Reconstruction of population size over time using the EBSP approach indicated that C. obesa in the ECS experienced significant population size changes. After a prolonged stable period, the ECS population decreased from approximately 20000 years ago and increased from approximately 2000 years ago (Figure 4). The subsequent goodness-of-fit tests also supported the null hypothesis of the sudden expansion model, with non-significant values for SSD.Figure 4. Historical population size change of C. obesain the ECS based on EBSPs 4. Discussion In the present study, we used the mitochondrial sequence COI to examine the genetic diversity and phylogeographical structure of the sea penC. obesa in the ECS. Genetic variation among the ECS populations was generally low, perhaps due to a combination of high contemporary gene flow and the recent common ancestry of haplotypes. Larvae of sea pens, called planulae, usually drift freely for approximately 1 week before settling in sediments(López-González et al., 2000). If appropriate sediments are not available, settlement can be delayed by up to 1 month. The long planktonic larval stage in C. obesa may facilitate gene flow by current-driven dispersal of pelagic larvae, and consequently decrease the genetic structure among distant populations in the ECS. Ocean currents play an important role in the genetic flow connections between populations(York et al., 2008). In summer, the ECSCC enters the ECS from the South China Sea and the YSCC from the Yellow Sea. These prevailing currents transport large numbers of planktonic larvae across the marginal seas of the northwest Pacific. The CDW has been reported to act as a physical barrier for some marine species. However, the influence of the CDW on population differentiation is taxonomically variable; some species show no genetic breaks between populations from each side of the CDW(Ni et al., 2017). Species with a long planktonic larval stage usually show substantial mitochondrial homogeneity across the CDW, whereas species with a sessile life history are more prone to biogeographic and historical barriers. The genetic structure of C. obesa in the ECS seems to be uninfluenced by the CDW and may benefit from the long planktonic larval stage. Mismatch distribution analyses indicated that the ECS population recently experienced a bottleneck, which may have resulted in low genetic diversity. Rare variants in small populations are predicted to be eliminated through genetic drift. Recent population isolation and fragmentation during the Pleistocene glacial age increased the role of genetic drift in COI variation in C. obesa(Luo et al., 2012). The mitochondrial gene evolution rate in sea pens is relatively slow(Williams, 2011), which causes them to exhibit lower genetic diversity than other species at the same time. We speculated that the mitochondrial genetic structure of C. obesa in the ECS may have retained the genetic features of the historical population during the Pleistocene. The Pleistocene glacial age, particularly the last glacial maximum (LGM), approximately 20,000 years ago, has had an important influence on the evolution and genetic structure of marine organisms. Some marine species appear to have undergone dramatic population expansion during the LGM when the sea level fluctuated. The population size of C. obesa decreased rapidly when sea level decreased and the ECS shrunk. When sea level rose, C. obesa experienced demographic expansion and reoccupied the seabeds reflooded by the ECS. In that case, the theoretical genetic homology of C. obesa populations in the ECS was high, which is consistent with our results. Most phylogeographic studies in the ECS have focused on economically important species such as fish and mollusks, and more comparative phylogeographic studies using additional species pairs are needed to explain the underlying mechanism of these discrepancies. Our results imply that sea pens such as C. obesa are good candidates for such comparative studies, as they are abundant in this region and suffer less from human-mediated activities than commercially exploited fish and mollusks.Funding: This research was funded by the National Key Research and Development Program of China (grant number 2021YFC3101702).Data Availability Statement: The data that support the findings of this study are available on request upon reasonable request.Acknowledgments: The authors thank Wang Hangjun for collecting the samples.Conflicts of Interest: The authors declare no conflicts of interest.
References
Avise, J.C., 2000. Phylogeography: the history and formation of species. Harvard University Press, Cambridge, Massachusetts.
Bohonak, A.J., 2002. IBD (isolation by distance): A program for analyses of isolation by distance. J. Hered. 93, 153–154. https://doi.org/10.1093/jhered/93.2.153
Coppard, S.E., Lessios, H.A., 2017. Phylogeography of the sand dollar genus Encope: Implications regarding the Central American Isthmus and rates of molecular evolution. Sci. Rep. 7, 1–12. https://doi.org/10.1038/s41598-017-11875-w
Dong, Y. wei, Wang, H. shan, Han, G.D., Ke, C. huan, Zhan, X., Nakano, T., Williams, G.A., 2012. The impact of Yangtze river discharge, ocean currents and historical events on the biogeographic pattern of cellana toreuma along the China coast. PLoS One 7. https://doi.org/10.1371/journal.pone.0036178
Du, X., Cai, S., Yu, C., Jiang, X., Lin, L., Gao, T., Han, Z., 2016. Population genetic structure of mantis shrimps Oratosquilla oratoria: Testing the barrier effect of the Yangtze River outflow. Biochem. Syst. Ecol. 66, 12–18. https://doi.org/10.1016/j.bse.2016.02.033
Excoffier, L., Laval, G., Schneider, S., 2005. Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol. Bioinforma. 1, 117693430500100. https://doi.org/10.1177/117693430500100003
Excoffier, L., Smouse, P.E., Quattro, J.M., 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131, 479–491. https://doi.org/10.1093/genetics/131.2.479
Fu, Y.X., 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Jaspers, C., Ehrlich, M., Pujolar, J.M., Kunzel, S., Bayer, T., Limborg, M.T., Lombard, F., Browne, W.E., Stefanova, K., Reusch, T.B.H., 2021. Invasion genomics uncover contrasting scenarios of genetic diversity in a widespread marine invader. Proc. Natl. Acad. Sci. U. S. A. 118. https://doi.org/10.1073/pnas.2116211118
Kumar, S., Tamura, K., Nei, M., 2004. MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief. Bioinform. 5, 150–163. https://doi.org/10.1093/bib/5.2.150
Lima-Junior, D.P., Bellay, S., Hoeinghaus, D.J., Bini, L.M., Lima, L.B., Yotoko, K., Agostinho, A.A., 2021. Host diversity, phylogenetic relationships and local environmental factors drive infection patterns of a non-native parasite in tropical floodplain fish assemblages. Hydrobiologia 848, 1041–1057. https://doi.org/10.1007/s10750-020-04509-2
López-González, P.J., Gili, J.M., Williams, G.C., 2000. On some veretillid pennatulaceans from the eastern Atlantic and western Pacific Oceans (Anthozoa: Octocorallia), with a review of the genus Cavernularia, and descriptions of new taxa. J. Zool. 250, 201–216. https://doi.org/10.1017/S0952836900002053
Luo, M.F., Pan, H.J., Liu, Z.J., Li, M., 2012. Balancing selection and genetic drift at major histocompatibility complex class II genes in isolated populations of golden snub-nosed monkey (Rhinopithecus roxellana). BMC Evol. Biol. 12, 1–5. https://doi.org/10.1186/1471-2148-12-207
Mccartney, M.A., Burton, M.L., Lima, T.G., 2013. Mitochondrial DNA differentiation between populations of black sea bass (Centropristis striata) across Cape Hatteras, North Carolina (USA). J. Biogeogr. 40, 1386–1398. https://doi.org/10.1111/jbi.12103
McFadden, C.S., France, S.C., Sánchez, J.A., Alderslade, P., 2006. A molecular phylogenetic analysis of the Octocorallia (Cnidaria: Anthozoa) based on mitochondrial protein-coding sequences. Mol. Phylogenet. Evol. 41, 513–527. https://doi.org/10.1016/j.ympev.2006.06.010
Ni, G., Kern, E., Dong, Y.W., Li, Q., Park, J.K., 2017. More than meets the eye: The barrier effect of the Yangtze River outflow. Mol. Ecol. 26, 4591–4602. https://doi.org/10.1111/mec.14235
Ni, G., Li, Q., Kong, L., Yu, H., 2014. Comparative phylogeography in marginal seas of the northwestern Pacific. Mol. Ecol. 23, 534–548. https://doi.org/10.1111/mec.12620
Ni, G., Li, Q., Ni, L., Kong, L., Yu, H., 2015. Population subdivision of the surf clam Mactra chinensis in the East China Sea: Changjiang River outflow is not the sole driver. PeerJ 3, e1240. https://doi.org/10.7717/peerj.1240
Novembre, J., Johnson, T., Bryc, K., Kutalik, Z., Boyko, A.R., Auton, A., Indap, A., King, K.S., Bergmann, S., Nelson, M.R., Stephens, M., Bustamante, C.D., 2008. Genes mirror geography within Europe. Nature 456, 98–101. https://doi.org/10.1038/nature07331
Rius, M., Turon, X., 2020. Phylogeography and the Description of Geographic Patterns in Invasion Genomics. Front. Ecol. Evol. 8, 1–6. https://doi.org/10.3389/fevo.2020.595711
Slatkin, M., 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139, 457–462. https://doi.org/10.1093/genetics/139.1.457
Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595. https://doi.org/10.1093/genetics/123.3.585
Waelbroeck, C., Labeyrie, L., Michel, E., Duplessy, J.C., McManus, J.F., Lambeck, K., Balbon, E., Labracherie, M., 2002. Sea-level and deep water temperature changes derived from benthic foraminifera isotopic records. Quat. Sci. Rev. 21, 295–305. https://doi.org/10.1016/S0277-3791(01)00101-9
Wang, P., 1999. Response of Western Pacific marginal seas to glacial cycles: Paleoceanographic and sedimentological features. Mar. Geol. 156, 5–39. https://doi.org/10.1016/S0025-3227(98)00172-8
Williams, G.C., 2011. The global diversity of sea pens (cnidaria: Octocorallia: Pennatulacea). PLoS One 6. https://doi.org/10.1371/journal.pone.0022747
Xue, D.X., Wang, H.Y., Zhang, T., 2021. Phylogeography and Taxonomic Revision of the Pen Shell Atrina pectinata Species Complex in the South China Sea. Front. Mar. Sci. 8, 1–17. https://doi.org/10.3389/fmars.2021.753553
York, K.L., Blacket, M.J., Appleton, B.R., 2008. The Bassian Isthmus and the major ocean currents of southeast Australia influence the phylogeography and population structure of a southern Australian intertidal barnacle Catomerus polymerus (Darwin). Mol. Ecol. 17, 1948–1961. https://doi.org/10.1111/j.1365-294X.2008.03735.x