and isotope data from samples collected on the breeding grounds and is able to achieve levels of assignment accuracy that exceed those of either method alone. When applied at large scale the method can reveal specific migratory connectivity patterns. In Wilsons warblers (Wilsonia pusilla), we detect a subgroup of birds wintering in Baja that uniquely migrate preferentially from the coastal Pacific Northwest. Our approach is implemented in a way that is easily extended to accommodate additional sources of information (e.g. bi‐allelic markers, species distribution models, etc.) or adapted to other species or assignment problems.

Differences in timing of migration and response to sexual signalling drive asymmetric hybridization across a migratory divide

Ecological traits and sexual signals may both contribute to the process of ecological speciation. Here we investigate the roles of an ecological trait, seasonal migratory behaviour and a sexual trait, song, in restricting or directing gene flow across a migratory divide in the Swainson’s thrush (Catharus ustulatus). We show that short‐distance migratory ecotypes wintering in Central America arrive earlier at the breeding grounds than long‐distance migratory ecotypes wintering primarily in South America, providing the potential for some premating isolation. Playback experiments suggest that early‐ and late‐arriving forms recognize each other as competitors, but that the early‐arriving form responds more aggressively to a broader spectrum of stimuli. Genetic analysis suggests that hybridization occurs more often between males of the early‐arriving ecotype and females of the late‐arriving ecotype. Together our results suggest that differences in arrival times may reduce the temporal coincidence of mate choice, but asymmetry in response to heterotypic song may hinder complete divergence. These data provide further insight into the roles of ecological traits and sexual signals during the incipient stages of speciation.

Genomic islands of divergence or opportunities for introgression

In animals, introgression between species is often perceived as the breakdown of reproductive isolating mechanisms, but gene flow between incipient species can also represent a source for potentially beneficial alleles. Recently, genome-wide datasets have revealed clusters of differentiated loci (‘genomic islands of divergence’) that are thought to play a role in reproductive isolation and therefore have reduced gene flow. We use simulations to further examine the evolutionary forces that shape and maintain genomic islands of divergence between two subspecies of the migratory songbird, Swainsons thrush (Catharus ustulatus), which have come into secondary contact since the last glacial maximum. We find that, contrary to expectation, gene flow is high within islands and is highly asymmetric. In addition, patterns of nucleotide diversity at highly differentiated loci suggest selection was more frequent in a single ecotype. We propose a mechanism whereby beneficial alleles spread via selective sweeps following a post-glacial demographic expansion in one subspecies and move preferentially across the hybrid zone. We find no evidence that genomic islands are the result of divergent selection or reproductive isolation, rather our results suggest that differentiated loci both within and outside islands could provide opportunities for adaptive introgression across porous species boundaries.

Genomic divergence across ecological gradients in the Central African rainforest songbird (Andropadus virens)

The little greenbul, a common rainforest passerine from sub‐Saharan Africa, has been the subject of long‐term evolutionary studies to understand the mechanisms leading to rainforest speciation. Previous research found morphological and behavioural divergence across rainforest–savannah transition zones (ecotones), and a pattern of divergence with gene flow suggesting divergent natural selection has contributed to adaptive divergence and ecotones could be important areas for rainforests speciation. Recent advances in genomics and environmental modelling make it possible to examine patterns of genetic divergence in a more comprehensive fashion. To assess the extent to which natural selection may drive patterns of differentiation, here we investigate patterns of genomic differentiation among populations across environmental gradients and regions. We find compelling evidence that individuals form discrete genetic clusters corresponding to distinctive environmental characteristics and habitat types. Pairwise FST between populations in different habitats is significantly higher than within habitats, and this differentiation is greater than what is expected from geographic distance alone. Moreover, we identified 140 SNPs that showed extreme differentiation among populations through a genomewide selection scan. These outliers were significantly enriched in exonic and coding regions, suggesting their functional importance. Environmental association analysis of SNP variation indicates that several environmental variables, including temperature and elevation, play important roles in driving the pattern of genomic diversification. Results lend important new genomic evidence for environmental gradients being important in population differentiation.

Response to Comment on “Genomic signals of selection predict climate-driven population declines in a migratory bird”

Fitzpatrick et al. discuss issues that they had with analyses and interpretation in our recent manuscript on genomic correlates of climate in yellow warblers. We provide evidence that our findings would not change with different analysis and maintain that our study represents a promising direction for integrating the potential for climate adaptation as one of many tools in conservation management.