Jeffrey R. Row

Dispersal promotes high gene flow among Canada lynx populations across mainland North America

The amount and extent of dispersal can have a large effect on the evolutionary trajectory, dynamics and structure of populations. Thus, understanding patterns of genetic structure provide information about the needs and approaches for population management and species conservation. To date studies addressing the population structure of Canada lynx (Lynx canadensis) have been surprisingly equivocal, despite a large amount of research quantifying population cyclicity and synchrony and the species’ species at-risk status in the contiguous United States and eastern provinces of Canada. Here we use 17 microsatellite loci to conduct a large-scale genetic structuring assessment for Canada lynx, including most of its geographic range from Alaska to Newfoundland. We found large differentiation between lynx populations on the island of Newfoundland and those on the mainland. Yet, contrary to previous studies we found little genetic differentiation (FST, Dest, RST) owing to the Rocky Mountains, but some evidence of a subtle gene flow restriction between Ontario and Manitoba as previously proposed to be the result of a climatic barrier. Bayesian clustering analysis, however, only suggested two genetic clusters, one consisting of lynx from Newfoundland, and the other consisting of lynx from the rest of the North American range. Because Canada lynx are harvested for fur across most of their range, our results are informative for effective management strategies (e.g., defining management units) aimed at ensuring long-term population connectivity and species persistence.

Intense harvesting of eastern wolves facilitated hybridization with coyotes

Despite ethical arguments against lethal control of wildlife populations, culling is routinely used for the management of predators, invasive or pest species, and infectious diseases. Here, we demonstrate that culling of wildlife can have unforeseen impacts that can be detrimental to future conservation efforts. Specifically, we analyzed genetic data from eastern wolves (Canis lycaon) sampled in Algonquin Provincial Park (APP), Ontario, Canada from 1964 to 2007. Research culls in 1964 and 1965 killed the majority of wolves within a study region of APP, accounting for approximately 36% of the parks wolf population at a time when coyotes were colonizing the region. The culls were followed by a significant decrease in an eastern wolf mitochondrial DNA (mtDNA) haplotype (C1) in the Parks wolf population, as well as an increase in coyote mitochondrial and nuclear DNA. The introgression of nuclear DNA from coyotes, however, appears to have been curtailed by legislation that extended wolf protection outside park boundaries in 2001, although eastern wolf mtDNA haplotype C1 continued to decline and is now rare within the park population. We conclude that the wolf culls transformed the genetic composition of this unique eastern wolf population by facilitating coyote introgression. These results demonstrate that intense localized harvest of a seemingly abundant species can lead to unexpected hybridization events that encumber future conservation efforts. Ultimately, researchers need to contemplate not only the ethics of research methods, but also that future implications may be obscured by gaps in our current scientific understanding.

Landscape characteristics influencing the genetic structure of greater sage-grouse within the stronghold of their range: a holistic modeling approach.

Given the significance of animal dispersal to population dynamics and geographic variability, understanding how dispersal is impacted by landscape patterns has major ecological and conservation importance. Speaking to the importance of dispersal, the use of linear mixed models to compare genetic differentiation with pairwise resistance derived from landscape resistance surfaces has presented new opportunities to disentangle the menagerie of factors behind effective dispersal across a given landscape. Here, we combine these approaches with novel resistance surface parameterization to determine how the distribution of high- and low-quality seasonal habitat and individual landscape components shape patterns of gene flow for the greater sage-grouse (Centrocercus urophasianus) across Wyoming. We found that pairwise resistance derived from the distribution of low-quality nesting and winter, but not summer, seasonal habitat had the strongest correlation with genetic differentiation. Although the patterns were not as strong as with habitat distribution, multivariate models with sagebrush cover and landscape ruggedness or forest cover and ruggedness similarly had a much stronger fit with genetic differentiation than an undifferentiated landscape. In most cases, landscape resistance surfaces transformed with 17.33-km-diameter moving windows were preferred, suggesting small-scale differences in habitat were unimportant at this large spatial extent. Despite the emergence of these overall patterns, there were differences in the selection of top models depending on the model selection criteria, suggesting research into the most appropriate criteria for landscape genetics is required. Overall, our results highlight the importance of differences in seasonal habitat preferences to patterns of gene flow and suggest the combination of habitat suitability modeling and linear mixed models with our resistance parameterization is a powerful approach to discerning the effects of landscape on gene flow.

The subtle role of climate change on population genetic structure in Canada lynx

Anthropogenically driven climatic change is expected to reshape global patterns of species distribution and abundance. Given recent links between genetic variation and environmental patterns, climate change may similarly impact genetic population structure, but we lack information on the spatial and mechanistic underpinnings of genetic-climate associations. Here, we show that current genetic variability of Canada lynx (Lynx canadensis) is strongly correlated with a winter climate gradient (i.e. increasing snow depth and winter precipitation from west-to-east) across the Pacific-North American (PNO) to North Atlantic Oscillation (NAO) climatic systems. This relationship was stronger than isolation by distance and not explained by landscape variables or changes in abundance. Thus, these patterns suggest that individuals restricted dispersal across the climate boundary, likely in the absence of changes in habitat quality. We propose habitat imprinting on snow conditions as one possible explanation for this unusual phenomenon. Coupling historical climate data with future projections, we also found increasingly diverging snow conditions between the two climate systems. Based on genetic simulations using projected climate data (2041-2070), we predicted that this divergence could lead to a threefold increase in genetic differentiation, potentially leading to isolated east-west populations of lynx in North America. Our results imply that subtle genetic structure can be governed by current climate and that substantive genetic differentiation and related ecological divergence may arise from changing climate patterns.

Developing approaches for linear mixed modeling in landscape genetics through landscape‐directed dispersal simulations

Abstract Dispersal can impact population dynamics and geographic variation, and thus, genetic approaches that can establish which landscape factors influence population connectivity have ecological and evolutionary importance. Mixed models that account for the error structure of pairwise datasets are increasingly used to compare models relating genetic differentiation to pairwise measures of landscape resistance. A model selection framework based on information criteria metrics or explained variance may help disentangle the ecological and landscape factors influencing genetic structure, yet there are currently no consensus for the best protocols. Here, we develop landscape‐directed simulations and test a series of replicates that emulate independent empirical datasets of two species with different life history characteristics (greater sage‐grouse; eastern foxsnake). We determined that in our simulated scenarios, AIC and BIC were the best model selection indices and that marginal R 2 values were biased toward more complex models. The model coefficients for landscape variables generally reflected the underlying dispersal model with confidence intervals that did not overlap with zero across the entire model set. When we controlled for geographic distance, variables not in the underlying dispersal models (i.e., nontrue) typically overlapped zero. Our study helps establish methods for using linear mixed models to identify the features underlying patterns of dispersal across a variety of landscapes.

Anatomy of a population cycle: the role of density dependence and demographic variability on numerical instability and periodicity

Determining the causes of cyclic fluctuations in population size is a central tenet in population ecology and provides insights into population regulatory mechanisms. We have a firm understanding of how direct and delayed density dependence affects population stability and cyclic dynamics, but there remains considerable uncertainty in the specific processes contributing to demographic variability and consequent change in cyclic propensity. Spatiotemporal variability in cyclic propensity, including recent attenuation or loss of cyclicity among several temperate populations and the implications of habitat fragmentation and climate change on this pattern, highlights the heightened need to understand processes underlying cyclic variation. Because these stressors can differentially impact survival and productivity and thereby impose variable time delays in density dependence, there is a specific need to elucidate how demographic vital rates interact with the type and action of density dependence to contribute to population stability and cyclic variation. Here, we address this knowledge gap by comparing the stability of time series derived from general and species-specific (Canada lynx: Lynx canadensis; small rodents: Microtus, Lemmus and Clethrionomys spp.) matrix population models, which vary in their demographic rates and the direct action of density dependence. Our results reveal that density dependence acting exclusively on survival as opposed to productivity is destabilizing, suggesting that a shift in the action of population regulation toward reproductive output may decrease cyclic propensity and cycle amplitude. This result was the same whether delayed density dependence was pulsatile and acted on a single time period (e.g. t-1, t-2 or t-3) vs. more constant by affecting a successive range of years (e.g. t-1,…, t-3). Consistent with our general models, reductions in reproductive potential in both the lynx and small rodent systems led to notably large drops in cyclic propensity and amplitude, suggesting that changes in this vital rate may contribute to the spatial or temporal variability observed in the cyclic dynamics of both systems. Collectively, our results reveal that the type of density dependence and its effect on different demographic parameters can profoundly influence numeric stability and cyclic propensity and therefore may shift populations across the cyclic-to-noncyclic boundary.

Continental divide: Predicting climate-mediated fragmentation and biodiversity loss in the boreal forest

Climate change threatens natural landscapes through shifting distribution and abundance of species and attendant change in the structure and function of ecosystems. However, it remains unclear how climate-mediated variation in species’ environmental niche space may lead to large-scale fragmentation of species distributions, altered meta-population dynamics and gene flow, and disrupted ecosystem integrity. Such change may be especially relevant when species distributions are restricted either spatially or to a narrow environmental niche, or when environments are rapidly changing. Here, we use range-wide environmental niche models to posit that climate-mediated range fragmentation aggravates the direct effects of climate change on species in the boreal forest of North America. We show that climate change will directly alter environmental niche suitability for boreal-obligate species of trees, birds and mammals (n = 12), with most species ranges becoming smaller and shifting northward through time. Importantly, species distributions will become increasingly fragmented, as characterized by smaller mean size and greater isolation of environmentally-suitable landscape patches. This loss is especially pronounced along the Ontario-Québec border, where the boreal forest is narrowest and roughly 78% of suitable niche space could disappear by 2080. Despite the diversity of taxa surveyed, patterns of range fragmentation are remarkably consistent, with our models predicting that spruce grouse (Dendragapus canadensis), boreal chickadee (Poecile hudsonicus), moose (Alces americanus) and caribou (Rangifer tarandus) could have entirely disjunct east-west population segments in North America. These findings reveal potentially dire consequences of climate change on population continuity and species diversity in the boreal forest, highlighting the need to better understand: 1) extent and primary drivers of anticipated climate-mediated range loss and fragmentation; 2) diversity of species to be affected by such change; 3) potential for rapid adaptation in the most strongly-affected areas; and 4) potential for invasion by replacement species.

The genetic network of greater sage-grouse: Range-wide identification of keystone hubs of connectivity

Abstract Genetic networks can characterize complex genetic relationships among groups of individuals, which can be used to rank nodes most important to the overall connectivity of the system. Ranking allows scarce resources to be guided toward nodes integral to connectivity. The greater sage‐grouse (Centrocercus urophasianus) is a species of conservation concern that breeds on spatially discrete leks that must remain connected by genetic exchange for population persistence. We genotyped 5,950 individuals from 1,200 greater sage‐grouse leks distributed across the entire species’ geographic range. We found a small‐world network composed of 458 nodes connected by 14,481 edges. This network was composed of hubs—that is, nodes facilitating gene flow across the network—and spokes—that is, nodes where connectivity is served by hubs. It is within these hubs that the greatest genetic diversity was housed. Using indices of network centrality, we identified hub nodes of greatest conservation importance. We also identified keystone nodes with elevated centrality despite low local population size. Hub and keystone nodes were found across the entire species’ contiguous range, although nodes with elevated importance to network‐wide connectivity were found more central: especially in northeastern, central, and southwestern Wyoming and eastern Idaho. Nodes among which genes are most readily exchanged were mostly located in Montana and northern Wyoming, as well as Utah and eastern Nevada. The loss of hub or keystone nodes could lead to the disintegration of the network into smaller, isolated subnetworks. Protecting both hub nodes and keystone nodes will conserve genetic diversity and should maintain network connections to ensure a resilient and viable population over time. Our analysis shows that network models can be used to model gene flow, offering insights into its pattern and process, with application to prioritizing landscapes for conservation.

Selection and drift influence genetic differentiation of insular Canada lynx (Lynx canadensis) on Newfoundland and Cape Breton Island

Abstract Island populations have long been important for understanding the dynamics and mechanisms of evolution in natural systems. While genetic drift is often strong on islands due to founder events and population bottlenecks, the strength of selection can also be strong enough to counteract the effects of drift. Here, we used several analyses to identify the roles of genetic drift and selection on genetic differentiation and diversity of Canada lynx (Lynx canadensis) across eastern Canada, including the islands of Cape Breton and Newfoundland. Specifically, we assessed whether we could identify a genetic component to the observed morphological differentiation that has been reported across insular and mainland lynx. We used a dinucleotide repeat within the promoter region of a functional gene that has been linked to mammalian body size, insulin‐like growth factor‐1 (IGF‐1). We found high genetic differentiation at neutral molecular markers but convergence of allele frequencies at the IGF‐1 locus. Thus, we showed that while genetic drift has influenced the observed genetic structure of lynx at neutral molecular markers, natural selection has also played a role in the observed patterns of genetic diversity at the IGF‐1 locus of insular lynx.

Tissue-specific transcriptome characterization for developing tadpoles of the northern leopard frog (Lithobates pipiens)

A potential cause of amphibian population declines are the impacts of environmental degradation on tadpole development. We conducted RNA sequencing on developing northern leopard frog tadpoles and through de novo transcriptome assembly we annotated a large number of open reading frames comparable in number and extent to genes identified in Xenopus. Using our transcriptome, we found transcript level changes between early (Gosner 26-31) and late (Gosner 36-41) stage tadpoles were the greatest in the tail, which is reabsorbed throughout development. There was an up-regulation of immunity genes in both the head and tail of the late tadpoles and a down-regulation of genes associated with the energy pathways of the mitochondria and the production of myosin. Overall, transcript level changes across development were consistent with studies on Xenopus and our findings highlight the broader utility of using RNA-seq to identify genes differentially expressed throughout development and in response to environmental pressures.