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

Abstract

Brown and polar bears have become prominent examples in phylogeography, but previous phylogeographic studies relied largely on maternally inherited mitochondrial DNA (mtDNA) or were geographically restricted. The male-specific Y chromosome, a natural counterpart to mtDNA, has remained underexplored. Although this paternally inherited chromosome is indispensable for comprehensive analyses of phylogeographic patterns, technical difficulties and low variability have hampered its application in most mammals. We developed 13 novel Y-chromosomal sequence and microsatellite markers from the polar bear genome and screened these in a broad geographic sample of 130 brown and polar bears. We also analyzed a 390-kb-long Y-chromosomal scaffold using sequencing data from published male ursine genomes. Y chromosome evidence support the emerging understanding that brown and polar bears started to diverge no later than the Middle Pleistocene. Contrary to mtDNA patterns, we found 1) brown and polar bears to be reciprocally monophyletic sister (or rather brother) lineages, without signals of introgression, 2) male-biased gene flow across continents and on phylogeographic time scales, and 3) male dispersal that links the Alaskan ABC islands population to mainland brown bears. Due to female philopatry, mtDNA provides a highly structured estimate of population differentiation, while male-biased gene flow is a homogenizing force for nuclear genetic variation. Our findings highlight the importance of analyzing both maternally and paternally inherited loci for a comprehensive view of phylogeographic history, and that mtDNA-based phylogeographic studies of many mammals should be reevaluated. Recent advances in sequencing technology render the analysis of Y-chromosomal variation feasible, even in nonmodel organisms.

High genetic variability of vagrant polar bears illustrates importance of population connectivity in fragmented sea ice habitats

“…This would decrease the likelihood that a subpopulation would receive novel genetic variants from immigrants. However, consistent with the high dispersal capability of polar bears, genetic differentiation among the 19 recognized subpopulations is low (Paetkau et al, 1999;Edwards et al, 2011;Miller et al, 2012b;Campagna et al, 2013;Bidon et al, 2014;Cronin et al, 2014;Malenfant, Coltman & Davis, 2015;Peacock et al, 2015). Further, a study that included data from 18 of the recognized subpopulations detected gene flow among clusters of subpopulations (Peacock et al, 2015).…”

“…1), including 41 blood or tissue samples from Chukchi Sea and Southern Beaufort Sea (divergent ecoregion) and from Baffin Bay and Davis Strait (seasonal ice ecoregion), four tissue samples from vagrant individuals reaching Iceland, and 13 DNA samples from Barents Sea (divergent ecoregion), Kane Basin (Archipelago ecoregion), eastern Greenland (convergent ecoregion), Baffin Bay, Alaska (Chukchi Sea and Southern Beaufort Sea), and from a captive animal with unclear geographic ancestry. In addition, we used previously published data from 112 individuals (Lindqvist et al, 2010;Hailer et al, 2012;Miller et al, 2012b;Campagna et al, 2013;Bidon et al, 2014) from Alaska and the Barents Sea (divergent ecoregion), and from Gulf of Boothia and M'Clintock Channel (Archipelago ecoregion) ( Fig. 1) that was collated from GenBank.…”

“…A hypervariable 681-bp fragment of the mitochondrial control region was already published for 51 of the 58 samples Bidon et al, 2014) (Table S1), the remaining seven individuals were sequenced (ENA accession numbers: LN613410-LN613416) as described in Hailer et al (2012). Primers and PCR conditions are listed in Table S2.…”

“…We used 3.1 kb of Y-specific sequence data and one Y-linked microsatellite marker (369.1) from 39 male polar bears (Bidon et al, 2014;Aarnes et al, 2015) to construct a statistical parsimony haplotype network in TCS 1.21 (Clement, Posada & Crandall, 2000). These individuals had previously been sexed, using the approach of Bidon et al (2013).…”

“…1). Our analyses are based on data from autosomal microsatellites, mitochondrial control region sequences, and Y-chromosomal sequence and microsatellite haplotypes, including previously published (Lindqvist et al, 2010;Hailer et al, 2012;Miller et al, 2012b;Campagna et al, 2013;Bidon et al, 2014) and newly generated data (the latter mainly to produce comparable microsatellite datasets, given known variation in allele sizes obtained from different instruments and size markers; e.g. Morin et al, 2009).…”