Long-term sky islands generate highly divergent lineages of a narrowly distributed stream salamander (Pachyhynobius shangchengensis) in mid-latitude mountains of East Asia

Abstract

BackgroundClimate oscillation may have a profound effect on species distributions, gene flow patterns and population demography. In response to environmental change, those species restricted to montane habitats experienced expansions and contractions along elevation gradients, which can drive differentiation among sky islands.ResultsThe Shangcheng stout salamander (Pachyhynobius shangchengensis) is a cool stream amphibian restricted to high-elevation areas in the Dabie Mountains, East China. In the present study, we used mtDNA genes (Cyt b and ND2) of 193 individuals and 12 nuclear microsatellite loci genotyped on 370 individuals, representing 6 populations (JTX, KHJ, MW, TTZ, BYM and KJY) across the taxon’s distribution area, to investigate their genetic variation and evolutionary history of P. shangchengensis. Most populations showed unusually high levels of genetic diversity. Phylogenetic analyses revealed five monophyletic clades with divergence times ranging from 3.96 to 1.4 Mya. Accordingly, significant genetic differentiation was present between these populations. Bayesian skyline plot analyses provided that all populations underwent long-term population expansions since the last inter-glacial (0.13 Mya ~ 0.12 Mya). Msvar analyses found recent signals of population decline for two northern populations (JTX and KHJ) reflecting a strong bottleneck (approximately 15-fold decrease) during the mid-Holocene (about 6000 years ago). Ecological niche modelling has shown a discontinuity in suitable habitats for P. shangchengensis under different historical climatic conditions.ConclusionsOur results suggest that the niche conservatism of P. shangchengensis and sky island effects may have led to long-term isolation between populations. In sky island refuges, the mid-latitude Dabie Mountains have provided a long-term stable environment for P. shangchengensis, which has led to the accumulation of genetic diversity and has promoted genetic divergence.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1333-8) contains supplementary material, which is available to authorized users.

Effects of dispersal barriers and geographic distance on the genetic structure of a narrowly distributed frog in a spatially structured landscape

“…In this study, although O. tormota is a narrowly distributed species, each population still harbored relatively high levels of genetic diversity compared with other narrowly distributed amphibia (Table ), such as the Majorcan midwife toad ( Alytes muletensis ) in the mountainous regions of Majorca, red‐bellied newt ( Taricha rivularis ) in northern California in the United States, Sonoran tiger salamander ( Ambystoma mavortium stebbinsi ) in the San Pedro River of Arizona in the United States, Leora's stream salamander ( A. leorae ) in Iztaccihuatl‐Popocatepetl National Park of Mexico, Fourche Mountain salamander ( Plethodon fourchensis ) in the Ouachita Mountains of the central United States, and dwarf black‐bellied salamander ( Desmognathus folkertsi ) in the United States (Kraaijeveld‐Smit et al ., ; Shepard & Burbrink, ; Wooten, Camp & Rissler, ; Reilly et al ., ; Storfer et al ., ; Sunny et al ., ). In addition, the O. tormota genetic diversity was slightly lower than that of the Shangcheng stout salamander ( Pachyhynobius shangchengensis ) in the Dabie Mountains of eastern China and the Leishan spiny toad ( Leptobrachium leishanense ) in south‐western China, which were described having high genetic diversity (Zhang et al ., ; Pan et al ., ).…”

“…This phenomenon has also been observed in species from mid‐latitude Europe, such as the Maltese wall lizard ( Podarcis filfolensis ; Salvi et al ., ) and Italian wall lizard ( P. siculus ; Senczuk et al ., ). Our study further showed that some temperate species in mid‐latitude regions that are insensitive to environmental changes may have undergone attenuated glacial population contractions, or even experienced population expansion (Salvi et al ., ; Senczuk et al ., ; Pan et al ., ).…”

“…In this study, EBSP revealed that O. tormota experienced an effective population size expansion since 0.075 Mya and reached the largest population size around 0.017 Mya; this finding was also supported by the neutral tests, mismatch distribution analysis, and a star‐like network. The demographic expansion of O. tormota during this period is consistent with many species in East Asia, such as the Shangcheng stout salamander ( P. shangchengensis ; Pan et al ., ), Chinese bamboo partridge ( B. thoracica ; Huang et al ., ), Chinese hwamei ( Leucodioptron canorum ) (Li et al ., ), and tufted deer ( Elaphodus cephalophus ) (Sun et al ., ). This phenomenon has also been observed in species from mid‐latitude Europe, such as the Maltese wall lizard ( Podarcis filfolensis ; Salvi et al ., ) and Italian wall lizard ( P. siculus ; Senczuk et al ., ).…”

“…During the last million years, climatic changes associated with Pleistocene glacial cycles are thought to have caused montane species to expand and contract along altitudinal and latitudinal gradients, which led to current species distributions and interpopulation gene flow patterns (Hewitt, 2004;Zhou et al, 2010;Ikeda et al, 2017). However, among different animal groups, the influence of Pleistocene climate cycles on population demographics varied (Hewitt, 2004;Schmitt, 2007;Yan, Luo & Wu, 2011;Wang et al, 2015;Sun et al, 2016;Pan et al, 2019). For example, many organisms that are sensitive to environmental changes retreated to southern regions and recolonized their original northern ranges in response to the severe Pleistocene climate fluctuations, especially in Europe and North America (Hewitt, 2004;Schmitt, 2007;Huang et al, 2010;Ding et al, 2011;Sun et al, 2016); in contrast, insensitive species have similar original and present-day ranges (Li et al, 2009;Huang et al, 2010;Salvi et al, 2014;Sun et al, 2016;Senczuk et al, 2017;Pan et al, 2019).…”

“…East Asia is characterized by a mosaic of mountains and likely experienced a relatively mild Pleistocene climate (Rost, 1994;Weaver et al, 1998;Ju, Wang & Jiang, 2007). The climatic conditions in East Asia led to major differences in the magnitude and timing of historical climate impact on population demography of species endemic to this area (Li et al, 2009;Huang et al, 2010;Yan et al, 2013;Sun et al, 2016;Pan et al, 2019). To further elucidate the impact of Pleistocene climate change on population fluctuations of East Asian species, especially amphibians with narrow distributions, further studies on population demography of montane species in this region are needed.…”