Mountains as barriers to gene flow in amphibians: Quantifying the differential effect of a major mountain ridge on the genetic structure of four sympatric species with different life history traits

Abstract

Aim To test the role of mountains as barriers to gene flow in co‐distributed taxa with different life history traits. Location Sierra de Guadarrama, Central Spain. Methods We used larval genotypes of four amphibian species (Epidalea calamita, Hyla molleri, Pelophylax perezi and Pelobates cultripes) sampled on northern and southern slopes of Sierra de Guadarrama to describe genetic structure with FST, migration rates per generation, clustering algorithms and resistance by elevation surfaces. We also recorded individual displacement events as a proxy of dispersal potential during a seven‐year monitoring project based on capture–mark–recapture (CMR). Results All species travelled longer cumulative distances than those reported in the study area for P. cultripes (0.71 km). Individuals of E. calamita travelled up to 3.55 km, followed by H. molleri (2.84 km) and P. perezi (1.51 km). Pairwise FST estimates showed lower overall connectivity in P. cultripes. Average migration rates per generation were low in all species, with exceptions in same‐slope populations of H. molleri and P. cultripes. Clustering algorithms consistently recovered well‐differentiated population groups of P. cultripes in northern versus southern slopes, but widely admixed areas were observed in the other species, especially near mountain passes. Resistance by elevation surfaces showed a strong barrier effect of Sierra de Guadarrama in P. cultripes and suggested a potential role of topography in the genetic structure of E. calamita and H. molleri. Main conclusions Sierra de Guadarrama currently acts as a strong barrier to gene flow for P. cultripes and, to a lesser extent, for E. calamita, H. molleri and P. perezi. This differential effect can be partly explained by differences in life history traits, including dispersal potential. Our findings support the general role of the Central System as a key feature shaping population connectivity and genetic variation in amphibian communities.

Isolation by resistance analysis reveals major barrier effect imposed by the Tsinling Mountains on the Chinese wood frog

“…While our results contradict the conclusions of Zhan et al (2009), they are consistent with a large body of literature that has implicated mountains in the obstruction of gene flow for amphibians (e.g. Funk et al, 2005;Spear et al, 2005;Garcia, Ivy & Fu, 2017;S anchez-Montes et al, 2018).…”

“…Roads and rivers have frequently been detected to impede amphibian dispersal (e.g. Lougheed et al , ; Crosby et al , ; Li et al , ), and perhaps more prominently, mountain ranges are considered significant genetic barriers and are assumed to be a major contributor to population structure in amphibians (Lougheed et al , ; Funk et al , ; Spear et al , ; Sánchez‐Montes et al , ).…”

“…Roads and rivers have frequently been detected to impede amphibian dispersal (e.g. Lougheed et al, 1999;Crosby et al, 2009;Li et al, 2009), and perhaps more prominently, mountain ranges are considered significant genetic barriers and are assumed to be a major contributor to population structure in amphibians (Lougheed et al, 1999;Funk et al, 2005;Spear et al, 2005;S anchez-Montes et al, 2018). Zhan, Li & Fu (2009) conducted a landscape genetic analysis of the Chinese wood frog (Rana chensinensis) in northwestern China, and surprisingly, they detected no significant barrier effect of the Tsinling Mountains, which is a major climatic and biogeographic divider in continental East Asia (Zhang, 2004).…”

Phylogeny of spiny frogs Nanorana (Anura: Dicroglossidae) supports a Tibetan origin of a Himalayan species group

“…Accordingly, as observed in birds, butterflies, and plants (e.g., Li et al, ; Manish & Pandit, ; Martens et al, ; Xie et al, ), all lineages of Himalayan spiny frogs recorded at present would have dispersed from east to west or would have appeared during the potential range expansion along the Greater Himalaya. Thus, they must have been able to cross the many north–south stretching mountain ranges and the epigenetic transverse valleys, by which the Himalaya has always been intersected and that might form effective barriers to dispersal of amphibians (Sánchez‐Montes, Wang, Ariño, & Martínez‐Solano, ; Zhou et al, ). Relating thereto, the phylogenetic placement of the clade from the NW Himalaya is of particular interest.…”

Diversification of African tree frogs (genus Leptopelis) in the highlands of Ethiopia

“…Finally, a role of ecology cannot be excluded. Recent studies have shown that fossorial species tend to have low dispersal abilities and smaller geographic distributions than nonfossorial frogs (Eggert, ; Penner & Rödel, ; Sánchez‐Montes, Wang, Ariño, & Martínez‐Solano, ; Székely, Cogălniceanu, Székely, & Denoël, ) and it is thus possible that fossoriality played a role in the limited distribution of the different linages in L. gramineus .…”