Population genomic structure of a widespread, urban-dwelling mammal: The eastern grey squirrel (Sciurus carolinensis).

Urbanization is a persistent and widespread driver of global environmental change, potentially shaping evolutionary processes due to genetic drift and reduced gene flow in cities induced by habitat fragmentation and small population sizes. We tested this prediction for the eastern grey squirrel (Sciurus carolinensis), a common and conspicuous forest-dwelling rodent, by obtaining 44K SNPs using reduced representation sequencing (ddRAD) for 403 individuals sampled across the species' native range in eastern North America. We observed moderate levels of genetic diversity, low levels of inbreeding, and only a modest signal of isolation-by-distance. Clustering and migration analyses show that estimated levels of migration and genetic connectivity were higher than expected across cities and forested areas, specifically within the eastern portion of the species' range dominated by urbanization, and genetic connectivity was less than expected within the western range where the landscape is fragmented by agriculture. Landscape genetic methods revealed greater gene flow among individual squirrels in forested regions, which likely provide abundant food and shelter for squirrels. Although gene flow appears to be higher in areas with more tree cover, only slight discontinuities in gene flow suggest eastern grey squirrels have maintained connected populations across urban areas in all but the most heavily fragmented agricultural landscapes. Our results suggest urbanization shapes biological evolution in wildlife species depending strongly on the composition and habitability of the landscape matrix surrounding urban areas.

Rural selection drives the evolution of an urban-rural cline in coat color in gray squirrels.

Phenotypic differences between urban and rural populations are well-documented, but the evolutionary processes driving trait variation along urbanization gradients are often unclear. We combined spatial data on abundance, trait variation, and measurements of fitness to understand cline structure and test for natural selection on heritable coat color morphs (melanic, gray) of eastern gray squirrels (Sciurus carolinensis) along an urbanization gradient. Population surveys using remote cameras and visual counts at 76 sites along the urbanization gradient revealed a significant cline in melanism, decreasing from 48% in the city center to <5% in rural woodlands. Among 76 squirrels translocated to test for phenotypic selection, survival was lower for the melanic than gray morph in rural woodlands, whereas there was no difference in survival between color morphs in the city. These results suggest the urban-rural cline in melanism is explained by natural selection favoring the gray morph in rural woodlands combined with relaxed selection in the city. Our study illustrates how trait variation between urban and rural populations can emerge from selection primarily in rural populations rather than adaptation to novel features of the urban environment.

Testing the niche reduction hypothesis for a fossorial rodent (Geomys bursarius) experiencing agricultural intensification.

Habitat loss and fragmentation from conversion to agriculture are known threats to grassland species. However, continued agricultural intensification may further reduce a species distribution and realized niche. Here, we create species distribution models (SDMs) for the plains pocket gopher (Geomys bursarius), an ecosystem engineer in grasslands, for historic and contemporary eras in a dynamic agroecosystem and test the "niche reduction hypothesis." We compare SDMs created from gopher occurrences from the historic era (~1950s, pre-agricultural intensification) and the contemporary era (post-agricultural intensification) and assess model transferability. We evaluate shifts in environmental relationships, changes in limiting factors, and an overall decline in niche hypervolume. SDMs were nontransferable between the historic and contemporary eras. Environmental drivers of gopher distribution shifted from elevation, precipitation, and land cover in the 1950s to land cover, soil texture, and soil drainage presently. There also were shifts in environmental associations with gophers now occurring at lower elevations, in sandier soils, and less often in agriculture. Dominant limiting factors of gophers shifted from precipitation to land cover. Gophers were not detected at historic locations during recent resurveys. Contemporary niche hypervolume was reduced compared with the historic niche hypervolume. We found support for the niche reduction hypothesis for a fossorial, grassland species. Further application of the niche reduction hypothesis in landscapes experiencing agricultural intensification is warranted. Understanding niche reduction allows for conservation efforts that promote continued persistence in the contemporary niche while also identifying areas to restore within the historic niche.

Parallel evolution of urban-rural clines in melanism in a widespread mammal.

Urbanization is the dominant trend of global land use change. The replicated nature of environmental change associated with urbanization should drive parallel evolution, yet insight into the repeatability of evolutionary processes in urban areas has been limited by a lack of multi-city studies. Here we leverage community science data on coat color in > 60,000 eastern gray squirrels (Sciurus carolinensis) across 43 North American cities to test for parallel clines in melanism, a genetically based trait associated with thermoregulation and crypsis. We show the prevalence of melanism was positively associated with urbanization as measured by impervious cover. Urban-rural clines in melanism were strongest in the largest cities with extensive forest cover and weakest or absent in cities with warmer winter temperatures, where thermal selection likely limits the prevalence of melanism. Our results suggest that novel traits can evolve in a highly repeatable manner among urban areas, modified by factors intrinsic to individual cities, including their size, land cover, and climate.

Correlates of bird collisions with buildings across three North American countries.

Collisions with buildings cause up to 1 billion bird fatalities annually in the United States and Canada. However, efforts to reduce collisions would benefit from studies conducted at large spatial scales across multiple study sites with standardized methods and consideration of species- and life-history-related variation and correlates of collisions. We addressed these research needs through coordinated collection of data on bird collisions with buildings at sites in the United States (35), Canada (3), and Mexico (2). We collected all carcasses and identified species. After removing records for unidentified carcasses, species lacking distribution-wide population estimates, and species with distributions overlapping fewer than 10 sites, we retained 269 carcasses of 64 species for analysis. We estimated collision vulnerability for 40 bird species with ≥2 fatalities based on their North American population abundance, distribution overlap in study sites, and sampling effort. Of 10 species we identified as most vulnerable to collisions, some have been identified previously (e.g., Black-throated Blue Warbler [Setophaga caerulescens]), whereas others emerged for the first time (e.g., White-breasted Nuthatch [Sitta carolinensis]), possibly because we used a more standardized sampling approach than past studies. Building size and glass area were positively associated with number of collisions for 5 of 8 species with enough observations to analyze independently. Vegetation around buildings influenced collisions for only 1 of those 8 species (Swainson's Thrush [Catharus ustulatus]). Life history predicted collisions; numbers of collisions were greatest for migratory, insectivorous, and woodland-inhabiting species. Our results provide new insight into the species most vulnerable to building collisions, making them potentially in greatest need of conservation attention to reduce collisions and into species- and life-history-related variation and correlates of building collisions, information that can help refine collision management.

Correlaciones de las Colisiones de Aves contra Edificios en Tres Países de América del Norte Resumen Las colisiones contra los edificios causan hasta mil millones de fatalidades de aves al año en los Estados Unidos y en Canadá. Sin embargo, los esfuerzos por reducir estas colisiones se beneficiarían con estudios realizados a grandes escalas espaciales en varios sitios de estudio con métodos estandarizados y considerando las variaciones relacionadas a la historia de vida y a la especie y las correlaciones de las colisiones. Abordamos estas necesidades de investigación por medio de una recolección coordinada de datos sobre las colisiones de aves contra edificios en los Estados Unidos (35), Canadá (3) y México (2). Recolectamos todos los cadáveres y los identificamos hasta especie. Después de retirar los registros de cadáveres no identificados, las especies sin estimaciones poblacionales a nivel distribución y las especies con distribuciones traslapadas en menos de diez sitios, nos quedamos con 269 cadáveres de 64 especies para el análisis. Estimamos la vulnerabilidad a colisiones para 40 especies con ≥2 fatalidades con base en la abundancia poblacional para América del Norte, el traslape de su distribución entre los sitios de estudio y el esfuerzo de muestreo. De las diez especies que identificamos como las más vulnerables a las colisiones, algunas han sido identificadas previamente (Setophaga caerulescens), y otras aparecieron por primera vez (Sitta carolinensis), posiblemente debido a que usamos una estrategia de muestreo más estandarizada que en los estudios previos. El tamaño del edificio y el área del vidrio estuvieron asociados positivamente con el número de colisiones para cinco de ocho especies con suficientes observaciones para ser analizadas independientemente. La vegetación alrededor de los edificios influyó sobre las colisiones solamente para una de esas ocho especies Catharus ustulatus). Las historias de vida pronosticaron las colisiones; el número de colisiones fue mayor para las especies migratorias, insectívoras y aquellas que habitan en las zonas boscosas. Nuestros resultados proporcionan una nueva perspectiva hacia las especies más vulnerables a las colisiones contra edificios, lo que las pone en una necesidad potencialmente mayor de atención conservacionista para reducir estas colisiones y de estudio de las variaciones relacionadas con la especie y la historia de vida y las correlaciones de las colisiones contra edificios, información que puede ayudar a refinar el manejo de colisiones.

From CREATE Workshop to Course Implementation: Examining Downstream Impacts on Teaching Practices and Student Learning at 4-Year Institutions.

The faculty workshop model has long been used for disseminating innovative methods in STEM education. Despite significant investments by researchers and funding agencies, there is a dearth of evidence regarding downstream impacts of faculty development. CREATE is an evidence-based strategy for teaching science using primary literature. In this study, we examined whether workshop-trained faculty applied CREATE methods effectively and whether their students achieved either cognitive or affective gains. We followed 10 workshop alumni at different 4-year institutions throughout the United States. External observations of the teaching indicated a high fidelity of CREATE implementation. The students made significant gains in cognitive (e.g., designing experiments) and affective (e.g., self-efficacy in science process skills) domains. Some student outcomes correlated with particular characteristics (e.g., class size) but not with others (e.g., teaching experience). These findings provide evidence for the robustness of the CREATE dissemination model and provide perspective on factors that may influence pedagogical reform efforts.

Effects of urbanization on the population structure of freshwater turtles across the United States.

Landscape-scale alterations that accompany urbanization may negatively affect the population structure of wildlife species such as freshwater turtles. Changes to nesting sites and higher mortality rates due to vehicular collisions and increased predator populations may particularly affect immature turtles and mature female turtles. We hypothesized that the proportions of adult female and immature turtles in a population will negatively correlate with landscape urbanization. As a collaborative effort of the Ecological Research as Education Network (EREN), we sampled freshwater turtle populations in 11 states across the central and eastern United States. Contrary to expectations, we found a significant positive relationship between proportions of mature female painted turtles (Chrysemys picta) and urbanization. We did not detect a relationship between urbanization and proportions of immature turtles. Urbanization may alter the thermal environment of nesting sites such that more females are produced as urbanization increases. Our approach of creating a collaborative network of scientists and students at undergraduate institutions proved valuable in terms of testing our hypothesis over a large spatial scale while also allowing students to gain hands-on experience in conservation science.

Evolutionary response to global change: Climate and land use interact to shape color polymorphism in a woodland salamander.

Evolutionary change has been demonstrated to occur rapidly in human-modified systems, yet understanding how multiple components of global change interact to affect adaptive evolution remains a critical knowledge gap. Climate change is predicted to impose directional selection on traits to reduce thermal stress, but the strength of directional selection may be mediated by changes in the thermal environment driven by land use. We examined how regional climatic conditions and land use interact to affect genetically based color polymorphism in the eastern red-backed salamander (Plethodon cinereus). P. cinereus is a woodland salamander with two primary discrete color morphs (striped, unstriped) that have been associated with macroclimatic conditions. Striped individuals are most common in colder regions, but morph frequencies can be variable within climate zones. We used path analysis to analyze morph frequencies among 238,591 individual salamanders across 1,170 sites in North America. Frequency of striped individuals was positively related to forest cover in populations occurring in warmer regions (>7°C annually), a relationship that was weak to nonexistent in populations located in colder regions (≤7°C annually). Our results suggest that directional selection imposed by climate warming at a regional scale may be amplified by forest loss and suppressed by forest persistence, with a mediating effect of land use that varies geographically. Our work highlights how the complex interaction of selection pressures imposed by different components of global change may lead to divergent evolutionary trajectories among populations.

Rapid genetic restoration of a keystone species exhibiting delayed demographic response.

Genetic founder effects are often expected when animals colonize restored habitat in fragmented landscapes, but empirical data on genetic responses to restoration are limited. We examined the genetic response of banner-tailed kangaroo rats (Dipodomys spectabilis) to landscape-scale grassland restoration in the Chihuahuan Desert of New Mexico, USA. Dipodomys spectabilis is a grassland specialist and keystone species. At sites treated with herbicide to remove shrubs, colonization by D. spectabilis is slow and populations persist at low density for ≥10 years (≥6 generations). Persistence at low density and low gene flow may cause strong founder effects. We compared genetic structure of D. spectabilis populations between treated sites and remnant grasslands, and we examined how the genetic response to restoration depended on treatment age, area, and connectivity to source populations. Allelic richness and heterozygosity were similar between treated sites and remnant grasslands. Allelic richness at treated sites was greatest early in the restoration trajectory, and genetic divergence did not differ between recently colonized and established populations. These results indicated that founder effects during colonization of treated sites were weak or absent. Moreover, our results suggested founder effects were not mitigated by treatment area or connectivity. Dispersal is negatively density-dependent in D. spectabilis, and we hypothesize that high gene flow may occur early in the restoration trajectory when density is low. Our study shows genetic diversity can be recovered more rapidly than demographic components of populations after habitat restoration and that founder effects are not inevitable for animals colonizing restored habitat in fragmented landscapes.

Window area and development drive spatial variation in bird-window collisions in an urban landscape.

Collisions with windows are an important human-related threat to birds in urban landscapes. However, the proximate drivers of collisions are not well understood, and no study has examined spatial variation in mortality in an urban setting. We hypothesized that the number of fatalities at buildings varies with window area and habitat features that influence avian community structure. In 2010 we documented bird-window collisions (BWCs) and characterized avian community structure at 20 buildings in an urban landscape in northwestern Illinois, USA. For each building and season, we conducted 21 daily surveys for carcasses and nine point count surveys to estimate relative abundance, richness, and diversity. Our sampling design was informed by experimentally estimated carcass persistence times and detection probabilities. We used linear and generalized linear mixed models to evaluate how habitat features influenced community structure and how mortality was affected by window area and factors that correlated with community structure. The most-supported model was consistent for all community indices and included effects of season, development, and distance to vegetated lots. BWCs were related positively to window area and negatively to development. We documented mortalities for 16/72 (22%) species (34 total carcasses) recorded at buildings, and BWCs were greater for juveniles than adults. Based on the most-supported model of BWCs, the median number of annual predicted fatalities at study buildings was 3 (range = 0-52). These results suggest that patchily distributed environmental resources and levels of window area in buildings create spatial variation in BWCs within and among urban areas. Current mortality estimates place little emphasis on spatial variation, which precludes a fundamental understanding of the issue. To focus conservation efforts, we illustrate how knowledge of the structural and environmental factors that influence bird-window collisions can be used to predict fatalities in the broader landscape.

Decoupling of genetic and phenotypic divergence in a headwater landscape.

In stream organisms, the landscape affecting intraspecific genetic and phenotypic divergence is comprised of two fundamental components: the stream network and terrestrial matrix. These components are known to differentially influence genetic structure in stream species, but to our knowledge, no study has compared their effects on genetic and phenotypic divergence. We examined how the stream network and terrestrial matrix affect genetic and phenotypic divergence in two stream salamanders, Gyrinophilus porphyriticus and Eurycea bislineata, in the Hubbard Brook Watershed, New Hampshire, USA. On the basis of previous findings and differences in adult terrestriality, we predicted that genetic divergence and phenotypic divergence in body morphology would be correlated in both species, but structured primarily by distance along the stream network in G. porphyriticus, and by overland distance in E. bislineata. Surprisingly, spatial patterns of genetic and phenotypic divergence were not strongly correlated. Genetic divergence, based on amplified DNA fragment length polymorphisms, increased with absolute geographic distance between sites. Phenotypic divergence was unrelated to absolute geographic distance, but related to relative stream vs. overland distances. In G. porphyriticus, phenotypic divergence was low when sites were close by stream distance alone and high when sites were close by overland distance alone. The opposite was true for E. bislineata. These results show that small differences in life history can produce large differences in patterns of intraspecific divergence, and the limitations of landscape genetic data for inferring phenotypic divergence. Our results also underscore the importance of explicitly comparing how terrestrial and aquatic conditions affect spatial patterns of divergence in species with biphasic life cycles.

Linking extinction-colonization dynamics to genetic structure in a salamander metapopulation.

Theory predicts that founder effects have a primary role in determining metapopulation genetic structure. However, ecological factors that affect extinction-colonization dynamics may also create spatial variation in the strength of genetic drift and migration. We tested the hypothesis that ecological factors underlying extinction-colonization dynamics influenced the genetic structure of a tiger salamander (Ambystoma tigrinum) metapopulation. We used empirical data on metapopulation dynamics to make a priori predictions about the effects of population age and ecological factors on genetic diversity and divergence among 41 populations. Metapopulation dynamics of A. tigrinum depended on wetland area, connectivity and presence of predatory fish. We found that newly colonized populations were more genetically differentiated than established populations, suggesting that founder effects influenced genetic structure. However, ecological drivers of metapopulation dynamics were more important than age in predicting genetic structure. Consistent with demographic predictions from metapopulation theory, genetic diversity and divergence depended on wetland area and connectivity. Divergence was greatest in small, isolated wetlands where genetic diversity was low. Our results show that ecological factors underlying metapopulation dynamics can be key determinants of spatial genetic structure, and that habitat area and isolation may mediate the contributions of drift and migration to divergence and evolution in local populations.

Linking movement behaviour to dispersal and divergence in plethodontid salamanders.

To better understand the evolutionary and ecological effects of dispersal, there is growing emphasis on the need to integrate direct data on movement behaviour into landscape-scale analyses. However, little is known about the general link between movement behaviour and large-scale patterns of dispersal and gene flow. Likewise, although recent studies suggest that nonrandom, directionally biased movement and dispersal can promote evolutionary divergence, the generality of this mechanism is unknown. We test the hypothesis that directionally biased movement and dispersal by plethodontid salamanders interact with the topography of headwater areas to affect genetic and phenotypic divergence. Movements by Gyrinophilus porphyriticus and Eurycea bislineata show contrasting directional biases: upstream bias in G. porphyriticus and downstream bias in E. bislineata. Consistent with predictions of how these biases interact with slope to affect dispersal and gene flow, genetic distance increased with slope in G. porphyriticus and decreased with slope in E. bislineata over a standardized distance of 1 km along six headwater streams. In both species, phenotypic divergence in relative trunk length was positively related to genetic divergence. These results indicate that landscape-scale patterns of dispersal and gene flow are closely related to movement behaviour in G. porphyriticus and E. bislineata, and underscore the value of information on movement behaviour for predicting and interpreting patterns of dispersal and gene flow in complex landscapes. This study also provides new evidence that directionally biased movement and dispersal can be important sources of intra- and interspecific variation in population divergence, and highlights the value of explicit, a priori predictions in landscape genetic studies.