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      Climatic Factors Drive Population Divergence and Demography: Insights Based on the Phylogeography of a Riparian Plant Species Endemic to the Hengduan Mountains and Adjacent Regions

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          Abstract

          Quaternary climatic factors have played a significant role in population divergence and demography. Here we investigated the phylogeography of Osteomeles schwerinae, a dominant riparian plant species of the hot/warm-dry river valleys of the Hengduan Mountains (HDM), Qinling Mountains (QLM) and Yunnan-Guizhou Plateau (YGP). Three chloroplast DNA (cpDNA) regions ( trnD- trnT, psbD- trnT, petL- psbE), one single copy nuclear gene (glyceraldehyde 3-phosphate dehydrogenase; G3pdh), and climatic data during the Last Interglacial (LIG; c. 120–140 ka), Last Glacial Maximum (LGM; c. 21 ka), and Current ( c. 1950–2000) periods were used in this study. Six cpDNA haplotypes and 15 nuclear DNA (nDNA) haplotypes were identified in the 40 populations of O. schwerinae. Spatial Analysis of Molecular Variance, median-joining networks, and Bayesian phylogenetic trees based on the cpDNA and nDNA datasets, all suggested population divergence between the QLM and HDM-YGP regions. Our climatic analysis identified significant heterogeneity of the climatic factors in the QLM and HDM-YGP regions during the aforementioned three periods. The divergence times based on cpDNA and nDNA haplotypes were estimated to be 466.4–159.4 ka and 315.8–160.3 ka, respectively, which coincide with the time of the weakening of the Asian monsoons in these regions. In addition, unimodal pairwise mismatch distribution curves, expansion times, and Ecological Niche Modeling suggested a history of population expansion (rather than contraction) during the last glaciation. Interestingly, the expansion times were found being well consistent with the intensification of the Asian monsoons during this period. We inferred that the divergence between the two main lineages is probably caused by disruption of more continuous distribution because of weakening of monsoons/less precipitation, whilst subsequent intensification of the Asian monsoons during the last glaciation facilitated the expansion of O. schwerinae populations.

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          Most cited references21

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          Millennial- and orbital-scale changes in the East Asian monsoon over the past 224,000 years.

          High-resolution speleothem records from China have provided insights into the factors that control the strength of the East Asian monsoon. Our understanding of these factors remains incomplete, however, owing to gaps in the record of monsoon history over the past two interglacial-glacial cycles. In particular, missing sections have hampered our ability to test ideas about orbital-scale controls on the monsoon, the causes of millennial-scale events and relationships between changes in the monsoon and climate in other regions. Here we present an absolute-dated oxygen isotope record from Sanbao cave, central China, that completes a Chinese-cave-based record of the strength of the East Asian monsoon that covers the past 224,000 years. The record is dominated by 23,000-year-long cycles that are synchronous within dating errors with summer insolation at 65 degrees N (ref. 10), supporting the idea that tropical/subtropical monsoons respond dominantly and directly to changes in Northern Hemisphere summer insolation on orbital timescales. The cycles are punctuated by millennial-scale strong-summer-monsoon events (Chinese interstadials), and the new record allows us to identify the complete series of these events over the past two interglacial-glacial cycles. Their duration decreases and their frequency increases during glacial build-up in both the last and penultimate glacial periods, indicating that ice sheet size affects their character and pacing. The ages of the events are exceptionally well constrained and may thus serve as benchmarks for correlating and calibrating climate records.
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            A simulated annealing approach to define the genetic structure of populations.

            We present a new approach for defining groups of populations that are geographically homogeneous and maximally differentiated from each other. As a by-product, it also leads to the identification of genetic barriers between these groups. The method is based on a simulated annealing procedure that aims to maximize the proportion of total genetic variance due to differences between groups of populations (spatial analysis of molecular variance; samova). Monte Carlo simulations were used to study the performance of our approach and, for comparison, the behaviour of the Monmonier algorithm, a procedure commonly used to identify zones of sharp genetic changes in a geographical area. Simulations showed that the samova algorithm indeed finds maximally differentiated groups, which do not always correspond to the simulated group structure in the presence of isolation by distance, especially when data from a single locus are available. In this case, the Monmonier algorithm seems slightly better at finding predefined genetic barriers, but can often lead to the definition of groups of populations not differentiated genetically. The samova algorithm was then applied to a set of European roe deer populations examined for their mitochondrial DNA (mtDNA) HVRI diversity. The inferred genetic structure seemed to confirm the hypothesis that some Italian populations were recently reintroduced from a Balkanic stock, as well as the differentiation of groups of populations possibly due to the postglacial recolonization of Europe or the action of a specific barrier to gene flow.
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              Rapid diversification of a species-rich genus of neotropical rain forest trees.

              Species richness in the tropics has been attributed to the gradual accumulation of species over a long geological period in stable equatorial climates or, conversely, to speciation in response to late Tertiary geological events and unstable Pleistocene climates. DNA sequence data are consistent with recent diversification in Inga, a species-rich neotropical tree genus. We estimate that speciation was concentrated in the past 10 million years, with many species arising as recently as 2 million years ago. This coincides with the more recent major uplifts of the Andes, the bridging of the Isthmus of Panama, and Quaternary glacial cycles. Inga may be representative of other species-rich neotropical genera with rapid growth and reproduction, which contribute substantially to species numbers in the world's most diverse flora.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                21 December 2015
                2015
                : 10
                : 12
                : e0145014
                Affiliations
                [1 ]Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China
                [2 ]University of Chinese Academy of Sciences, Beijing, 100049, China
                Technical University in Zvolen, SLOVAKIA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: HS. Performed the experiments: Z-WW. Analyzed the data: Z-WW S-TC. Contributed reagents/materials/analysis tools: Z-WW Z-LN J-WZ ZZ TD. Wrote the paper: Z-WW.

                Article
                PONE-D-15-38722
                10.1371/journal.pone.0145014
                4687034
                26689776
                54371640-7925-4ff2-bb05-271d69c44f7d
                © 2015 Wang et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 2 September 2015
                : 26 November 2015
                Page count
                Figures: 6, Tables: 4, Pages: 21
                Funding
                The study was supported by the Strategic Priority Research Program (B) of the Chinese Academy of Sciences (XDB03030112 to HS), NSFC-Yunnan Natural Science Foundation Combining Program (U1136601 to HS), the Hundred Talents Program of the Chinese Academy of Sciences (2011312D11022 to HS) and the CAS/SAFEA International Partnership Program for Creative Teams. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                All relevant data are within the paper and its Supporting Information files except the DNA sequences. They can be available from the GenBank database (accession numbers KT724331–KT724335, KT750890–KT750920).

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