Dynamics behind disjunct distribution, hotspot-edge refugia, and discordant RADseq/mtDNA variability: insights from the Emei mustache toad

Abstract Background The distribution of genetic diversity and the underlying processes are important for conservation planning but are unknown for most species and have not been well studied in many regions. In East Asia, the Sichuan Basin and surrounding mountains constitute an understudied region...

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Main Authors: Yuchi Zheng, Qiang Dai, Xianguang Guo, Xiaomao Zeng
Format: Article
Language:English
Published: BMC 2020-08-01
Series:BMC Evolutionary Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12862-020-01675-8
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spelling doaj-c6046049fdb54925ada045eca5de40fa2021-09-02T15:43:35ZengBMCBMC Evolutionary Biology1471-21482020-08-0120111610.1186/s12862-020-01675-8Dynamics behind disjunct distribution, hotspot-edge refugia, and discordant RADseq/mtDNA variability: insights from the Emei mustache toadYuchi Zheng0Qiang Dai1Xianguang Guo2Xiaomao Zeng3Chengdu Institute of Biology, Chinese Academy of SciencesChengdu Institute of Biology, Chinese Academy of SciencesChengdu Institute of Biology, Chinese Academy of SciencesChengdu Institute of Biology, Chinese Academy of SciencesAbstract Background The distribution of genetic diversity and the underlying processes are important for conservation planning but are unknown for most species and have not been well studied in many regions. In East Asia, the Sichuan Basin and surrounding mountains constitute an understudied region that exhibits a “ring” of high species richness overlapping the eastern edge of the global biodiversity hotspot Mountains of Southwest China. We examine the distributional history and genetic diversification of the Emei mustache toad Leptobrachium boringii, a typical “ring” element characterized by disjunct ranges in the mountains, by integrating time-calibrated gene tree, genetic variability, individual-level clustering, inference of population splitting and mixing from allele frequencies, and paleoclimatic suitability modeling. Results The results reveal extensive range dynamics, including secondary contact after long-term isolation via westward dispersal accompanied by variability loss. They allow the proposal of a model that combines recurrent contractions caused by Quaternary climatic changes and some failed expansions under suitable conditions for explaining the shared disjunct distribution pattern. Providing exceptional low-elevation habitats in the hotspot area, the eastern edge harbors both long-term refugial and young immigrant populations. This finding and a synthesis of evidence from other taxa demonstrate that a certain contributor to biodiversity, one that preserves and receives low-elevation elements of the east in this case, can be significant for only a particular part of a hotspot. By clarifying the low variability of these refugial populations, we show that discordant mitochondrial estimates of diversity can be obtained for populations that experienced admixture, which would have unlikely left proportional immigrant alleles for each locus. Conclusions Dispersal after long-term isolation can explain much of the spatial distribution of genetic diversity in this species, while secondary contact and long-term persistence do not guarantee a large variation. The model for the formation of disjunct ranges may apply to many other taxa isolated in the mountains surrounding the Sichuan Basin. Furthermore, this study provides insights into the heterogeneous nature of hotspots and discordant variability obtained from genome-wide and mitochondrial data.http://link.springer.com/article/10.1186/s12862-020-01675-8Sichuan BasinLeptobrachium boringiiDisjunct distributionClimate stabilityLast interglacial periodBiodiversity hotspot
collection DOAJ
language English
format Article
sources DOAJ
author Yuchi Zheng
Qiang Dai
Xianguang Guo
Xiaomao Zeng
spellingShingle Yuchi Zheng
Qiang Dai
Xianguang Guo
Xiaomao Zeng
Dynamics behind disjunct distribution, hotspot-edge refugia, and discordant RADseq/mtDNA variability: insights from the Emei mustache toad
BMC Evolutionary Biology
Sichuan Basin
Leptobrachium boringii
Disjunct distribution
Climate stability
Last interglacial period
Biodiversity hotspot
author_facet Yuchi Zheng
Qiang Dai
Xianguang Guo
Xiaomao Zeng
author_sort Yuchi Zheng
title Dynamics behind disjunct distribution, hotspot-edge refugia, and discordant RADseq/mtDNA variability: insights from the Emei mustache toad
title_short Dynamics behind disjunct distribution, hotspot-edge refugia, and discordant RADseq/mtDNA variability: insights from the Emei mustache toad
title_full Dynamics behind disjunct distribution, hotspot-edge refugia, and discordant RADseq/mtDNA variability: insights from the Emei mustache toad
title_fullStr Dynamics behind disjunct distribution, hotspot-edge refugia, and discordant RADseq/mtDNA variability: insights from the Emei mustache toad
title_full_unstemmed Dynamics behind disjunct distribution, hotspot-edge refugia, and discordant RADseq/mtDNA variability: insights from the Emei mustache toad
title_sort dynamics behind disjunct distribution, hotspot-edge refugia, and discordant radseq/mtdna variability: insights from the emei mustache toad
publisher BMC
series BMC Evolutionary Biology
issn 1471-2148
publishDate 2020-08-01
description Abstract Background The distribution of genetic diversity and the underlying processes are important for conservation planning but are unknown for most species and have not been well studied in many regions. In East Asia, the Sichuan Basin and surrounding mountains constitute an understudied region that exhibits a “ring” of high species richness overlapping the eastern edge of the global biodiversity hotspot Mountains of Southwest China. We examine the distributional history and genetic diversification of the Emei mustache toad Leptobrachium boringii, a typical “ring” element characterized by disjunct ranges in the mountains, by integrating time-calibrated gene tree, genetic variability, individual-level clustering, inference of population splitting and mixing from allele frequencies, and paleoclimatic suitability modeling. Results The results reveal extensive range dynamics, including secondary contact after long-term isolation via westward dispersal accompanied by variability loss. They allow the proposal of a model that combines recurrent contractions caused by Quaternary climatic changes and some failed expansions under suitable conditions for explaining the shared disjunct distribution pattern. Providing exceptional low-elevation habitats in the hotspot area, the eastern edge harbors both long-term refugial and young immigrant populations. This finding and a synthesis of evidence from other taxa demonstrate that a certain contributor to biodiversity, one that preserves and receives low-elevation elements of the east in this case, can be significant for only a particular part of a hotspot. By clarifying the low variability of these refugial populations, we show that discordant mitochondrial estimates of diversity can be obtained for populations that experienced admixture, which would have unlikely left proportional immigrant alleles for each locus. Conclusions Dispersal after long-term isolation can explain much of the spatial distribution of genetic diversity in this species, while secondary contact and long-term persistence do not guarantee a large variation. The model for the formation of disjunct ranges may apply to many other taxa isolated in the mountains surrounding the Sichuan Basin. Furthermore, this study provides insights into the heterogeneous nature of hotspots and discordant variability obtained from genome-wide and mitochondrial data.
topic Sichuan Basin
Leptobrachium boringii
Disjunct distribution
Climate stability
Last interglacial period
Biodiversity hotspot
url http://link.springer.com/article/10.1186/s12862-020-01675-8
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