Abstract
Large tropical continental islands could serve as refugia for southward retreating taxa during climatic oscillations. To test this expectation, we investigated the genetic diversity of Diaphanosoma dubium Manujlova (1964) from Hainan Island (> 30,000 km2), one of the largest islands of China, and its adjacent mainland. We collected 37 populations represented by 1159 individuals from diverse habitats across the whole island and its adjacent mainland and sequenced their mtDNA COI and eleven microsatellite markers (SSR). The island populations had high haplotype diversity for mtDNA and average expected heterozygosity for SSR. Phylogenetic analysis revealed that D. dubium had three lineages (A–C), with Lineage C endemic to Hainan Island. Lineage A was the largest group and experienced post-LGM demographic expansion, and Lineage C was the deepest one, represented by only one haplotype, and thought to be the most ancient one. SAMOVA for both COI and SSR datasets showed the lowlands of northwest of Hainan Island could be a refugium during ice ages. STRUCTURE and DAPC analyses for SSR revealed an admixture genetic structure, which was supported by strong gene flow between the insular and mainland populations.
Similar content being viewed by others
References
Ali, J. R., 2018. New explanation for elements of Hainan Island’s biological assemblage may stretch things a little too far. Ecography 41: 457–460.
Andrews, C. A., 2010. Natural selection, genetic drift, and gene flow do not act in isolation in natural populations. Nature Education Knowledge 3(10): 5.
Arnaud-Haond, S., S. Stoeckel & D. Bailleul, 2020. New insights into the population genetics of partially clonal organisms: when seagrass data meet theoretical expectations. Molecular Ecology 29: 3248–3260.
Beerli, P. & M. Palczewski, 2010. Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185: 31–463.
Bekker, E. I., D. P. Karabanov, Y. R. Galimov, C. R. Haag, T. V. Neretina & A. A. Kotov, 2018. Phylogeography of Daphnia magna Straus (Crustacea: Cladocera) in Northern Eurasia: evidence for a deep longitudinal split between mitochondrial lineages. PLoS ONE 13(3): e0194045.
Bintanja, R., R. S. W. van de Wal & J. Oerlemans, 2005. Modelled atmospheric temperatures and global sea levels over the past million years. Nature 437: 125–128.
Bittkau, C. & H. P. Comes, 2005. Evolutionary processes in a continental island system: molecular phylogeography of the Aegean Nigella arvensis alliance (Ranunculaceae) inferred from chloroplast DNA. Molecular Ecology 14(13): 4065–4083.
Cabrera-Toledo, D., J. González-Astorga & A. P. Vovides, 2008. Heterozygote excess in ancient populations of the critically endangered Dioon caputoi (Zamiaceae, Cycadales) from central Mexico. Botanical Journal of the Linnean Society 158: 436–447.
Chen, H., D. Cheng, L. Xu, Q. Lin & B.-P. Han, 2011. Distribution of Diaphanosoma dubium and D. orghidani in reservoirs of Guangdong Province, southern China. Journal of Lake Sciences 23(5): 801–805.
Clark, P. U., A. Dyke, J. D. Shakun, A. E. Carlson, J. Clark, B. Wohlfarth, J. X. Mitrovica, S. W. Hostetler & A. M. McCabe, 2009. The last glacial maximum. Science 325: 710.
Clement, M., Q. Snell, P. Walke, D. Posada, & K. Crandall, 2002. TCS: estimating gene genealogies. Proc 16th Int Parallel Distrib Process Symp 2: 184.
Cornetti, L., D. F. Peter, K. Van Damme & D. Ebert, 2019. A fossil-calibrated phylogenomic analysis of Daphnia and the Daphniidae. Molecular Phylogenetics and Evolution 137: 250–262.
Costa, F. O., J. R. deWaard, J. Boutillier, J. Boutillier, S. Ratnasingham, R. T. Dooh, M. Hajibabaei & P. D. N. Hebert, 2007. Biological identifications through DNA barcodes: the case of the crustacea. Canadian Journal of Fisheries and Aquatic Science 64: 272–295.
Drummond, A. J., M. A. Suchard, D. Xie & A. Rambaut, 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29: 1969–1973.
Dumont, H. J., 1994. On the diversity of the Cladocera in the tropics. Hydrobiologia 272: 27–38.
Dupanloup, I., S. Schneider & L. Excoffier, 2002. A simulated annealing approach to define the genetic structure of populations. Molecular Ecology 11(12): 2571–2581.
Evanno, G., S. Regnaut & J. Goudet, 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620.
Excoffier, L., G. Laval & S. Schneider, 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics 1: 47–50.
Ezard, T., T. Fujisawa, & T. Barraclough, 2014. Splits: SPecies'LImits by Threshold Statistics. R Package Version 1.0–20/r56.
Falush, D., M. Stephens & J. Pritchard, 2007. Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes 7(4): 574–578.
Fujisawa, T. & T. G. Barraclough, 2013. Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent (GMYC) approach: a revised method and evaluation on simulated datasets. Systematic Biology 62: 707–724.
Geffen, E., M. J. Anderson & R. K. Wayne, 2004. Climate and habitat barriers to dispersal in the highly mobile grey wolf. Molecular Ecology 13: 2481–2490.
Halbritter, D. A., C. G. Storer, A. Y. Kawahara & J. C. Daniels, 2019. Phylogeography and population genetics of pine butterflies: sky island increase genetic divergence. Ecology and Evolution 9: 13389–13401.
Hammoud, C., K. Kougioumoutzis, K. F. Rijsdijk, S. M. Simaiakis, S. J. Norder, J. Foufopoulos, E. Georgopoulou & E. E. Van Loon, 2021. Past connections with the mainland structure pattern of insular species richness in a continental-shelf archipelago (Aegean Sea, Greece). Ecology and Evolution 11(10): 5441–5448.
Han, B. P., J. Yin, X. Lin & H. J. Dumont, 2011. Why is Diaphanosoma (Crustacea: Ctenopoda) so common in the tropics? Influence of temperature and food on the population parameters of Diaphanosoma dubium, and a hypothesis on the nature of tropic cladocerans. Hydrobiologia 668: 109–115.
Hewitt, G., 2000. The genetic legacy of the quaternary ice ages. Nature 405: 907–913.
Hijmans, R. J., S. E. Cameron, J. L. Parra, P. G. Jones & A. Jarvis, 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: 1965–1978.
Hochmuth, J. D., L. De Meester, C. M. S. Pereira, C. R. Janssen & K. A. C. De Schamphelaere, 2015. Rapid adaptation of a Daphnia magna population to metal stress is associated with heterozygote excess. Environmental Science & Technology 49: 9298–9307.
Huang, Y., X. Guo, S. Y. W. Ho, H. Shi, J. Li, B. Cai & Y. Wang, 2013. Diversification and demography of the oriental garden lizard (Calotes versicolor) on Hainan Island and the adjacent mainland. PLoS ONE 8(6): e64754.
Huang, X. X., K. C. Hsu, B. Kang, P. H. Kuo, W. H. Tsai, C. M. Liang, H. D. Lin & W. K. Wang, 2019. Population structure of Aphyocypris normalis: phylogeography and systematics. Zookeys 872: 77–90.
Hubisz, M. J., D. Falush, M. Stephens & J. K. Pritchard, 2009. Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources 9: 1322–1332.
Jombart, T., 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403–1405.
Jombart, T., S. Devillard & F. Balloux, 2010. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics 11: 94.
Katoh, K. & D. M. Standley, 2013. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution 30: 772–780.
Korovchinsky, N. M., 2000. Redescription of Diaphanosoma dubium Manuilova, 1964 (Branchiopoda: Ctenopoda: Sididae), and description of a new, related species. Hydrobiologia 441: 73–92.
Korovchinsky, N. M. & O. S. Boikova, 1996. The resting eggs of the Ctenopoda (Crustacea: Branchiopoda): a review. Hydrobiologia 320: 131–140.
Kotov, A. A. & D. J. Taylor, 2019. Contrasting endemism in pond-dwelling cyclic parthenogens: the Daphnia curvirostris species group (Crustacea: Cladocera). Scientific Reports 9: 6812.
Kotov, A. A., D. P. Karabanov, E. I. Bekker, T. V. Neretina & D. J. Taylor, 2016. Phylogeography of the Chydorus sphaericus Group (Cladocera: Chydoridae) in the Northern Palearctic. PLoSONE 11(12): e0168711.
Lawson, L. P., J. Niedzwiecki & K. Petren, 2019. Darwin’s finches: a model of landscape effects on metacommunity dynamics in the Galápagos Archipelago. Ecography 42: 1636–1647.
Li, S., F. Jiang, H. Lu, X. Kang, Y. Wang, Z. Zou, D. Wen, A. Zheng, C. Liu, Q.-Y. Liu, L. Kang, Q. Xia & F. Cui, 2020. Mosquito Diversity and population genetic structure of six mosquito species from Hainan Island. Frontiers in Genetics 11: 602863.
Liang, B., R.-B. Zhou, Y.-L. Liu, B. Chen, L. L. Grismer & N. Wang, 2018. Renewed classification within Goniurosaurus (Squamata: Eublepharidae) uncovers the dual roles of a continental island (Hainan) in species evolution. Molecular Phylogenetics and Evolution 127: 646–654.
Lin, X. D. & Y. Q. Zong, 1987. More on the origin of the Qiongzhou Strait. Tropical Geography Quarterly 7(4): 338–345.
Lin, R. C., C. K. L. Yeung & S. H. Li, 2008. Drastic post-LGM expansion and lack of historical genetic structure of a subtropical fig-pollinating wasp (Ceratosolen sp. 1) of Ficus septica in Taiwan. Molecular Biology 17(23): 5008–5022.
Liu, P., L. Xu, S. L. Xu, A. Martínez, H. Chen, D. Cheng, H. J. Dumont, B. P. Han & D. Fontaneto, 2018. Species and hybrids in the genus Diaphanosoma Fisher, 1850 (Crustacea: Branchiopoda: Cladocera). Molecular Phylogenetics and Evolution 118: 369–378.
Liu, Q., D. Deng, K. Zhang, P. He, Y. Sun, T. Zhang, W. Yang & W. Liu, 2019. Genetic diversity and differentiation of Daphnia galeata in the middle and lower reaches of the Yangtze River, China. Ecology and Evolution 9: 12688–12700.
Liu, P., S.-L. Xu, J. Liao, H. J. Dumont & B.-P. Han, 2021. Development of microsatellite markers for Diaphanosoma dubium (Crustacea, Cladocera) and application to seasonal population dynamics. Aquatic Ecology 55: 1189–1206.
Losos, J. B. & D. Schluter, 2000. Analysis of an evolutionary species-area relationship. Nature 408: 847–850.
MacArthur, R. H. & E. O. Wilson, 1967. The theory of island biogeography, Princeton University Press, Princeton:
Maddison, W. P., & D. R. Maddison, 2016. Mesquite: a molecular system for evolutionary analysis. Version 3.10, Available at: http://mesquiteproject.org.
Mo, Y. Q. & Y. S. Shi, 1987. Palaeomagnatic study and tectonic evolution of Hainan Terrane and its vicinal continental coast the late Mesozoic to Cenozoic. Journal of Nanjing University 23(3): 521–532.
Norder, S. J., K. V. Proios, R. J. Whittaker, M. R. Alonso, P. A. V. Borges, M. K. Borregaard, R. H. Cowie, F. B. V. Florens, A. M. de Frias Martins, M. Ibáñez, W. D. Kissling, L. de Nascimento, R. Otto, C. E. Parent, F. Rigal, B. H. Warren, J. M. Fernández-Palacios, E. E. van Loon, K. A. Triantis & K. F. Rijsdijk, 2019. Beyond the last glacial maximum: island endemism is best explained by long-lasting archipelago configurations. Global Ecology and Biogeography 28: 184–197.
Nylander, J. A. A., 2004. MrModeltest v2, Evolutionary Biology Centre, Uppsala University, Program distributed by the author:
Peakall, R. & P. E. Smouse, 2006. GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6: 288–295.
Peakall, R. & P. E. Smouse, 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research - an update. Bioinformatics 28: 2537–2539.
Peres-Neto, P. R. & P. Legendre, 2010. Estimating and controlling for spatial autocorrelation in the study of ecological communities. Global Ecology and Biogeography 19: 174–184.
Pritchard, J. K., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.
Prosser, S., A. Martínez-Arce & M. Elías-Gutiérrez, 2013. A new set of primers and some methodological improvements for COI amplification in freshwater microcrustaceans. Molecular Ecology Resources 13: 1151–1155.
Puillandre, N., A. Lambert, S. Brouillet & G. Achaz, 2012. ABGD, automatic barcode gap discovery for primary species delimitation. Molecular Ecology 21: 1864–1877.
R Core Team., 2013. R: a language and environment for statistical computing, R Foundation for Statistical computing, Vienna:
Rambaut, A., M. A. Suchard, D. Xie, & A. J. Drummond, 2014. Tracer v1.7. Available from http://tree.bio.ed.ac.uk/software/tracer/
Rannala, B., 2007. BayesAss, Version 3.0. University of California, Davis, California.
Richter, S., J. Olesen & W. C. Wheeler, 2007. Phylogeny of Branchiopoda (Crustacea) based on a combined analysis of morphological data and six molecular loci. Cladistics 23: 301–336.
Riley, S. P. D., J. P. Pollinger, R. M. Sauvajot, E. C. York, C. Bromley, T. K. Fuller & R. K. Wayne, 2006. A southern California freeway is a physical and social barrier to gene flow in carnivores. Molecular Ecology 15: 1733–1742.
Rozas, J., A. Ferrer-Mata, J. C. Sánchez-DelBarrio, S. Guirao-Rico, P. Librado, S. E. Ramos-Onsins & A. Sánchez-Gracia, 2017. DnaSP 6: DNA sequence polymorphism analysis of large datasets. Molecular Biology and Evolution 34: 3299–3302.
Shi, Y.-F., Z.-Z. Kong, S.-M. Wang, L.-Y. Tang, F.-B. Wang, T.-D. Yao, X.-T. Zhao & P.-Y. Zhang, 1994. The climatic fluctuation and important events of Holocene Megathermal in China. Science in China 37(3): 353–365.
Shih, H. T. & P. K. L. Ng, 2011. Diversity and biogeography of freshwater crabs (Crustacea: Brachyura: Potamidae, Gecarcinucidae) from East Asia. Systematics and Biodiversity 9(1): 1–16.
Shih, H. T., D. C. J. Yeo & P. K. L. Ng, 2009. The collision of the Indian plate with Asia: molecular evidence for its impact on the phylogeny of freshwater crabs (Brachyura: Potamidae). Journal of Biogeography 36(4): 703–719.
Stoeckel, S., J. Grange, J. F. Fernández-Manjarres, I. Bilger, N. Frascaria-Lacoste & S. Mariette, 2006. Heterozygote excess in a self-incompatible and partially clonal forest tree species—Prunus avium L. Molecular Ecology 15: 2019–2118.
Su, Y.-J., T. Wang, B. Zheng, Y. Jiang, G.-P. Chen, P.-Y. Ouyang & Y.-F. Sun, 2005. Genetic differentiation of relictual populations of Alsophila spinulosa in southern China inferred from cpDNA trnL–F noncoding sequences. Molecular Phylogenetics and Evolution 34: 323–333.
Suchard, M. A., P. Lemey, G. Baele, D. L. Ayres, A. J. Drummond & A. Rambaut, 2018. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evolution 4(1): vey016.
Sun, Y. & C. F. Vargas-Mendoza, 2017. Population structure, genetic diversity, and evolutionary history of Kleinia neriifolia (Asteraceae) on the Canary Islands. Frontiers in Plant Science 8: 1180.
Tamura, K., J. Dudley, M. Nei & S. Kumar, 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24(8): 1596–1599.
Tang, S., Z. Zhao, H. Bi & G. Xie, 2008. Analysis of characteristics and development of climate resources in Hainan. Journal of Hainan Normal University 21(3): 343–346.
Tang, C. Q., T. Matsui, H. Ohashi, Y.-F. Dong, A. Momohara, S. Herrando-Moraira, S. Qian, Y. Yang, M. Ohsawa, H. T. Luu, P. J. Grote, P. V. Krestov, B. LePage, M. Werger, K. Robertson, C. Hobohm, C.-Y. Wang, M.-C. Peng, X. Chen, H.-C. Wang, W.-H. Su, R. Zhou, S. Li, L.-Y. He, K. Yan, M.-Y. Zhu, J. Hu, R.-Y. Yang, W.-J. Li, M. Tomita, Z.-L. Wu, H.-Z. Yan, G.-F. Zhang, H. He, S.-R. Yi, H. Gong, K. Song, D. Song, X.-S. Li, Z.-Y. Zhang, P.-B. Han, L.-Q. Shen, D.-S. Huang, K. Luo & J. López-Pujol, 2018. Identifying long-term stable refugia for relict plant species in East Asia. Nature Communications 9(1): 4488.
Tian, S., L.-C. Luo, S. Ge & Z.-Y. Zhang, 2008. Clear genetic structure of Pinus kwangtungensis (Pinaceae) revealed by a plastid DNA fragment with a novel minisatellite. Annals of Botany 102: 69–78.
Tsai, C. L., K. Kubota, H. T. Pham & W. B. Yeh, 2021. ancestral haplotype retention and population expansion determine the complicated population genetic structure of the hilly lineage of Neolucanus swinhoei Complex (Coleoptera, Lucanidae) on the subtropical Taiwan Island. Insects 12(3): 227.
Van Damme, K. & A. A. Kotov, 2016. The fossil record of the Cladocera (Crustacea: Branchiopoda): evidence and hypotheses. Earth Science Reviews 163: 162–189.
Van Damme, K., L. Cornetti, P. D. Fields & D. Ebert, 2022. Whole-genome phylogenetic reconstruction as a powerful tool to reveal homoplasy and ancient rapid radiation in waterflea evolution. Systematic Biology 71(4): 777–787.
Van Oosterhout, C., W. F. Hutchinson, D. P. M. Wills & P. Shipley, 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 35–538.
Ventura, M., A. Petrusek, A. Miró, E. Hamrová, D. Buñay, L. De Meester & J. Mergeay, 2014. Local and regional founder effects in lake zooplankton persist after thousands of years despite high dispersal potential. Molecular Ecology 23: 1014–1027.
Wang, X. H., J. Li, L. M. Zhang, Z. W. He, Q. M. Mei, X. Gong & S. G. Jian, 2019. Population differentiation and demographic history of the Cycas taiwaniana Complex (Cycadaceae) endemic to South China as indicated by DNA sequences and microsatellite markers. Frontiers in Genetics 10: 1238.
Weider, L. J., A. Hobaek, J. K. Colbourne, T. J. Crease, F. Dufresne & P. D. N. Hebert, 1999. Holarctic phylogeography of an asexual species complex. I. Mitochondrial DNA variation in arctic Daphnia. Evolution 53(3): 777–792.
Whittaker, R. J., J. M. Fernández-Palacios, T. J. Matthews, M. K. Borregaard & K. A. Triantis, 2017. Island biogeography: taking the long view of nature’s laboratories. Science 357: 6354.
Wilke, T., R. Schultheiß & C. Albrecht, 2009. As time goes by: a simple fool’s guide to molecular clock approaches in invertebrates. American Malacological Bulletin 27: 25–45.
Wu, Y., J. Huang, M. Zhang, S. Luo, Y. Zhang, F. Lei, F. H. Sheldon & F. Zou, 2012. Genetic divergence and population demography of the Hainan endemic Black-throated Laughingthrush (Aves: Timaliidae, Garrulax chinensis monachus) and adjacent mainland subspecies. Molecular Phylogenetics and Evolution 65: 482–489.
Xu, L., B. P. Han, K. Van Damme, A. Vierstraete, J. R. Vanfleteren & H. J. Dumont, 2011. Biogeography and evolution of the Holarctic zooplankton genus Leptodora (Crustacea: Branchiopoda: Haplopoda). Journal of Biogeography 38: 359–370.
Xu, S. L., B.-P. Han, A. Martínez, M. Schwentner, D. Fontaneto, H. J. Dumont & A. Kotov, 2021. Mitogenomics of Cladocera (Branchiopoda): marked gene order rearrangements and independent predation roots. Molecular Phylogenetics and Evolution 164: 107275.
Yu, W., Z. Chen, Y. Li & L. Wu, 2012. Phylogeographic relationships of Scotophilus kuhlii between Hainan Island and mainland China. Mammal Study 37: 139–146.
Zhang, H. N., 1996. Volcanism marks for rift valley of Qiongzhou strait. Seismological and Geomangnetic Observation and Research 17(4): 42–50.
Zhang, E., J. Chang, J. Shulmeister, P. Langdon, W. Sun, Y. Cao, X. Yang & J. Shen, 2019. Summer temperature fluctuations in Southwestern China during the end of the LGM and the last deglaciation. Earth and Planetary Science Letters 509: 78–87.
Zhao, H. T., L. R. Wang & J. Y. Yuan, 2007. Origin and time of Qiongzhou Stait. Marine Geology & Quaternary Geology 27(2): 33–40.
Zhu, H., 2016. Biogeographical evidences help revealing the origin of Hainan Island. PLoS ONE 11(4): e0151941.
Acknowledgements
The study was supported by grants from NSF of China (Grant Nos. 31901098 and 32171538).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest to declare, relevant to the content of this article.
Additional information
Handling editor: Diego Fontaneto
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Liu, P., Zhang, X., Huang, Q. et al. Genetic diversity, lineage divergence, and demography of Diaphanosoma dubium (Crustacea: Cladocera) on Hainan Island, China. Hydrobiologia 849, 4221–4239 (2022). https://doi.org/10.1007/s10750-022-04975-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-022-04975-w