Multisource noninvasive genetics of brown bears (Ursus arctos) in Greece reveals a highly structured population and a new matrilineal contact zone in southern Europe

Abstract

In human‐dominated landscapes, connectivity is crucial for maintaining demographically stable mammalian populations. Here, we provide a comprehensive noninvasive genetic study for the brown bear population in the Hellenic Peninsula. We analyze its population structuring and connectivity, estimate its population size throughout its distribution, and describe its phylogeography in detail for the first time. Our results, based on 150 multilocus genotypes and on 244‐bp sequences of the mtDNA control region, show the population is comprised by three highly differentiated genetic clusters, consistent with geographical populations of Pindos, Peristeri, and Rhodope. By detecting two male bears with Rhodopean ancestry in the western demes, we provide strong evidence for the ongoing genetic connectivity of the geographically fragmented eastern and western distributions, which suggests connectivity of the larger East Balkan and Pindos‐Dinara populations. Total effective population size ( N e ) was estimated to be 199 individuals, and total combined population size ( N C ) was 499, with each cluster showing a relatively high level of genetic variability, suggesting that migration has been sufficient to counteract genetic erosion. The mtNDA results were congruent with the microsatellite data, and the three genetic clusters were matched predominantly with an equal number of mtDNA haplotypes that belong to the brown bear Western mitochondrial lineage (Clade 1), with two haplotypes being globally new and endemic. The detection of a fourth haplotype that belongs to the Eastern lineage (Clade 3a1) in three bears from the western distribution places the southernmost secondary contact zone between the Eastern and Western lineages in Greece and generates new hypotheses about postglacial maxima migration routes. This work indicates that the genetic composition and diversity of Europe's low‐latitude fringe population are the outcome of ancient and historical events and highlight its importance for the connectivity and long‐term persistence of the species in the Balkans.

Genetic Analysis and Status of Brown Bear Sub-Populations in Three National Parks of Greece Functioning as Strongholds for the Species’ Conservation

“…Regarding the 65 unique bears found in Pindos, our findings show that they are characterized by relatively high genetic diversity and low values for Fis in the majority of loci. This declares a low inbreeding level of the population, which agrees with some of the previous studies [ 9 , 26 ] that are shown in Table 10 . Therefore, high genetic diversity combined with low inbreeding coefficient and relatively high Nc/Ne ratio, shows that the bear population in Pindos NP is not currently threatened by genetic instability [ 26 ].…”

“…To our knowledge, this is the first study that includes bears from the overall area of Prespa National Park (MBPNP), but there are studies that have conducted genetic analysis of bears from regions close or part of MBPNP (e.g., Peristeri, Kastoria, Amyntaio) [ 6 , 9 , 59 ]. Based on the genetic data produced from this study we found that in the Prespa population the microsatellite loci are informative for the estimation of the population size and we can use them for the analysis of genetic variance (PIC > 0.5).…”

“…Regarding the genetic diversity, the census population size (Nc) and the effective population size (Ne), our findings agree with some previous studies [ 6 , 59 ]. Based on our genetic data retrieved from the 53 samples of this region, we estimated that the census population size (Nc) of the brown bear population of Prespa NP consists of 191 individuals, while Pylidis et al found 109 individuals based on analysis of 30 samples received from Peristeri mountain, a mountain massif adjacent at the eastern border of Prespa lake basin [ 9 ].…”

“…The Pindos/Peristeri bear population comprises two geographical sub-nuclei populations: one is located in the Peristeri range, including Prespa NP, and the other in the main mountain range of Pindos (North Pindos and Central–Southern Pindos [ 4 ]). They are all connected to the bear populations of Albania and North Macedonia, while the Rhodopi population is connected to the East Balkan population in Bulgaria [ 7 , 8 , 9 ]. A variety of management and protection approaches has been suggested, in the context of a comprehensive human–bear conflict management plan, including measures relating to local communities’ property protection and compensation, habitat conservation, and bear population control [ 10 , 11 ].…”

Noninvasive Genetics Knowledge from the Brown Bear Populations to Assist Biodiversity Conservation

“…Most of the genetic studies conducted on brown bear populations from Europe estimated the number of individuals, their density, and sex ratio to reveal the species' conservation status and distribution [69,81]. Some authors made assumptions and demonstrated the current need for connectivity between bear populations starting from these indicators [56,64,65,71,76,79,80,84,87,89,107] or the sex-biased philopatry [53,65,74,79,95,[156][157][158].…”