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      Phylogeographic structure, cryptic speciation and demographic history of the sharpbelly ( Hemiculter leucisculus), a freshwater habitat generalist from southern China

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          Abstract

          Background

          Species with broad distributions frequently divide into multiple genetic forms and may therefore be viewed as “cryptic species”. Here, we used the mitochondrial cytochrome b (Cytb) and 12 nuclear DNA loci to investigate phylogeographic structures of the sharpbelly ( Hemiculter leucisculus) in rivers in southern China and explored how the geological and climatic factors have shaped the genetic diversity and evolutionary history of this species.

          Results

          Our mitochondrial phylogenetic analysis identified three major lineages (lineages A, B, and C). Lineages B and C showed a relatively narrower geographic distribution, whereas lineage A was widely distributed in numerous drainages. Divergence dates suggested that H. leucisculus populations diverged between 1.61–2.38 Ma. Bayesian species delimitation analysis using 12 nuclear DNA loci indicated the three lineages probably represented three valid taxa. Isolation-with-migration (IM) analysis found substantial gene flow has occurred among the three lineages. Demographic analyses showed that lineages B and C have experienced rapid demographic expansion at 0.03 Ma and 0.08 Ma, respectively.

          Conclusions

          Hemiculter leucisculus populations in drainages in southern China comprise three mtDNA lineages, and each of which may represent a separate species. Intense uplift of the Qinghai–Tibetan Plateau, evolution of Asian monsoons, changes in paleo-drainages, and poor dispersal ability may have driven the divergence of the three putative species. However, gene flow occurs among the three lineages. Climatic fluctuations have a prominent impact on the populations from the lineages B and C, but exerted little influence on the lineage A.

          Electronic supplementary material

          The online version of this article (10.1186/s12862-017-1058-0) contains supplementary material, which is available to authorized users.

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          Cryptic species as a window on diversity and conservation.

          David P. Bickford, David Lohman, Navjot Sodhi … (2007)
          The taxonomic challenge posed by cryptic species (two or more distinct species classified as a single species) has been recognized for nearly 300 years, but the advent of relatively inexpensive and rapid DNA sequencing has given biologists a new tool for detecting and differentiating morphologically similar species. Here, we synthesize the literature on cryptic and sibling species and discuss trends in their discovery. However, a lack of systematic studies leaves many questions open, such as whether cryptic species are more common in particular habitats, latitudes or taxonomic groups. The discovery of cryptic species is likely to be non-random with regard to taxon and biome and, hence, could have profound implications for evolutionary theory, biogeography and conservation planning.
          Article 0 comments Cited 1058 times – based on 0 reviews     Review now
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            Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques.

            S. Aljanabi (1997)
            A very simple, fast, universally applicable and reproducible method to extract high quality megabase genomic DNA from different organisms is described. We applied the same method to extract high quality complex genomic DNA from different tissues (wheat, barley, potato, beans, pear and almond leaves as well as fungi, insects and shrimps' fresh tissue) without any modification. The method does not require expensive and environmentally hazardous reagents and equipment. It can be performed even in low technology laboratories. The amount of tissue required by this method is approximately 50-100 mg. The quantity and the quality of the DNA extracted by this method is high enough to perform hundreds of PCR-based reactions and also to be used in other DNA manipulation techniques such as restriction digestion, Southern blot and cloning.
            Article 0 comments Cited 721 times – based on 0 reviews     Review now
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              Evolution of Asian monsoons and phased uplift of the Himalaya-Tibetan plateau since Late Miocene times.

              An Zhisheng, John E Kutzbach, Warren Prell … (2001)
              The climates of Asia are affected significantly by the extent and height of the Himalayan mountains and the Tibetan plateau. Uplift of this region began about 50 Myr ago, and further significant increases in altitude of the Tibetan plateau are thought to have occurred about 10-8 Myr ago, or more recently. However, the climatic consequences of this uplift remain unclear. Here we use records of aeolian sediments from China and marine sediments from the Indian and North Pacific oceans to identify three stages of evolution of Asian climates: first, enhanced aridity in the Asian interior and onset of the Indian and east Asian monsoons, about 9-8 Myr ago; next, continued intensification of the east Asian summer and winter monsoons, together with increased dust transport to the North Pacific Ocean, about 3.6-2.6 Myr ago; and last, increased variability and possible weakening of the Indian and east Asian summer monsoons and continued strengthening of the east Asian winter monsoon since about 2.6 Myr ago. The results of a numerical climate-model experiment, using idealized stepwise increases of mountain-plateau elevation, support the argument that the stages in evolution of Asian monsoons are linked to phases of Himalaya-Tibetan plateau uplift and to Northern Hemisphere glaciation.
              Article 0 comments Cited 600 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Shunping He:
                ORCID: http://orcid.org/0000-0001-9087-7890
                clad@ihb.ac.cn
                Journal
                Journal ID (nlm-ta): BMC Evol Biol
                Journal ID (iso-abbrev): BMC Evol. Biol
                Title: BMC Evolutionary Biology
                Publisher: BioMed Central (London )
                ISSN (Electronic): 1471-2148
                Publication date (Electronic): 12 September 2017
                Publication date PMC-release: 12 September 2017
                Publication date Collection: 2017
                Volume: 17
                Electronic Location Identifier: 216
                Affiliations
                [1 ]ISNI 0000 0004 1792 6029, GRID grid.429211.d, The Key Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, , Institute of Hydrobiology, Chinese Academy of Sciences, ; Wuhan, Hubei 430072 China
                [2 ]ISNI 0000 0004 1797 8419, GRID grid.410726.6, University of Chinese Academy of Sciences, ; Beijing, 100049 People’s Republic of China
                Author information
                http://orcid.org/0000-0001-9087-7890
                Article
                Publisher ID: 1058
                DOI: 10.1186/s12862-017-1058-0
                PMC ID: 5596851
                PubMed ID: 28899345
                SO-VID: 42882a97-6741-4e7d-8d47-9b15fb924cda
                Copyright © © The Author(s). 2017
                License:

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                Date received : 20 February 2017
                Date accepted : 30 August 2017
                Funding
                Funded by: the Key Fund and NSFC-Yunnan mutual funds of the National Natural Science Foundation of China
                Award ID: Nos. 31130049 and U1036603
                Award Recipient :
                Funded by: Pilot projects
                Award ID: Nos. XDB13020100
                Award Recipient :
                Categories
                Subject: Research Article
                Custom metadata
                issue-copyright-statement © The Author(s) 2017

                ScienceOpen disciplines: Evolutionary Biology
                Keywords: phylogeographic structure,cryptic speciation,hemiculter leucisculus,southern china,multilocus
                Data availability:
                ScienceOpen disciplines: Evolutionary Biology
                Keywords: phylogeographic structure, cryptic speciation, hemiculter leucisculus, southern china, multilocus

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