Sex-specific behavioural patterns significantly affect the phylogeographic process of secondary contact in the red fox: male dispersibility and female philopatry

Abstract

Secondary contact is a key evolutionary event in understanding biodiversity formation. Elucidating the spatiotemporal effects of sex-specific behavioural patterns on gene flow associated with secondary contact provides valuable perspectives into population dynamics of organisms. The red fox (Vulpes vulpes) is highly dispersible and adaptable, possessing the broadest natural distribution range among the Carnivora. The Hondo red fox (V. v. japonica) is an endemic subspecies inhabiting three predominant islands of the Japanese Archipelago and is believed to have experienced secondary contact between eastern and western ancestral populations after the Last Glacial. Because their dispersal patterns exhibit sexual dimorphism characterised by male mobility and female philopatry, patrilineal and matrilineal genes are expected to reflect different aspects of the distributional fusion process. Here, we estimated the phylogeographic structure based on 11 Y-chromosome-specific microsatellite loci using 50 males and compared it to that based on mitochondrial DNA (mtDNA) sequences from 153 individuals. The phylogeny of Y-chromosomal DNA (yDNA) diverged into two clades with a high support rate and was analogous to that of mtDNA. However, no phylogeographic pattern was observed in yDNA, unlike mtDNA, which exhibited a distinct east–west structuring. In contrast to mtDNA clades, both yDNA clades were distributed across the three islands. These findings indicate that secondary contact of paternal lineages progressed earlier (prior to island segmentation through marine transgression in the post-glacial stage) and more broadly than that of maternal lineages. Historical east–west vicariance probably isolated not only females but also males over a long duration, resulting in similar phylogenetic divergence between yDNA and mtDNA. Subsequently, male-biased dispersal likely enhanced gene flow between the ancestral populations, whereas female natal philopatry restricted it. This study offers crucial insights into the evolutionary dynamics of terrestrial mammals with sex-specific life histories and underscores the significance of incorporating multifaceted markers in phylogeographic studies.