Molecular Ecology (2015) 24, 6041–6060 doi: 10.1111/mec.13448 Y chromosome haplotype distribution of brown bears (Ursus arctos) in Northern Europe provides insight into population history and recovery JULIA SCHREGEL,*† HANS GEIR EIKEN,* FINN AUDUN GRØNDAHL,‡ FRANK HAILER,§¶ JOUNI ASPI,** ILPO KOJOLA,†† KONSTANTIN TIRRONEN,‡‡ PIOTR DANILOV,‡‡ ALEXANDER RYKOV,§§ EUGENE POROSHIN,¶¶ AXEL JANKE,¶*** JON E. SWENSON†††† and SNORRE B. HAGEN* *Norwegian Institute of Bioeconomy Research, NIBIO – Svanhovd, 9925 Svanvik, Norway, †Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, 1432 As, Norway, ‡Randsfjordmuseene Ltd., Kongevegen 92, 2770 Jaren, Norway, §School of Biosciences, Cardiff University, Cardiff CF10 3AX, Wales, UK, ¶Biodiversity and Climate Research Centre (BiK-F), Senckenberg Gesellschaft fur€ Naturforschung, Senckenberganlage 25, 60325 Frankfurt am Main, Germany, **Department of Genetics and Physiology, University of Oulu, P.O. Box 3000, 90014 Oulu, Finland, ††Natural Resources Institute, P.O. Box 16, 96301 Rovaniemi, Finland, ‡‡Institute of Biology, Karelian Research Centre of the Russian Academy of Science, 185910 Petrozavodsk, Russian Federation, §§Pinezhsky Strict Nature Reserve, Pervomayskaja 123a, 164610 Pinega, Russian Federation, ¶¶Institute of Biology, Komi Research Centre of the Russian Academy of Science, 016761 Syktvkar, Russian Federation, ***Goethe University Frankfurt, Institute for Ecology, Evolution & Diversity, 60438 Frankfurt am Main, Germany, †††Norwegian Institute for Nature Research, 7485 Trondheim, Norway Abstract High-resolution, male-inherited Y-chromosomal markers are a useful tool for popula- tion genetic analyses of wildlife species, but to date have only been applied in this context to relatively few species besides humans. Using nine Y-chromosomal STRs and three Y-chromosomal single nucleotide polymorphism markers (Y-SNPs), we stud- ied whether male gene flow was important for the recent recovery of the brown bear (Ursus arctos) in Northern Europe, where the species declined dramatically in numbers and geographical distribution during the last centuries but is expanding now. We found 36 haplotypes in 443 male extant brown bears from Sweden, Norway, Finland and northwestern Russia. In 14 individuals from southern Norway from 1780 to 1920, we found two Y chromosome haplotypes present in the extant population as well as four Y chromosome haplotypes not present among the modern samples. Our results suggested major differences in genetic connectivity, diversity and structure between the eastern and the western populations in Northern Europe. In the west, our results indicated that the recovered population originated from only four male lineages, dis- playing pronounced spatial structuring suggestive of large-scale population size increase under limited male gene flow within the western subpopulation. In the east, we found a contrasting pattern, with high haplotype diversity and admixture. This first population genetic analysis of male brown bears shows conclusively that male gene flow was not the main force of population recovery. Keywords: gene flow, haplogroups, haplotypes, male dispersal, Y-SNP, Y-STR Received 17 April 2015; revision received 17 October 2015; accepted 26 October 2015 Introduction Correspondence: Julia Schregel and Snorre B. Hagen, Fax: +47 The genetic structure and diversity of a population are 78 99 56 00 and +47 78 99 56 00; E-mails: julia.schregel@nibio. greatly influenced by gene flow. A large number of no and [email protected] studies have shown that lack of immigration, and thus © 2015 John Wiley & Sons Ltd 6042 J. SCHREGEL ET AL. lack of gene flow from outside the population, can lead markers (Y-SNPs), especially in human studies (Karafet to a significant reduction of population viability (e.g. et al. 2008; Roewer et al. 2013; Larmuseau et al. 2014). Y- Dunn et al. 2011; Hedrick et al. 2014). The concept of SNPs have a slower mutation rate than Y-STRs and thus ‘genetic rescue’ is based on the prevention or reversal can form the phylogenetic backbone onto which the Y- of this situation, and an increase in gene flow has been STR haplotypes can be arranged (Jobling 2012). As such, shown to lead to higher fitness and demographic they can give insight into phylogenetic events that date growth (La Haye et al. 2012; Heber et al. 2013). Most back in time much longer than Y-STRs (Karafet et al. mammals display male-biased dispersal; that is, males 2008; Geppert et al. 2011; Wei et al. 2013) and represent a disperse farther and more frequently from the natal higher level of order than Y-STRs, whose phylogenetic home range than females. Therefore, males may display relationship with each other can be obscured, due to higher levels of gene flow among regions than females allele size homoplasy (Hailer & Leonard 2008). (Greenwood 1980), resulting in males generally exhibit- In wildlife species, population genetic studies using ing a weaker spatial genetic structure and a stronger Y-STRs are still rare, although a growing number of contribution to both genetic diversity within and phylogeographic and phylogenetic studies exist, such as genetic connectivity among populations than the for brown hares (Lepus europaeus) in Europe and Anato- females (Ishibashi et al. 2013; Quaglietta et al. 2013). lia (Mamuris et al. 2010), sheep (Ovis ssp.) (Meadows Thus, it can be hypothesized that in species with male- et al. 2006), colobine monkeys (Colobinae) (Roos et al. biased dispersal, males are responsible for 2011), or snow voles (genus: Chionomys) (Yannic et al. counteracting the effects of genetic drift and population 2012). Here, we apply high-resolution Y-chromosomal fragmentation, and therefore may play an important markers to assess the importance of male gene flow role in population recovery and demographic growth. during the recovery of a large terrestrial carnivore from However, this hypothesis has not been sufficiently eval- near extinction across its distribution range in Northern uated, partly because the male contribution to popula- Europe. All four large terrestrial carnivores, lynx (Lynx tion genetic connectivity, diversity, and structure is lynx), wolves (Canis lupus), wolverines (Gulo gulo), and poorly understood in most wildlife species. brown bears, declined dramatically in abundance and Previous studies have mostly assessed male gene flow geographical distribution during the last centuries, but either indirectly, by contrasting data on autosomal are recovering now and expanding into areas of previ- microsatellites [short tandem repeats (STRs)] and ous extirpation across Europe (Chapron et al. 2014). mtDNA (e.g. Baker et al. 2013; Hua et al. 2013; Ishibashi This ‘carnivore comeback’ provides an opportunity to et al. 2013) or by comparing male versus female genetic determine the role of genetic connectivity as population spatial autocorrelation (Banks & Peakall 2012). However, recovery proceeds (Hagen et al. 2015). For the study due to differences in marker systems (in the case of com- species, we used the brown bear (Ursus arctos) in North- parisons between mtDNA and autosomal markers) and ern Europe, owing to the pronounced male-biased dis- recombination of biparental markers, these approaches persal and female philopatry that has been documented only give an imprecise measure of the occurrence and in the species (McLellan & Hovey 2001; Støen et al. influence of male migration and gene flow. In contrast, 2005, 2006; Zedrosser et al. 2007a), which suggests that the analysis of male-inherited, Y-chromosomal variation connectivity among populations occurs primarily via enables the direct assessment of male gene flow indepen- male dispersal (Manel et al. 2004). Recently, using auto- dently of mtDNA and autosomal DNA variation (Hurles somal STRs, Kopatz et al. (2014) documented that the & Jobling 2001; Kayser et al. 2005; Roewer et al. 2005). In demographic recovery, that is the increase of popula- addition, being similar to autosomal STRs in terms of tion size after the bottleneck, of the brown bears in Fin- diversity, mutation rates, and methodological unambigu- land was supported by immigration from Russia, ity of allele designation (Hurles & Jobling 2001; Kayser whereas in Sweden and Norway, brown bear numbers et al. 2005; Roewer et al. 2005), Y-STRs can be applied to increased from near extinction without significant immi- answer similar questions regarding population structure gration of eastern bears. In addition, genetic connectiv- and connectivity at the same temporal and spatial reso- ity between the eastern (Finland, Russia) and western lution as autosomal STRs. Y-STRs have therefore been (Norway, Sweden) subpopulations (Fig. 1) of the North- increasingly used to investigate population genetic pro- ern European brown bear has been found to be low cesses both in humans (e.g. Rubicz et al. 2010; Salazar- (Schregel et al. 2012; Kopatz et al. 2014). These differen- Flores et al. 2010; Zupan et al. 2013; Tateno et al. 2014; tial recovery histories and the low connectivity between Karmin et al. 2015) and other primates (Langergraber the eastern and western parts of the species’ range offer et al. 2007; Schubert et al. 2011; Nietlisbach et al. 2012; an opportunity for applying Y-chromosomal markers to Inoue et al. 2013). Y-STRs are often combined with study the impact of male gene flow in the recovering Y-chromosomal single nucleotide polymorphism brown bear populations in Northern Europe. © 2015 John Wiley & Sons Ltd MALE GENE FLOW AND POPULATION