Environmental and anthropogenic factors mediating the functional connectivity of the mesquite lizard along the eastern Trans-Mexican Volcanic Belt.

Functional connectivity, the extent to which a landscape facilitates or impedes the dispersal of individuals across the landscape, is a key factor for the survival of species. Anthropogenic activities, such as urbanization, agriculture and roads, negatively impact functional connectivity of most species, particularly low-vagility species like lizards. Here, we examine how a landscape modified by anthropogenic activities affects the functional connectivity, at both broad and fine scales, of a widely distributed generalist lizard Sceloporus grammicus in the eastern Trans-Mexican Volcanic Belt, Mexico. We estimated for the first time the species' genetic structure, gene flow and functional connectivity in agricultural and forest zones using genomic data, a comprehensive landscape characterization and novel methods including gravity models. Our results showed not only marked genetic differentiation across the study region but also that functional connectivity is maintained for tens of kilometres despite S. grammicus low vagility. Specifically, we found that substrate and air temperature facilitated connectivity over broad and fine scales, respectively, while agricultural cover, relative humidity and slope were important for connectivity and gene flow. Contrastingly, forest cover and roads favoured (broad-scale) and limited (fine-scale) connectivity, likely associated with movement facilitated by small forest patches and with thermoregulation. Altogether, these results support that S. grammicus alternates its thermoregulatory behaviour depending on the distance travelled and the habitat environmental conditions, and that it can disperse through relatively modified landscapes, mainly using agricultural zones. The information obtained is crucial to understanding the response of lizards to current anthropogenic pressures and their potential to adapt.

Natural and anthropogenic landscape factors shape functional connectivity of an ecological specialist in urban Southern California.

Identifying how natural (i.e., unaltered by human activity) and anthropogenic landscape variables influence contemporary functional connectivity in terrestrial organisms can elucidate the genetic consequences of environmental change. We examine population genetic structure and functional connectivity among populations of a declining species, the Blainville's horned lizard (Phrynosoma blainvillii), in the urbanized landscape of the Greater Los Angeles Area in Southern California, USA. Using single nucleotide polymorphism data, we assessed genetic structure among populations occurring at the interface of two abutting evolutionary lineages, and at a fine scale among habitat fragments within the heavily urbanized area. Based on the ecology of P. blainvillii, we predicted which environmental variables influence population structure and gene flow and used gravity models to distinguish among hypotheses to best explain population connectivity. Our results show evidence of admixture between two evolutionary lineages and strong population genetic structure across small habitat fragments. We also show that topography, microclimate, and soil and vegetation types are important predictors of functional connectivity, and that anthropogenic disturbance, including recent fire history and urban development, are key factors impacting contemporary population dynamics. Examining how natural and anthropogenic sources of landscape variation affect contemporary population genetics is critical to understanding how to best manage sensitive species in a rapidly changing landscape.

A test of the Niche Variation Hypothesis in a ruminant herbivore.

Despite the shared prediction that the width of a population's dietary niche expands as food becomes limiting, the Niche Variation Hypothesis (NVH) and Optimal Foraging Theory (OFT) offer contrasting views about how individuals alter diet selection when food is limited. Classical OFT predicts that dietary preferences do not change as food becomes limiting, so individuals expand their diets as they compensate for a lack of preferred foods. In contrast, the NVH predicts that among-individual variation in cognition, physiology or morphology create functional trade-offs in foraging efficiency, thereby causing individuals to specialize on different subsets of food as food becomes limiting. To evaluate (a) the predictions of the NVH and OFT and (b) evidence for physiological and cognitive-based functional trade-offs, we used DNA microsatellites and metabarcoding to quantify the diet, microbiome and genetic relatedness (a proxy for social learning) of 218 moose Alces alces across six populations that varied in their degree of food limitation. Consistent with both the NVH and OFT, dietary niche breadth increased with food limitation. Increased diet breadth of individuals-rather than increased diet specialization-was strongly correlated with both food limitation and dietary niche breadth of populations, indicating that moose foraged in accordance with OFT. Diets were not constrained by inheritance of the microbiome or inheritance of diet selection, offering support for the little-tested hypothesis that functional trade-offs in food use (or lack thereof) determine whether populations adhere to the predictions of the NVH or OFT. Our results indicate that both the absence of strong functional trade-offs and the digestive physiology of ruminants provide contexts under which populations should forage in accordance with OFT rather than the NVH. Also, because dietary niche width increased with increased food limitation, OFT and the NVH provide theoretical support for the notion that plant-herbivore interaction networks are plastic rather than static, which has important implications for understanding interspecific niche partitioning. Lastly, because population-level dietary niche breadth and calf recruitment are correlated, and because calf recruitment can be a proxy for food limitation, our work demonstrates how diet data can be employed to understand a populations' proximity to carrying capacity.

Regional variation in drivers of connectivity for two frog species (Rana pretiosa and R. luteiventris) from the U.S. Pacific Northwest.

Comparative landscape genetics has uncovered high levels of variability in which landscape factors affect connectivity among species and regions. However, the relative importance of species traits versus environmental variation for predicting landscape patterns of connectivity is unresolved. We provide evidence from a landscape genetics study of two sister taxa of frogs, the Oregon spotted frog (Rana pretiosa) and the Columbia spotted frog (Rana luteiventris) in Oregon and Idaho, USA. Rana pretiosa is relatively more dependent on moisture for dispersal than R. luteiventris, so if species traits influence connectivity, we predicted that connectivity among R. pretiosa populations would be more positively associated with moisture than R. luteiventris. However, if environmental differences are important drivers of gene flow, we predicted that connectivity would be more positively related to moisture in arid regions. We tested these predictions using eight microsatellite loci and gravity models in two R. pretiosa regions and four R. luteiventris regions (n = 1,168 frogs). In R. pretiosa, but not R. luteiventris, connectivity was positively related to mean annual precipitation, supporting our first prediction. In contrast, connectivity was not more positively related to moisture in more arid regions. Various temperature metrics were important predictors for both species and in all regions, but the directionality of their effects varied. Therefore, the pattern of variation in drivers of connectivity was consistent with predictions based on species traits rather than on environmental variation.

Landscape Composition and Management History Affect Alfalfa Weevil but not its Parasitoid.

It is widely recognized that both local and landscape-scale factors can be important drivers of crop pests, natural enemies, and biocontrol services. However, recent syntheses have found that landscape effects are inconsistent across study systems, highlighting the need for system-specific research to guide management decisions. In particular, studies conducted in perennial crops and that examine landscape configuration, not just composition, are especially lacking. We studied the impact of local and landscape factors on alfalfa weevil Hypera postica and its parasitoid Bathyplectes curculionis. Although classical biological control efforts have largely suppressed H. postica in the eastern United States, it remains problematic in the western United States. We sampled 20 production alfalfa fields in southeastern Wyoming to estimate H. postica density, parasitism rates by B. curculionis, and vegetation at local scales. We used remotely sensed imagery to characterize both landscape composition and configuration surrounding each sampled field. We used a hypothesis-driven modeling approach to determine which model was most predictive of H. postica and parasitism rate by B. curculionis. Landscape composition was the best model to predict H. postica densities. Host density was the best predictor of parasitism rates by B. curculionis. Production fields that had received insecticide applications in the last 5 years had higher weevil densities than fields that had not received insecticide applications. Stand age was not associated with weevil density or parasitism rate. In conclusion, we found local, landscape, and management components to be important in this system.

Testing evolutionary hypotheses for phenotypic divergence using landscape genetics.

Understanding the evolutionary causes of phenotypic variation among populations has long been a central theme in evolutionary biology. Several factors can influence phenotypic divergence, including geographic isolation, genetic drift, divergent natural or sexual selection, and phenotypic plasticity. But the relative importance of these factors in generating phenotypic divergence in nature is still a tantalizing and unresolved problem in evolutionary biology. The origin and maintenance of phenotypic divergence is also at the root of many ongoing debates in evolutionary biology, such as the extent to which gene flow constrains adaptive divergence (Garant et al. 2007) and the relative importance of genetic drift, natural selection, and sexual selection in initiating reproductive isolation and speciation (Coyne & Orr 2004). In this issue, Wang & Summers (2010) test the causes of one of the most fantastic examples of phenotypic divergence in nature: colour pattern divergence among populations of the strawberry poison frog (Dendrobates pumilio) in Panama and Costa Rica (Fig. 1). This study provides a beautiful example of the use of the emerging field of landscape genetics to differentiate among hypotheses for phenotypic divergence. Using landscape genetic analyses, Wang & Summers were able to reject the hypotheses that colour pattern divergence is due to isolation-by-distance (IBD) or landscape resistance. Instead, the hypothesis left standing is that colour divergence is due to divergent selection, in turn driving reproductive isolation among populations with different colour morphs. More generally, this study provides a wonderful example of how the emerging field of landscape genetics, which has primarily been applied to questions in conservation and ecology, now plays an essential role in evolutionary research.

Landscape genetics of high mountain frog metapopulations.

Explaining functional connectivity among occupied habitats is crucial for understanding metapopulation dynamics and species ecology. Landscape genetics has primarily focused on elucidating how ecological features between observations influence gene flow. Functional connectivity, however, may be the result of both these between-site (landscape resistance) landscape characteristics and at-site (patch quality) landscape processes that can be captured using network based models. We test hypotheses of functional connectivity that include both between-site and at-site landscape processes in metapopulations of Columbia spotted frogs (Rana luteiventris) by employing a novel justification of gravity models for landscape genetics (eight microsatellite loci, 37 sites, n = 441). Primarily used in transportation and economic geography, gravity models are a unique approach as flow (e.g. gene flow) is explained as a function of three basic components: distance between sites, production/attraction (e.g. at-site landscape process) and resistance (e.g. between-site landscape process). The study system contains a network of nutrient poor high mountain lakes where we hypothesized a short growing season and complex topography between sites limit R. luteiventris gene flow. In addition, we hypothesized production of offspring is limited by breeding site characteristics such as the introduction of predatory fish and inherent site productivity. We found that R. luteiventris connectivity was negatively correlated with distance between sites, presence of predatory fish (at-site) and topographic complexity (between-site). Conversely, site productivity (as measured by heat load index, at-site) and growing season (as measured by frost-free period between-sites) were positively correlated with gene flow. The negative effect of predation and positive effect of site productivity, in concert with bottleneck tests, support the presence of source-sink dynamics. In conclusion, gravity models provide a powerful new modelling approach for examining a wide range of both basic and applied questions in landscape genetics.

Landscape genetics: where are we now?

Landscape genetics has seen rapid growth in number of publications since the term was coined in 2003. An extensive literature search from 1998 to 2008 using keywords associated with landscape genetics yielded 655 articles encompassing a vast array of study organisms, study designs and methodology. These publications were screened to identify 174 studies that explicitly incorporated at least one landscape variable with genetic data. We systematically reviewed this set of papers to assess taxonomic and temporal trends in: (i) geographic regions studied; (ii) types of questions addressed; (iii) molecular markers used; (iv) statistical analyses used; and (v) types and nature of spatial data used. Overall, studies have occurred in geographic regions proximal to developed countries and more commonly in terrestrial vs. aquatic habitats. Questions most often focused on effects of barriers and/or landscape variables on gene flow. The most commonly used molecular markers were microsatellites and amplified fragment length polymorphism (AFLPs), with AFLPs used more frequently in plants than animals. Analysis methods were dominated by Mantel and assignment tests. We also assessed differences among journals to evaluate the uniformity of reporting and publication standards. Few studies presented an explicit study design or explicit descriptions of spatial extent. While some landscape variables such as topographic relief affected most species studied, effects were not universal, and some species appeared unaffected by the landscape. Effects of habitat fragmentation were mixed, with some species altering movement paths and others unaffected. Taken together, although some generalities emerged regarding effects of specific landscape variables, results varied, thereby reinforcing the need for species-specific work. We conclude by: highlighting gaps in knowledge and methodology, providing guidelines to authors and reviewers of landscape genetics studies, and suggesting promising future directions of inquiry.

Quantifying Bufo boreas connectivity in Yellowstone National Park with landscape genetics.

A major objective of ecology is to understand how ecological processes limit population connectivity and species' distributions. By spatially quantifying ecological components driving functional connectivity, we can understand why some locally suitable habitats are unoccupied, resulting in observed discontinuities in distribution. However, estimating connectivity may be difficult due to population stochasticity and violations of assumptions of parametric statistics. To address these issues, we present a novel application of Random Forests to landscape genetic data. We address the effects of three key ecological components on Bufo boreas connectivity in Yellowstone National Park: ecological process, scale, and hierarchical organization. Habitat permeability, topographic morphology, and temperature-moisture regime are all significant ecological processes associated with B. boreas connectivity. Connectivity was influenced by growing-season precipitation, 1988 Yellowstone fires, cover, temperature, impervious surfaces (roads and development), and topographic complexity (56% variation explained). We found that habitat permeability generally operates on fine scales, while topographic morphology and temperature-moisture regime operate across multiple scales, thus demonstrating the importance of cross-scale analysis for ecological interpretation. In a hierarchical analysis, we were able to explain more variation within genetic clusters as identified using Structure (a Bayesian algorithm) (74%; dispersal cover, growing-season precipitation, impervious surfaces) as opposed to between genetic clusters (45%; ridgelines, hot, dry slopes, length of hot season, and annual precipitation). Finally, the analytical methods we developed are powerful and can be applied to any species or system with appropriate landscape and genetic data.

Navigating fragmented landscapes: Canada lynx brave poor quality habitats while traveling.

Anthropogenic and natural habitat fragmentation inhibit movement of animals through landscapes. An important challenge for connectivity conservation is determining which conditions facilitate or limit movements, so that these areas can be prioritized for protection or restoration. We examine Canada lynx Lynx canadensis habitat connectivity in the fragmented North Cascade Mountains of Washington, as an example of a highly mobile species that is specialized both on prey and in habitat needs. We identify lynx Habitat Concentration Areas based on Core Habitat Models, parameterize resistance surfaces from our Matrix Habitat Model, and develop linkages of habitat lynx use to move between patches of high quality habitat. We identify a number of linkages for lynx comprised of habitat conditions that differed from high quality core patches identified from our habitat modeling. Radio-locations from lynx confirm lower-quality habitats of low resistance to movement were used by traveling lynx. Our results thus suggest traveling lynx do indeed use a much broader range of habitats than do lynx moving within core areas. For lynx in the North Cascades, our results show that maintaining connectivity will require preserving habitats and linkages that would previously have been deemed unsuitable for lynx. Maintaining connectivity for lynx is particularly important given the many recent large wildfires in this region that have reduced the number of mature forest stands that form prime habitat for lynx. Policy implications. Our results strongly suggest that habitat connectivity models should be based on empirical information of animal location data and focused on matrix habitat analysis. Traveling predators use a wide suite of habitats, resulting in more and broader linkage zones that should inform conservation efforts. Failure to identify these areas of functional connectivity could result in the oversight of usable linkage zones, leaving them without protection and vulnerable to degradation.

Canada lynx use of burned areas: Conservation implications of changing fire regimes.

A fundamental problem in ecology is forecasting how species will react to major disturbances. As the climate warms, large, frequent, and severe fires are restructuring forested landscapes at large spatial scales, with unknown impacts on imperilled predators. We use the United States federally Threatened Canada lynx as a case study to examine how predators navigate recent large burns, with particular focus on habitat features and the spatial configuration (e.g., distance to edge) that enabled lynx use of these transformed landscapes. We coupled GPS location data of lynx in Washington in an area with several recent large fires and a number of GIS layers of habitat data to develop models of lynx habitat selection in recent burns. Random Forest habitat models showed lynx-selected islands of forest skipped by large fires, residual vegetation, and areas where some trees survived to use newly burned areas. Lynx used burned areas as early as 1 year postfire, which is much earlier than the 2-4 decades postfire previously thought for this predator. These findings are encouraging for predator persistence in the face of fires, but increasingly severe fires or management that reduces postfire residual trees or slow regeneration will likely jeopardize lynx and other predators. Fire management should change to ensure heterogeneity is retained within the footprint of large fires to enable viable predator populations as fire regimes worsen with climate change.

Complementary Network-Based Approaches for Exploring Genetic Structure and Functional Connectivity in Two Vulnerable, Endemic Ground Squirrels.

The persistence of small populations is influenced by genetic structure and functional connectivity. We used two network-based approaches to understand the persistence of the northern Idaho ground squirrel (Urocitellus brunneus) and the southern Idaho ground squirrel (U. endemicus), two congeners of conservation concern. These graph theoretic approaches are conventionally applied to social or transportation networks, but here are used to study population persistence and connectivity. Population graph analyses revealed that local extinction rapidly reduced connectivity for the southern species, while connectivity for the northern species could be maintained following local extinction. Results from gravity models complemented those of population graph analyses, and indicated that potential vegetation productivity and topography drove connectivity in the northern species. For the southern species, development (roads) and small-scale topography reduced connectivity, while greater potential vegetation productivity increased connectivity. Taken together, the results of the two network-based methods (population graph analyses and gravity models) suggest the need for increased conservation action for the southern species, and that management efforts have been effective at maintaining habitat quality throughout the current range of the northern species. To prevent further declines, we encourage the continuation of management efforts for the northern species, whereas conservation of the southern species requires active management and additional measures to curtail habitat fragmentation. Our combination of population graph analyses and gravity models can inform conservation strategies of other species exhibiting patchy distributions.

Changing climate mediates sapsucker (Aves: Sphyrapicus) hybrid zone movement.

Hybrid zones, where two divergent taxa meet and interbreed, offer unique opportunities to investigate how climate contributes to reproductive isolation between closely related taxa and how these taxa may respond to climatic changes. Red-naped (Sphyrapicus nuchalis) and Red-breasted (Sphyrapicus ruber) sapsuckers (Aves: Picidae) hybridize along a narrow contact zone that stretches from northern California to British Columbia. The hybrid zone between these species has been studied extensively for more than 100 years and represents an excellent system for investigations of the evolution of reproductive isolation. Shifts in the proportions of phenotypes at hybrid localities since 1910 that were inferred using specimens from museum collections were confirmed using species distribution models. We predicted the historical, current, and future distributions of parental and hybrid sapsuckers using Random Forests models to quantify how climate change is affecting hybrid zone movement in the Pacific Northwest. We found observed distribution shifts of parental sapsuckers were likely the result of climate change over the past 100 years, with these shifts predicted to continue for both sapsuckers over the next 80 years. We found Red-breasted Sapsuckers are predicted to continue to expand, while Red-naped Sapsuckers are predicted to contract substantially under future climate scenarios. As a result of the predicted changes, the amount of overlap in the distribution of these sapsuckers may decrease. Using hybrid phenotypes, we found the climate niche occupied by the hybrid zone is predicted to disappear under future conditions. The disappearance of this climate niche where the two parental species come into contact and hybridize may lead to a substantial reduction in genetic introgression. Understanding the impacts of global climate change on hybrid zones may help us to better understand how speciation has been shaped by climate in the past, as well as how evolution may respond to climate change in the future.

Effects of changing climate on aquatic habitat and connectivity for remnant populations of a wide-ranging frog species in an arid landscape.

Amphibian species persisting in isolated streams and wetlands in desert environments can be susceptible to low connectivity, genetic isolation, and climate changes. We evaluated the past (1900-1930), recent (1981-2010), and future (2071-2100) climate suitability of the arid Great Basin (USA) for the Columbia spotted frog (Rana luteiventris) and assessed whether changes in surface water may affect connectivity for remaining populations. We developed a predictive model of current climate suitability and used it to predict the historic and future distribution of suitable climates. We then modeled changes in surface water availability at each time period. Finally, we quantified connectivity among existing populations on the basis of hydrology and correlated it with interpopulation genetic distance. We found that the area of the Great Basin with suitable climate conditions has declined by approximately 49% over the last century and will likely continue to decline under future climate scenarios. Climate conditions at currently occupied locations have been relatively stable over the last century, which may explain persistence at these sites. However, future climates at these currently occupied locations are predicted to become warmer throughout the year and drier during the frog's activity period (May - September). Fall and winter precipitation may increase, but as rain instead of snow. Earlier runoff and lower summer base flows may reduce connectivity between neighboring populations, which is already limited. Many of these changes could have negative effects on remaining populations over the next 50-80 years, but milder winters, longer growing seasons, and wetter falls might positively affect survival and dispersal. Collectively, however, seasonal shifts in temperature, precipitation, and stream flow patterns could reduce habitat suitability and connectivity for frogs and possibly other aquatic species inhabiting streams in this arid region.

How spatio-temporal habitat connectivity affects amphibian genetic structure.

Heterogeneous landscapes and fluctuating environmental conditions can affect species dispersal, population genetics, and genetic structure, yet understanding how biotic and abiotic factors affect population dynamics in a fluctuating environment is critical for species management. We evaluated how spatio-temporal habitat connectivity influences dispersal and genetic structure in a population of boreal chorus frogs (Pseudacris maculata) using a landscape genetics approach. We developed gravity models to assess the contribution of various factors to the observed genetic distance as a measure of functional connectivity. We selected (a) wetland (within-site) and (b) landscape matrix (between-site) characteristics; and (c) wetland connectivity metrics using a unique methodology. Specifically, we developed three networks that quantify wetland connectivity based on: (i) P. maculata dispersal ability, (ii) temporal variation in wetland quality, and (iii) contribution of wetland stepping-stones to frog dispersal. We examined 18 wetlands in Colorado, and quantified 12 microsatellite loci from 322 individual frogs. We found that genetic connectivity was related to topographic complexity, within- and between-wetland differences in moisture, and wetland functional connectivity as contributed by stepping-stone wetlands. Our results highlight the role that dynamic environmental factors have on dispersal-limited species and illustrate how complex asynchronous interactions contribute to the structure of spatially-explicit metapopulations.

The influence of diet on faecal DNA amplification and sex identification in brown bears (Ursus arctos).

To evaluate the influence of diet on faecal DNA amplification, 11 captive brown bears (Ursus arctos) were placed on six restricted diets: grass (Trifolium spp., Haplopappus hirtus and Poa pratensis), alfalfa (Lupinus spp.), carrots (Daucus spp.), white-tailed deer (Odocoileus virginianus), blueberries (Vaccinium spp.) and salmon (Salmo spp.). DNA was extracted from 50 faecal samples of each restricted diet, and amplification of brown bear DNA was attempted for a mitochondrial DNA (mtDNA) locus and nuclear DNA (nDNA) locus. For mtDNA, no significant differences were observed in amplification success rates across diets. For nDNA, amplification success rates for salmon diet extracts were significantly lower than all other diet extracts (P < 0.001). To evaluate the accuracy of faecal DNA sex identification when female carnivores consume male mammalian prey, female bears were fed male white-tailed deer. Four of 10 extracts amplified, and all extracts were incorrectly scored as male due to amplification of X and Y-chromosome fragments. The potential biases highlighted in this study have broad implications for researchers using faecal DNA for individual and sex identification, and should be evaluated in other species.