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      Multilocus phylogeny and cryptic diversity of white-toothed shrews (Mammalia, Eulipotyphla, Crocidura) in China

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          Abstract

          Background

          Crocidura, the most speciose mammalian genus, occurs across much of Asia, Europe and Africa. The taxonomy of Chinese representatives has been studied primarily based on cursory morphological comparisons and their molecular phylogenetic analyses remain unexplored. In order to understand the phylogeny of this group in China, we estimated the first multilocus phylogeny and conducted species delimitation, including taxon sampling throughout their distribution range.

          Results

          We obtained one mitochondrial gene ( cytb) (~ 1, 134 bp) and three nuclear genes ( ApoB, BRCA1, RAG1) (~ 2, 170 bp) for 132 samples from 57 localities. Molecular analyses identified at least 14 putative species that occur within two major well-supported groups in China. Polyphyletic C. wuchihensis appears to be composed of two putative species. Two subspecies, C. rapax rapax and C. rapax kurodai should be elevated to full species status. A phylogenetic tree based on mitochondrial gene from Asian Crocidura species showed that the C. rapax rapax is embedded within C. attenuata, making the latter a paraphyletic group. Three strongly supported undescribed species ( C. sp.1, C. sp.2 and C. sp.3) are revealed from Zada County of Tibet (Western China), Hongjiang County of Hunan Province (Central China) and Dongyang County of Zhejiang Province (Eastern China), Motuo County of Tibet, respectively. The divergence time estimation suggested that China’s Crocidura species began to diversify during the late Pliocene (3.66 Ma) and the Early Pleistocene (2.29 Ma), followed by a series of diversifications through the Pleistocene.

          Conclusions

          The cryptic diversity found in this study indicated that the number of species is strongly underestimated under the current taxonomy. We propose that the three undescribed species should be evaluated using extensive taxon sampling and comprehensive morphological and morphometric approaches. Climate change since the late Pliocene and the uplift of the Qinghai-Tibet Plateau may result in the diversification and speciation of China’s Crocidura species. In short, the underestimated diversity underlines the need for a taxonomic revision of Chinese Crocidura species.

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          Most cited references76

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          Bayesian species delimitation using multilocus sequence data.

          In the absence of recent admixture between species, bipartitions of individuals in gene trees that are shared across loci can potentially be used to infer the presence of two or more species. This approach to species delimitation via molecular sequence data has been constrained by the fact that genealogies for individual loci are often poorly resolved and that ancestral lineage sorting, hybridization, and other population genetic processes can lead to discordant gene trees. Here we use a Bayesian modeling approach to generate the posterior probabilities of species assignments taking account of uncertainties due to unknown gene trees and the ancestral coalescent process. For tractability, we rely on a user-specified guide tree to avoid integrating over all possible species delimitations. The statistical performance of the method is examined using simulations, and the method is illustrated by analyzing sequence data from rotifers, fence lizards, and human populations.
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            Is a new and general theory of molecular systematics emerging?

            The advent and maturation of algorithms for estimating species trees-phylogenetic trees that allow gene tree heterogeneity and whose tips represent lineages, populations and species, as opposed to genes-represent an exciting confluence of phylogenetics, phylogeography, and population genetics, and ushers in a new generation of concepts and challenges for the molecular systematist. In this essay I argue that to better deal with the large multilocus datasets brought on by phylogenomics, and to better align the fields of phylogeography and phylogenetics, we should embrace the primacy of species trees, not only as a new and useful practical tool for systematics, but also as a long-standing conceptual goal of systematics that, largely due to the lack of appropriate computational tools, has been eclipsed in the past few decades. I suggest that phylogenies as gene trees are a "local optimum" for systematics, and review recent advances that will bring us to the broader optimum inherent in species trees. In addition to adopting new methods of phylogenetic analysis (and ideally reserving the term "phylogeny" for species trees rather than gene trees), the new paradigm suggests shifts in a number of practices, such as sampling data to maximize not only the number of accumulated sites but also the number of independently segregating genes; routinely using coalescent or other models in computer simulations to allow gene tree heterogeneity; and understanding better the role of concatenation in influencing topologies and confidence in phylogenies. By building on the foundation laid by concepts of gene trees and coalescent theory, and by taking cues from recent trends in multilocus phylogeography, molecular systematics stands to be enriched. Many of the challenges and lessons learned for estimating gene trees will carry over to the challenge of estimating species trees, although adopting the species tree paradigm will clarify many issues (such as the nature of polytomies and the star tree paradox), raise conceptually new challenges, or provide new answers to old questions.
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              Mutation rates in mammalian genomes.

              Knowledge of the rate of point mutation is of fundamental importance, because mutations are a vital source of genetic novelty and a significant cause of human diseases. Currently, mutation rate is thought to vary many fold among genes within a genome and among lineages in mammals. We have conducted a computational analysis of 5,669 genes (17,208 sequences) from species representing major groups of placental mammals to characterize the extent of mutation rate differences among genes in a genome and among diverse mammalian lineages. We find that mutation rate is approximately constant per year and largely similar among genes. Similarity of mutation rates among lineages with vastly different generation lengths and physiological attributes points to a much greater contribution of replication-independent mutational processes to the overall mutation rate. Our results suggest that the average mammalian genome mutation rate is 2.2 x 10(-9) per base pair per year, which provides further opportunities for estimating species and population divergence times by using molecular clocks.
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                Author and article information

                Contributors
                jiangxl@mail.kiz.ac.cn
                Shaoyliu@163.com
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                14 February 2020
                14 February 2020
                2020
                : 20
                : 29
                Affiliations
                [1 ]ISNI 0000 0000 9479 9538, GRID grid.412600.1, College of Life Sciences, , Sichuan Normal University, ; Chengdu, 610066 China
                [2 ]ISNI 0000000119573309, GRID grid.9227.e, Kunming Institute of Zoology, , Chinese Academy of Sciences, ; Kunming, 650223 China
                [3 ]GRID grid.443847.8, College of Life Science and Technology, , Mudanjiang Normal University, ; Mudanjiang, 157011 China
                [4 ]ISNI 0000 0004 0445 3867, GRID grid.464457.0, Sichuan Academy of Forestry, ; Chengdu, 610081 China
                [5 ]ISNI 0000 0001 2197 9375, GRID grid.421647.2, Centre for Biodiversity and Conservation Biology, , Royal Ontario Museum, ; 100 Queen’s Park, Toronto, M5S 2C6 Canada
                [6 ]Central South Forest Inventory and Planning Institute of State Forestry Administration, Changsha, 410014 China
                Article
                1588
                10.1186/s12862-020-1588-8
                7023792
                32059644
                658c456a-5bd4-4e19-afeb-f0efc8a1d1f7
                © The Author(s). 2020

                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
                : 15 August 2019
                : 27 January 2020
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2020

                Evolutionary Biology
                mitochondrial dna,nuclear dna,rapid radiation,soricidae,species delimitation
                Evolutionary Biology
                mitochondrial dna, nuclear dna, rapid radiation, soricidae, species delimitation

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