Microgeographic divergence in a single-island endemic: evolutionary patterns and conservation implications

2014 Summer.Understanding the processes that generate biological diversity is the central goal of evolutionary biology. Geographic isolation has traditionally been viewed as the primary scenario favoring evolutionary divergence. However, there is growing appreciation for the role of ecological variation and natural selection in driving adaptive differentiation, even in the absence of geographic barriers to gene flow. My dissertation tests for microgeographic patterns of local adaptation within one of the most range-restricted bird species in North America, the Island Scrub-Jay (Aphelocoma insularis). The species is restricted to Santa Cruz Island in southern California, USA, where it occurs in a diversity of habitat types within its narrow (250 km2) geographic range. Remarkably, I found that Island Scrub-Jays in three separate stands of pine habitat had longer, narrower bills than those in oak habitat, a pattern that mirrors adaptive differences between allopatric populations of the species' mainland congener (A. californica). Adaptive divergence was not constrained by genetic diversity, even though Island Scrub-Jays had much lower levels of neutral genetic diversity than A. californica. Genetic data indicate that Island Scrub-Jays in pine habitat were more closely related to individuals in adjacent oak habitat than to individuals in other pine stands, indicating that each pine stand can be considered an independent case where adaptive divergence has been maintained in the face of some gene flow with adjacent oak birds. Morphological differences were not abrupt across the pine-oak boundary, as bill length declined gradually with distance from pine habitat, a clinal pattern that is also consistent with a scenario of divergence-with-gene flow. Individuals mated non-randomly with respect to bill length within the population, which may be due to a combination of (1) isolation-by-distance (localized dispersal) across the landscape and spatial autocorrelation in bill morphology, and (2) assortative mating at a more local scale based on bill morphology or correlated acoustic signals. These findings provide strong support for the notion that microgeographic patterns of local adaptation may be more common than is currently appreciated, even in mobile taxonomic groups like birds. They also underscore the importance of conserving Island Scrub-Jays across the entire island in order to preserve the species' full range of biological diversity and to facilitate adaptive responses to future environmental changes

Data from: Bill morphology and neutral genetic structure both predict variation in acoustic signals within a bird population

Adaptive evolutionary divergence within a population can be facilitated by associated divergence in mating signals. Acoustic signals are often involved in mate choice, and are also known to diverge spatially in response to a variety of processes. In birds, for instance, variation in bill size and shape can result in correlated changes in vocalizations due to functional constraints on sound production. Acoustic signals can also vary spatially in relation to neutral genetic structure (due to cultural drift) and/or habitat structure (due to acoustic adaptation for optimal sound transmission). Here we test these alternative hypotheses as causes of variation in acoustic signal structure in the Island Scrub-Jay (Aphelocoma insularis), a species that is restricted to one small island (Santa Cruz Island, California, USA) and exhibits spatial genetic structure and microgeographic divergence in bill morphology across short distances and habitat types. We find that bill morphology is related to the structure of the female “rattle” call, a vocalization associated with territorial disputes and male-female interactions. Females with longer, shallower bills produced calls that were more rapid, and those with shallower bills also produced calls that were lower in frequency. In addition, rattle rapidity varied across the island in accordance with neutral genetic structure. Vocal characteristics were not related to habitat structure, suggesting that variation in rattle calls is unlikely to reflect optimization for sound transmission. Our findings indicate that selection on bill morphology and cultural drift can jointly shape variation in acoustic signal structure, even at fine spatial scales within populations

Sofaer_etal_OCWA_AdultSurvival

Files with input and results from analysis of orange-crowned warbler adult survival in Program MARK

Data from: Partial support for the central–marginal hypothesis within a population: reduced genetic diversity but not increased differentiation at the range edge of an island endemic bird

Large-scale population comparisons have contributed to our understanding of the evolution of geographic range limits and species boundaries, as well as the conservation value of populations at range margins. The central–marginal hypothesis (CMH) predicts a decline in genetic diversity and an increase in genetic differentiation toward the periphery of species’ ranges due to spatial variation in genetic drift and gene flow. Empirical studies on a diverse array of taxa have demonstrated support for the CMH. However, nearly all such studies come from widely distributed species, and have not considered if the same processes can be scaled down to single populations. Here, we test the CMH on a species composed of a single population: the Island Scrub-Jay (Aphelocoma insularis), endemic to a 250 km2 island. We examined microsatellite data from a quarter of the total population and found that homozygosity increased toward the island’s periphery. However, peripheral portions of the island did not exhibit higher genetic differentiation. Simulations revealed that highly localized dispersal and small total population size, but not spatial variation in population density, were critical for generating fine-scale variation in homozygosity. Collectively, these results demonstrate that microevolutionary processes driving spatial variation in genetic diversity among populations can also be important for generating spatial variation in genetic diversity within populations

Data from: Islands within an island: repeated adaptive divergence in a single population

Physical barriers to gene flow were once viewed as prerequisites for adaptive evolutionary divergence. However, a growing body of theoretical and empirical work suggests that divergence can proceed within a single population. Here we document genetic structure and spatially-replicated patterns of phenotypic divergence within a bird species endemic to 250 km2 Santa Cruz Island, California, USA. Island scrub-jays (Aphelocoma insularis) in three separate stands of pine habitat had longer, shallower bills than jays in oak habitat, a pattern that mirrors adaptive differences between allopatric populations of the species’ mainland congener. Variation in both bill measurements was heritable, and island scrub-jays mated non-randomly with respect to bill morphology. The population was not panmictic; instead, we found a continuous pattern of isolation by distance across the east-west axis of the island, as well as a subtle genetic discontinuity across the boundary between the largest pine stand and adjacent oak habitat. The ecological factors that appear to have facilitated adaptive differentiation at such a fine scale—environmental heterogeneity and localized dispersal—are ubiquitous in nature. These findings support recent arguments that microgeographic patterns of adaptive divergence may be more common than currently appreciated, even in mobile taxonomic groups like birds

Non-breeding season events influence sexual selection in a long-distance migratory bird

The study of sexual selection has traditionally focused on events and behaviours immediately surrounding copulation. In this study, we examine whether carry-over effects from the non-breeding season can influence the process of sexual selection in a long-distance migratory bird, the American redstart (Setophaga ruticilla). Previous work on American redstarts demonstrated that overwintering in a high-quality habitat influences spring departure dates from the wintering grounds, advances arrival dates on the breeding grounds and increases apparent reproductive success. We show that the mixed-mating strategy of American redstarts compounds the benefits of overwintering in high-quality winter habitats. Males arriving to breed in Canada from high-quality winter habitats arrive earlier than males from poor-quality habitats, resulting in a lower probability of paternity loss, a higher probability of achieving polygyny and ultimately higher realized reproductive success. Such results suggest that the process of sexual selection may be influenced by events interacting throughout the annual cycle

Sofaer_etal_OCWANestSurvival

Orange-crowned warbler nest survival data

Sofaer_etal_OCWAFecundityData

Orange-crowned warbler fecundity data