Differential introgression and the maintenance of species boundaries in an advanced generation avian hybrid zone

Background: Evolutionary processes, including selection and differential fitness, shape the introgression of genetic material across a hybrid zone, resulting in the exchange of some genes but not others. Differential introgression of molecular or phenotypic markers can thus provide insight into factors contributing to reproductive isolation. We characterized patterns of genetic variation across a hybrid zone between two tidal marsh birds, Saltmarsh (Ammodramus caudacutus) and Nelson’s (A. nelsoni) sparrows (n = 286), and compared patterns of introgression among multiple genetic markers and phenotypic traits. Results: Geographic and genomic cline analyses revealed variable patterns of introgression among marker types. Most markers exhibited gradual clines and indicated that introgression exceeds the spatial extent of the previously documented hybrid zone. We found steeper clines, indicating strong selection for loci associated with traits related to tidal marsh adaptations, including for a marker linked to a gene region associated with metabolic functions, including an osmotic regulatory pathway, as well as for a marker related to melanin-based pigmentation, supporting an adaptive role of darker plumage (salt marsh melanism) in tidal marshes. Narrow clines at mitochondrial and sex-linked markers also offer support for Haldane’s rule. We detected patterns of asymmetrical introgression toward A. caudacutus, which may be driven by differences in mating strategy or differences in population density between the two species. Conclusions: Our findings offer insight into the dynamics of a hybrid zone traversing a unique environmental gradient and provide evidence for a role of ecological divergence in the maintenance of pure species boundaries despite ongoing gene flow

Differential introgression and the maintenance of species boundaries in an advanced generation avian hybrid zone

Background: Evolutionary processes, including selection and differential fitness, shape the introgression of genetic material across a hybrid zone, resulting in the exchange of some genes but not others. Differential introgression of molecular or phenotypic markers can thus provide insight into factors contributing to reproductive isolation. We characterized patterns of genetic variation across a hybrid zone between two tidal marsh birds, Saltmarsh (Ammodramus caudacutus) and Nelson’s (A. nelsoni) sparrows (n = 286), and compared patterns of introgression among multiple genetic markers and phenotypic traits. Results: Geographic and genomic cline analyses revealed variable patterns of introgression among marker types. Most markers exhibited gradual clines and indicated that introgression exceeds the spatial extent of the previously documented hybrid zone. We found steeper clines, indicating strong selection for loci associated with traits related to tidal marsh adaptations, including for a marker linked to a gene region associated with metabolic functions, including an osmotic regulatory pathway, as well as for a marker related to melanin-based pigmentation, supporting an adaptive role of darker plumage (salt marsh melanism) in tidal marshes. Narrow clines at mitochondrial and sex-linked markers also offer support for Haldane’s rule. We detected patterns of asymmetrical introgression toward A. caudacutus, which may be driven by differences in mating strategy or differences in population density between the two species. Conclusions: Our findings offer insight into the dynamics of a hybrid zone traversing a unique environmental gradient and provide evidence for a role of ecological divergence in the maintenance of pure species boundaries despite ongoing gene flow

Fine-scale population structure and asymmetrical dispersal in an obligate salt-marsh passerine, the Saltmarsh Sparrow (Ammodramus Caudacutus)

Understanding the spatial scale of gene flow can yield valuable insight into the ecology of an organism and guide conservation strategies. Fine-scale genetic structure is uncommon in migratory passerines because of their high vagility and presumed high dispersal abilities. Aspects of the behavior and ecology of some migratory species, however, may promote structure on a finer scale in comparison to their mobility. We investigated population genetic structure in the Saltmarsh Sparrow (Ammodramus caudacutus), a migratory passerine that breeds along the northeastern coast of the United States, where it is restricted exclusively to a narrow strip of patchily distributed tidal marsh habitat. Using genotyping with 10 microsatellite loci, we detected weak but significant population structure among Saltmarsh Sparrows from nine marshes on the breeding grounds between Scarborough, Maine, and Oceanside, New York. Genetic variation among marshes was largely consistent with a pattern of isolation by distance, with some exceptions. One inland marsh was genetically divergent despite its proximity to other sampled marshes, which suggests that mechanisms besides geographic distance influence population genetic structure. Bayesian clustering, multivariate analyses, and assignment tests supported a population structure consisting of five groups. Estimates of migration rates indicated variation in gene flow among marshes, which suggests asymmetrical dispersal and possible source-sink population dynamics. The genetic structure that we found in Saltmarsh Sparrows may result from natal philopatry and breeding-site fidelity, combined with restricted dispersal due to obligate dependence on a patchy habitat. Our findings suggest that fine-scale population structure may be important in some migratory passerines. Received 12 July 2011, accepted 1 February 2012

Genotype-environment associations support a mosaic hybrid zone between two tidal marsh birds

Local environmental features can shape hybrid zone dynamics when hybrids are bounded by ecotones or when patchily distributed habitat types lead to a corresponding mosaic of genotypes. We investigated the role of marsh-level characteristics in shaping a hybrid zone between two recently diverged avian taxa – Saltmarsh (Ammodramus caudacutus) and Nelson\u27s (A. nelsoni) sparrows. These species occupy different niches where allopatric, with caudacutus restricted to coastal marshes and nelsoni found in a broader array of wetland and grassland habitats and co-occur in tidal marshes in sympatry. We determined the influence of habitat types on the distribution of pure and hybrid sparrows and assessed the degree of overlap in the ecological niche of each taxon. To do this, we sampled and genotyped 305 sparrows from 34 marshes across the hybrid zone and from adjacent regions. We used linear regression to test for associations between marsh characteristics and the distribution of pure and admixed sparrows. We found a positive correlation between genotype and environmental variables with a patchy distribution of genotypes and habitats across the hybrid zone. Ecological niche models suggest that the hybrid niche was more similar to that of A. nelsoni and habitat suitability was influenced strongly by distance from coastline. Our results support a mosaic model of hybrid zone maintenance, suggesting a role for local environmental features in shaping the distribution and frequency of pure species and hybrids across space

Genotype-environment associations support a mosaic hybrid zone between two tidal marsh birds

Local environmental features can shape hybrid zone dynamics when hybrids are bounded by ecotones or when patchily distributed habitat types lead to a corresponding mosaic of genotypes. We investigated the role of marsh-level characteristics in shaping a hybrid zone between two recently diverged avian taxa – Saltmarsh (Ammodramus caudacutus) and Nelson\u27s (A. nelsoni) sparrows. These species occupy different niches where allopatric, with caudacutus restricted to coastal marshes and nelsoni found in a broader array of wetland and grassland habitats and co-occur in tidal marshes in sympatry. We determined the influence of habitat types on the distribution of pure and hybrid sparrows and assessed the degree of overlap in the ecological niche of each taxon. To do this, we sampled and genotyped 305 sparrows from 34 marshes across the hybrid zone and from adjacent regions. We used linear regression to test for associations between marsh characteristics and the distribution of pure and admixed sparrows. We found a positive correlation between genotype and environmental variables with a patchy distribution of genotypes and habitats across the hybrid zone. Ecological niche models suggest that the hybrid niche was more similar to that of A. nelsoni and habitat suitability was influenced strongly by distance from coastline. Our results support a mosaic model of hybrid zone maintenance, suggesting a role for local environmental features in shaping the distribution and frequency of pure species and hybrids across space

Relationship of phenotypic variation and genetic admixture in the Saltmarsh–Nelson\u27s sparrow hybrid zone

Hybridization is influential in shaping species\u27 dynamics and has many evolutionary and conservation implications. Identification of hybrid individuals typically relies on morphological data, but the assumption that hybrids express intermediate traits is not always valid, because of complex patterns of introgression and selection. We characterized phenotypic and genotypic variation across a hybrid zone between 2 tidal-marsh birds, the Saltmarsh Sparrow (Ammodramus caudacutus) and Nelson\u27s Sparrow (A. nelsoni) (n = 290), and we sought to identify morphological traits that could be used to classify admixed individuals. Sparrows were sampled from a total of 34 marshes, including 23 sympatric and 11 putatively allopatric marshes. Each individual was scored at 13 plumage traits, and standard morphometric data were collected. We used genotyping analysis at 24 microsatellite loci to categorize individuals into genotypic classes of pure, F1–F2, or backcrossed. Genetic data revealed that 52% of individuals sampled along the geographic transect were of mixed ancestry, and the majority of these were backcrossed. Traits related to the definition of plumage features (streaking, crown, and face) showed less overlap between genotypic classes than traits related to the amount or color of plumage features. Although morphological data performed well in distinguishing between the 2 taxa, pure and backcrossed individuals of each parental type could not be distinguished because of substantial overlap in plumage and morphology. We conclude that the discrimination of pure and hybrid individuals is not possible in the absence of genetic data. Our results have implications for conservation of pure populations, as extensive backcrossing throughout the hybrid zone may present challenges for monitoring pure species identified by morphology alone

Anthropogenic Habitats Facilitate Dispersal of an Early Successional Obligate: Implications for Restoration of an Endangered Ecosystem

Landscape modification and habitat fragmentation disrupt the connectivity of natural landscapes, with major consequences for biodiversity. Species that require patchily distributed habitats, such as those that specialize on early successional ecosystems, must disperse through a landscape matrix with unsuitable habitat types. We evaluated landscape effects on dispersal of an early successional obligate, the New England cottontail (Sylvilagus transitionalis). Using a landscape genetics approach, we identified barriers and facilitators of gene flow and connectivity corridors for a population of cottontails in the northeastern United States. We modeled dispersal in relation to landscape structure and composition and tested hypotheses about the influence of habitat fragmentation on gene flow. Anthropogenic and natural shrubland habitats facilitated gene flow, while the remainder of the matrix, particularly development and forest, impeded gene flow. The relative influence of matrix habitats differed between study areas in relation to a fragmentation gradient. Barrier features had higher explanatory power in the more fragmented site, while facilitating features were important in the less fragmented site. Landscape models that included a simultaneous barrier and facilitating effect of roads had higher explanatory power than models that considered either effect separately, supporting the hypothesis that roads act as both barriers and facilitators at all spatial scales. The inclusion of LiDAR-identified shrubland habitat improved the fit of our facilitator models. Corridor analyses using circuit and least cost path approaches revealed the importance of anthropogenic, linear features for restoring connectivity between the study areas. In fragmented landscapes, human-modified habitats may enhance functional connectivity by providing suitable dispersal conduits for early successional specialists

Separating Proactive Conservation from Species Listing Decisions

Proactive Conservation is a paradigm of natural resource management in the United States that encourages voluntary, collaborative efforts to restore species before they need to be protected through government regulations. This paradigm is widely used to conserve at-risk species today, and when used in conjunction with the Policy for Evaluation of Conservation Efforts (PECE), it allows for successful conservation actions to preclude listing of species under the Endangered Species Act (ESA). Despite the popularity of this paradigm, and recent flagship examples of its use (e.g., greater sage grouse, Centrocercus urophasianus), critical assessments of the outcomes of Proactive Conservation are lacking from the standpoint of species status and recovery metrics. Here, we provide such an evaluation, using the New England cottontail (Sylvilagus transitionalis), heralded as a success of Proactive Conservation efforts in the northeastern United States, as a case study. We review the history and current status of the species, based on the state of the science, in the context of the Conservation Initiative, and the 2015 PECE decision not to the list the species under the ESA. In addition to the impacts of the PECE decision on the New England cottontail conservation specifically, our review also evaluates the benefits and limits of the Proactive Conservation paradigm more broadly, and we make recommendations for its role in relation to ESA implementation for the future of at-risk species management. We find that the status and assurances for recovery under the PECE policy, presented at the time of the New England cottontail listing decision, were overly optimistic, and the status of the species has worsened in subsequent years. We suggest that use of PECE to avoid listing may occur because of the perception of the ESA as a punitive law and a misconception that it is a failure, although very few listed species have gone extinct. Redefining recovery to decouple it from delisting and instead link it to probability of persistence under recommended conservation measures would remove some of the stigma of listing, and it would strengthen the role of Species Status Assessments in endangered species conservation

SECR output from simulated data with detection (g0) of 0.2

SECR density estimates and other associated output and error measures for simulated survey data with a detection probability at the home range center (g0) of 0.2. Data were simulated and densities estimated for multiple scenarios representing combinations of pellet spacing, transect spacing, and survey occasion. These scenarios represented a range of realistic survey options in the field, from low to high intensity survey effort. Each dataset was simulated for 4 different densities on the landscape: 0.5, 1.0, 2.0, and 3.0 rabbits/ha