Isolation by distance, resistance and/or clusters? Lessons learned from a forest‐dwelling carnivore inhabiting a heterogeneous landscape

Abstract

Landscape genetics provides a valuable framework to understand how landscape features influence gene flow and to disentangle the factors that lead to discrete and/or clinal population structure. Here, we attempt to differentiate between these processes in a forest-dwelling small carnivore [European pine marten (Martes martes)]. Specifically, we used complementary analytical approaches to quantify the spatially explicit genetic structure and diversity and analyse patterns of gene flow for 140 individuals genotyped at 15 microsatellite loci. We first used spatially explicit and nonspatial Bayesian clustering algorithms to partition the sample into discrete clusters and evaluate hypotheses of 'isolation by barriers' (IBB). We further characterized the relationships between genetic distance and geographical ('isolation by distance', IBD) and ecological distances ('isolation by resistance', IBR) obtained from optimized landscape models. Using a reciprocal causal modelling approach, we competed the IBD, IBR and IBB hypotheses with each other to unravel factors driving population genetic structure. Additionally, we further assessed spatially explicit indices of genetic diversity using sGD across potentially overlapping genetic neighbourhoods that matched the inferred population structure. Our results revealed a complex spatial genetic cline that appears to be driven jointly by IBD and partial barriers to gene flow (IBB) associated with poor habitat and interspecific competition. Habitat loss and fragmentation, in synergy with past overharvesting and possible interspecific competition with sympatric stone marten (Martes foina), are likely the main factors responsible for the spatial genetic structure we observed. These results emphasize the need for a more thorough evaluation of discrete and clinal hypotheses governing gene flow in landscape genetic studies, and the potential influence of different limiting factors affecting genetic structure at different spatial scales.

Walking in a heterogeneous landscape: Dispersal, gene flow and conservation implications for the giant panda in the Qinling Mountains

“…In consequence, more and more landscape genetic studies employ this approach. However, the number of empirical studies that have fully adopted it remains few (but see Cushman & Landguth, ; Cushman et al., ; Yang, Cushman, Song, Yang, & Zhang, ; Ruiz‐Gonzalez et al., ). Taking into consideration the clear advantage of this approach, we promote wider awareness and application of multihypothesis approaches in landscape genetic research, especially on endangered species.…”

“…Such misinterpretation could compromise future management and conservation of populations involving, for example, in situ habitat restoration and the configuration of dispersal corridors. Against this background, a comprehensive analytical framework is required, which simultaneously investigates the effects of IBD, IBB and IBR (Cushman & Landguth, ; Cushman et al., ; Ruiz‐Gonzalez, Cushman, Madeira, Randi, & Gómez‐Moliner, ). This approach is of particular importance for natural populations of threatened species, which face complex spatial effects because of small population size (e.g., Allee effects), fragmented habitat and human‐induced disturbance.…”

Low genetic diversity and strong population structure shaped by anthropogenic habitat fragmentation in a critically endangered primate, Trachypithecus leucocephalus

“…The results of the spatial Bayesian clustering method GENE-LAND are in agreement with the genetic divergence between the FS and CZ populations, yet further divide the FS samples into JCS and BZ groups. GENELAND is one of the most powerful statistical methods of inferring genetic discontinuities and has shown high detection success rates within fewer generations following the establishment of barriers Ruiz-Gonzalez et al, 2015). High levels of genetic differentiation among the three subpopulations are supported by the large and significant pairwise F ST values (0.10-0.22) obtained using microsatellite data.…”

Landscape effects on the contemporary genetic structure of Ruffed Grouse (Bonasa umbellus) populations

“…Differences in landscape resistance and physical distance can both dictate patterns of gene flow (Ruiz-Gonzalez, Cushman, Madeira, Randi, & Gómez-Moliner, 2015). When landscape heterogeneity exists between populations, suitable dispersal routes become more complex.…”

“…When landscape heterogeneity exists between populations, suitable dispersal routes become more complex. Physical distance between populations can also act as a barrier by creating clinal genetic variation (Ruiz-Gonzalez et al, 2015), or isolation by distance (IBD), as species dispersal is as a function of geographic distance. For this reason, landscape heterogeneity within a species' range means patterns of isolation by resistance (IBR) are more likely to occur (Fontaine et al, 2007;McRae & Beier, 2007;Ruiz-Gonzalez et al, 2015).…”