Complete mitochondrial genomes and a novel spatial genetic method reveal cryptic phylogeographical structure and migration patterns among brown bears in north‐western Eurasia

Abstract

Aim Using sequences of complete mitochondrial genomes, our aims were: (1) to investigate the matrilineal phylogeographical structure, migration patterns and lineage coalescence times in a large, continuous population of brown bears (Ursus arctos); and (2) to develop a novel spatial genetic method to identify migration corridors and barriers. Location North‐western Eurasia: from eastern European Russia to the Baltic Sea. Methods We sequenced the complete mitochondrial genomes of 95 brown bears. The phylogeographical resolution of complete genomes was compared to that derived from subsets of the genome, including the most commonly used shorter sequences. We conducted network and Bayesian phylogeographical analyses and developed a novel, spatially explicit, individual‐based approach (called DResD) for identifying migration corridors and barriers. Results Analysis of mitogenome sequences revealed five haplogroups, specific to particular geographical areas, exhibiting far greater resolving power than shorter sequences. Estimated coalescence times for the haplogroups ranged from 7.7 to 15.2 ka, suggesting that their divergence took place after the last glaciation. We found several migration trends, including a large westward migration from eastern European Russia towards Finland. We also found evidence of a potential barrier and a migration corridor in the south‐west of the study area. Main conclusions The use of complete mitochondrial genomes from a brown bear population in north‐western Eurasia allowed us to identify phylogeographical structure, signatures of demographic history and spatial processes that had not previously been detected using shorter sequences. These findings have implications for studies on other species and populations, especially those exhibiting low mtDNA diversity. The relatively recent divergence estimates for haplogroups highlight the significance not only of the last glaciation but also of climatic fluctuations during the post‐glacial period for the divergence of mammal populations in Europe. Our spatial genetic method represents a new tool for the analysis of genetic data in a geographical context and is applicable to any data that yield genetic distance matrices, including microsatellites, amplified fragment length polymorphisms (AFLPs) and single‐nucleotide polymorphisms (SNPs).

Spatial Genetic Analyses Reveal Cryptic Population Structure and Migration Patterns in a Continuously Harvested Grey Wolf (Canis lupus) Population in North-Eastern Europe

“…The DResD procedure represents a recently developed spatially explicit, individual-based approach for identifying migration corridors and barriers [7]. It is a tool for the analysis of genetic data in a geographical context that is applicable to any data that yield genetic distance matrices, including sequence data, microsatellites, amplified fragment length polymorphisms (AFLPs) and single nucleotide polymorphisms (SNPs).…”

“…To identify potential regions of the study area that might represent corridors or barriers to migration, as well as core, transition and blending areas of population subgroups, we performed DResD analysis, which is a recently introduced spatially explicit, individual-based approach that is based on IBD modelling and pairwise geographic and genetic distances [7]. Genetic distance values were corrected for IBD, considering the spatial distances between pairs.…”

“…The resulting residual values were interpolated throughout the study area using distance weighting (w = 1/dist. ), based on the mid-locations of each sample pair (for a step-by-step guide to the DResD procedure, see Keis et al [7]). We aimed to identify geographic regions where genetic distance between individuals is significantly higher or lower than is expected from the effect of IBD alone (the null-model), representing possible migration barriers or corridors, respectively.…”

“…americanus ) make suitable study species for investigating large-scale spatial and temporal population processes in large carnivores. Spatial genetic analyses have demonstrated, for example, how results from population viability analyses of Mexican wolf ( Canis lupus baileyi ) can be combined with habitat data to develop quantitative recovery criteria for population connectivity [5]; they have also revealed important geographic mixing areas for different brown bear subpopulations [6], cryptic brown bear phylogeographical patterns [7], and have demonstrated the impacts of anthropogenic forces on the spatial genetic structure of black bear populations [8]. Although a set of methodological approaches have been developed in spatial genetics over the last decade (reviewed in 9), the field would benefit from further conceptual and methodological advancement.…”

Brown and Polar Bear Y Chromosomes Reveal Extensive Male-Biased Gene Flow within Brother Lineages

“…Polar bears exhibit low levels of population differentiation at biparentally inherited and mitochondrial markers throughout their range (Paetkau et al 1999;Cronin and MacNeil 2012;Miller et al 2012;Campagna et al 2013). Brown bears, in contrast, show considerable phylogeographic structuring at mitochondrial markers (Davison et al 2011;Edwards et al 2011;Hirata et al 2013;Keis et al 2013), and population structuring can also be discerned at biparentally inherited microsatellites (Paetkau et al 1997;Tammeleht et al 2010;Kopatz et al 2012). Most mtDNA clades are confined to certain geographical regions and are not shared between continents, although one brown bear clade is widespread throughout Eurasia and extends into North America (Korsten et al 2009;Davison et al 2011).…”