Effects of Pleistocene sea-level fluctuations on mangrove population dynamics: a lesson from Sonneratia alba

BMC Evolutionary Biology, Jan 2017

Background A large-scale systematical investigation of the influence of Pleistocene climate oscillation on mangrove population dynamics could enrich our knowledge about the evolutionary history during times of historical climate change, which in turn may provide important information for their conservation. Results In this study, phylogeography of a mangrove tree Sonneratia alba was studied by sequencing three chloroplast fragments and seven nuclear genes. A low level of genetic diversity at the population level was detected across its range, especially at the range margins, which was mainly attributed to the steep sea-level drop and associated climate fluctuations during the Pleistocene glacial periods. Extremely small effective population size (Ne) was inferred in populations from both eastern and western Malay Peninsula (44 and 396, respectively), mirroring the fragility of mangrove plants and their paucity of robustness against future climate perturbations and human activity. Two major genetic lineages of high divergence were identified in the two mangrove biodiversity centres: the Indo-Malesia and Australasia regions. The estimated splitting time between these two lineages was 3.153 million year ago (MYA), suggesting a role for pre-Pleistocene events in shaping the major diversity patterns of mangrove species. Within the Indo-Malesia region, a subdivision was implicated between the South China Sea (SCS) and the remaining area with a divergence time of 1.874 MYA, corresponding to glacial vicariance when the emerged Sunda Shelf halted genetic exchange between the western and eastern coasts of the Malay Peninsula during Pleistocene sea-level drops. Notably, genetic admixture was observed in populations at the boundary regions, especially in the two populations near the Malacca Strait, indicating secondary contact between divergent lineages during interglacial periods. These interregional genetic exchanges provided ample opportunity for the re-use of standing genetic variation, which could facilitate mangrove establishment and adaptation in new habitats, especially in the context of global climate changes. Conclusion Phylogeogrpahic analysis in this study reveal that Pleistocene sea-level fluctuations had profound influence on population differentiation of the mangrove tree S. alba. Our study highlights the fragility of mangrove plants and offers a guide for the conservation of coastal mangrove communities experiencing ongoing changes in sea-level.

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Effects of Pleistocene sea-level fluctuations on mangrove population dynamics: a lesson from Sonneratia alba

Yang et al. BMC Evolutionary Biology Effects of Pleistocene sea-level fluctuations on mangrove population dynamics: a lesson from Sonneratia alba Yuchen Yang 0 Jianfang Li 0 Shuhuan Yang 0 Xinnian Li 0 Lu Fang 0 Cairong Zhong 2 Norman C. Duke 1 Renchao Zhou 0 Suhua Shi 0 0 State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, Sun Yat-sen University , Guangzhou 510275 , China 1 Trop WATER, James Cook University , Townsville, Quennsland , Australia 2 Hainan Dongzhai Harbor National Nature Reserve , Haikou 571129 , China Background: A large-scale systematical investigation of the influence of Pleistocene climate oscillation on mangrove population dynamics could enrich our knowledge about the evolutionary history during times of historical climate change, which in turn may provide important information for their conservation. Results: In this study, phylogeography of a mangrove tree Sonneratia alba was studied by sequencing three chloroplast fragments and seven nuclear genes. A low level of genetic diversity at the population level was detected across its range, especially at the range margins, which was mainly attributed to the steep sea-level drop and associated climate fluctuations during the Pleistocene glacial periods. Extremely small effective population size (Ne) was inferred in populations from both eastern and western Malay Peninsula (44 and 396, respectively), mirroring the fragility of mangrove plants and their paucity of robustness against future climate perturbations and human activity. Two major genetic lineages of high divergence were identified in the two mangrove biodiversity centres: the Indo-Malesia and Australasia regions. The estimated splitting time between these two lineages was 3.153 million year ago (MYA), suggesting a role for pre-Pleistocene events in shaping the major diversity patterns of mangrove species. Within the Indo-Malesia region, a subdivision was implicated between the South China Sea (SCS) and the remaining area with a divergence time of 1.874 MYA, corresponding to glacial vicariance when the emerged Sunda Shelf halted genetic exchange between the western and eastern coasts of the Malay Peninsula during Pleistocene sea-level drops. Notably, genetic admixture was observed in populations at the boundary regions, especially in the two populations near the Malacca Strait, indicating secondary contact between divergent lineages during interglacial periods. These interregional genetic exchanges provided ample opportunity for the re-use of standing genetic variation, which could facilitate mangrove establishment and adaptation in new habitats, especially in the context of global climate changes. Conclusion: Phylogeogrpahic analysis in this study reveal that Pleistocene sea-level fluctuations had profound influence on population differentiation of the mangrove tree S. alba. Our study highlights the fragility of mangrove plants and offers a guide for the conservation of coastal mangrove communities experiencing ongoing changes in sea-level. Gene flow; Genetic diversity; Indo-West Pacific; Mangroves; Pleistocene glaciations - Background Mangrove plants constitute a highly productive ecosystem of both ecological and economic importance that lies at the interface of terrestrial and marine environments [1]. They provide essential support to a variety of terrestrial and marine species through nutrient and organic matter sinking and transformation, protection from coastal erosion, and sediment control [2–4]. Mangroves also play crucial roles in daily human life, by creating fisheries, supplying primary raw materials for chemical and medical industries, and protecting against floods and tsunamis, especially for those living within 10 km of an area harboring significant mangrove forests [3, 5–7]. However, mangrove communities have faced rapid decline; between 35 and 86% of the area once home to mangroves has been lost over the past 30 years, due to both climate change and human activity [8]. This loss poses a serious ecological problem and requires urgent conservation in the face of further increases in climate fluctuation. To better protect mangrove communities, a comprehensive understanding of the evolutionary demography of mangrove plants during historical climate oscillations is necessary. Over the last 3 million years, Earth has experienced multiple glaciation events associated with steep sea-level fluctuations and climate changes that are thought to have shaped the modern biogeography of both terrestrial and marine organisms [9–11]. Unlike terrestrial plants, most mangrove species have water-dispersed seedlings that can float for an extended period of time [4], which may play a role in the geographical distribution and population dynamics of mangrove plants. However, traditional views have proposed that large landmasses could halt propogule dispersal, especially during glaciation, resulting in the genetic structure within mangrove speci (...truncated)


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Yuchen Yang, Jianfang Li, Shuhuan Yang, Xinnian Li, Lu Fang, Cairong Zhong, Norman Duke, Renchao Zhou, Suhua Shi. Effects of Pleistocene sea-level fluctuations on mangrove population dynamics: a lesson from Sonneratia alba, BMC Evolutionary Biology, 2017, pp. 22, 17, DOI: 10.1186/s12862-016-0849-z