Comparative Population Genetics of Two Alvinocaridid Shrimp Species in Chemosynthetic Ecosystems of the Western Pacific

Abstract

Deep-sea shrimps from the family Alvinocarididae are prominent inhabitants of chemosynthesis-based habitats worldwide. However, their genetic diversity and population connectivity remain poorly understood due to limited sampling. To fill these knowledge gaps, we compared the population genetics of two vent- and seep-dwelling alvinocaridid species with overlapped geographic ranges between the South China Sea and the Manus Basin. Alvinocaris longirostris has a wider distribution, ranging from 35°N to 3°S and at depths of 930 to 1736 m, while Alvinocaris kexueae is more restricted, found between 16°N and 3°S at depths of 1300 to 1910 m. Our analysis, based on the mitochondrial cytochrome c oxidase subunit 1 gene, revealed that A. longirostris had lower genetic diversity and minimal genetic differentiation across eight disjoint vent and seep populations. In contrast, the narrower-distributed A. kexueae exhibited higher genetic diversity and significant genetic differentiation, with stronger gene flow observed from its Haima seep population to the Manus Basin vent population. In addition, both species appear to have experienced population expansion in their recent evolutionary history. These results suggest that A. longirostris and A. kexueae may possess distinct life-history traits that contribute to their differing distribution ranges in the Western Pacific.

Keywords

Alvinocarididae / biogeography / chemosynthesis-based ecosystem / genetic diversity / population connectivity

References

[1] Allendorf, F. W. 2017. “Genetics and the Conservation of Natural Populations: Allozymes to Genomes.” Molecular Ecology 26: 420–430.

[2] Arellano, S. M., A. L. Van Gaest, S. B. Johnson, R. C. Vrijenhoek, and C. M. Young. 2014. “Larvae from Deep-Sea Methane Seeps Disperse in Surface Waters.” Proceedings of the Royal Society B Biological Sciences 281: 20133276.

[3] Baele, G., P. Lemey, T. Bedford, A. Rambaut, M. A. Suchard, and A. V. Alekseyenko. 2012. “Improving the Accuracy of Demographic and Molecular Clock Model Comparison While Accommodating Phylogenetic Uncertainty.” Molecular Biology and Evolution 29: 2157–2167.

[4] Bashevkin, S. M., C. D. Dibble, R. P. Dunn, et al. 2020. “Larval Dispersal in a Changing Ocean with an Emphasis on Upwelling Regions.” Ecosphere 11: e03015.

[5] Beerli, P., and M. Palczewski. 2010. “Unified Framework to Evaluate Panmixia and Migration Direction Among Multiple Sampling Locations.” Genetics 185: 313–326.

[6] Bouckaert, R., J. Heled, D. Kühnert, et al. 2014. “BEAST 2: A Software Platform for Bayesian Evolutionary Analysis.” PLoS Computational Biology 10: e1003537.

[7] Breusing, C., S. B. Johnson, and V. Tunnicliffe. 2015. “Population Structure and Connectivity in Indo-Pacific Deep-Sea Mussels of the Bathymodiolus septemdierum Complex.” Conservation Genetics 16: 1415–1430.

[8] Chen, C., J. T. Copley, K. Linse, and A. D. Rogers. 2015. “Low Connectivity Between ‘Scaly-Foot Gastropod’(Mollusca: Peltospiridae) Populations at Hydrothermal Vents on the Southwest Indian Ridge and the Central Indian Ridge.” Organisms Diversity & Evolution 15: 663–670.

[9] Chen, C., Y. Wu, J. Li, et al. 2023. “TBtools-II: A “One for All, All for One” Bioinformatics Platform for Biological Big-Data Mining.” Molecular Plant 16: 1733–1742.

[10] Cheng, J., H. Yan, M. Hui, and Z. Sha. 2024. “Novel Insights into Deep-Sea Hydrothermal Vent and Cold Seep Adaptation Inferred from Comparative Transcriptome Analysis of a Munidopsid Squat Lobster Distributed in Both Environments.” Deep Sea Research Part I: Oceanographic Research Papers 205: 104245.

[11] Clement, M., D. C. Posada, and K. A. Crandall. 2000. “TCS: A Computer Program to Estimate Gene Genealogies.” Molecular Ecology 9: 1657–1659.

[12] Copley, J. T., and C. M. Young. 2006. “Seasonality and Zonation in the Reproductive Biology and Population Structure of the Shrimp Alvinocaris stactophila (Caridea: Alvinocarididae) at a Louisiana Slope Cold Seep.” Marine Ecology Progress Series 315: 199–209.

[13] Earl, D. A., and B. M. VonHoldt. 2012. “STRUCTURE HARVESTER: A Website and Program for Visualizing STRUCTURE Output and Implementing the Evanno Method.” Conservation Genetics Resources 4: 359–361.

[14] DecaNet eds. 2024. “DecaNet. Alvinocarididae Christoffersen, 1986.” World Register of Marine Species. https://www.marinespecies.org/aphia.php?p=taxdetails&id=106779.

[15] Evanno, G., S. Regnaut, and J. Goudet. 2005. “Detecting the Number of Clusters of Individuals Using the Software STRUCTURE: A Simulation Study.” Molecular Ecology 14: 2611–2620.

[16] Excoffier, L., and H. E. Lischer. 2010. “Arlequin Suite Ver 3.5: A New Series of Programs to Perform Population Genetics Analyses Under Linux and Windows.” Molecular Ecology Resources 10: 564–567.

[17] Folmer, O., M. B. Black, and R. Vrijenhoek. 1994. “DNA Primers for Amplification of Mitochondrial Cytochrome c Oxidase Subunit I from Diverse Metazoan Invertebrates.” Molecular Marine Biology and Biotechnology 3: 294–299.

[18] Fu, Y. X. 1997. “Statistical Tests of Neutrality of Mutations Against Population Growth, Hitchhiking and Background Selection.” Genetics 147: 915–925.

[19] Gebruk, A. V., E. C. Southward, H. Kennedy, and A. J. Southward. 2000. “Food Sources, Behaviour, and Distribution of Hydrothermal Vent Shrimps at the Mid-Atlantic Ridge.” Journal of the Marine Biological Association of the United Kingdom 80: 485–499.

[20] Gonzalez-Castellano, I., J. Pons, E. González-Ortegón, and A. Martínez-Lage. 2020. “Mitogenome Phylogenetics in the Genus Palaemon (Crustacea: Decapoda) Sheds Light on Species Crypticism in the Rockpool Shrimp P. elegans.” PLoS ONE 15: e0237037.

[21] Gordon, A. L., B. A. Huber, E. J. Metzger, R. D. Susanto, H. E. Hurlburt, and T. R. Adi. 2012. “South China Sea Throughflow Impact on the Indonesian Throughflow.” Geophysical Research Letters 39: L11602.

[22] Harpending, H. C. 1994. “Signature of Ancient Population Growth in a Low-Resolution Mitochondrial DNA Mismatch Distribution.” Human Biology 66: 591–600.

[23] He, X., T. Xu, C. Chen, et al. 2023. “Same (sea) Bed Different Dreams: Biological Community Structure of the Haima Seep Reveals Distinct Biogeographic Affinities.” The Innovation Geoscience 1: 100019.

[24] Hernández-Ávila, I., M. A. Cambon-Bonavita, and F. Pradillon. 2015. “Morphology of First Zoeal Stage of Four Genera of Alvinocaridid Shrimps from Hydrothermal Vents and Cold Seeps: Implications for Ecology, Larval Biology and Phylogeny.” PLoS ONE 10: e0144657.

[25] Hudson, R. R., M. Slatkin, and W. P. Maddison. 1992. “Estimation of Levels of Gene Flow from DNA Sequence Data.” Genetics 132: 583–589.

[26] Jakobsson, M., and N. A. Rosenberg. 2007. “CLUMPP: A Cluster Matching and Permutation Program for Dealing with Label Switching and Multimodality in Analysis of Population Structure.” Bioinformatics 23: 1801–1806.

[27] Kanginakudru, S., M. Metta, R. D. Jakati, and J. Nagaraju. 2008. “Genetic Evidence from Indian Red Jungle Fowl Corroborates Multiple Domestication of Modern Day Chicken.” BMC Evolutionary Biology 8: 174.

[28] Kiel, S., Y. Aguilar, and T. Kase. 2020. “Mollusks from Pliocene and Pleistocene Seep Deposits in Leyte, Philippines.” Acta Palaeontologica Polonica 65: 589–627.

[29] Kikuchi, T., and S. Ohta. 1995. “Two Caridean Shrimps of the Families Bresiliidae and Hippolytidae from a Hydrothermal Field on the Iheya Ridge, off the Ryukyu Islands, Japan.” Journal of Crustacean Biology 15: 771–785.

[30] Kimura, M. 1980. “A Simple Method for Estimating Evolutionary Rates of Base Substitutions Through Comparative Studies of Nucleotide Sequences.” Journal of Molecular Evolution 16: 111–120.

[31] Knowlton, N., and L. A. Weigt. 1998. “New Dates and New Rates for Divergence Across the Isthmus of Panama.” Proceedings of the Royal Society of London B: Biological Sciences 265: 2257–2263.

[32] Leigh, J. W., D. Bryant, and S. Nakagawa. 2015. “POPART: Full-Feature Software for Haplotype Network Construction.” Methods in Ecology & Evolution 6: 1110–1116.

[33] Levin, L. A., A. R. Baco, D. A. Bowden, et al. 2016. “Hydrothermal Vents and Methane Seeps: Rethinking the Sphere of Influence.” Frontiers in Marine Science 3: 195812.

[34] Majima, R., T. Kase, S. Kawagata, Y. M. Aguilar, K. Hagino, and M. Maeda. 2007. “Fossil Cold-Seep Assemblages From Leyte Island, Philippines.” Journal of Geography (Chigaku Zasshi) 116: 643–652.

[35] McConachy, T., R. Binns, and H. Permana. 2001. “First Survey for Submarine Hydrothermal Vents in NE Sulawesi, Indonesia.” In AGU Fall Meeting Abstracts 2001, T52A–0923. https://ui.adsabs.harvard.edu/abs/2001AGUFM.T52A0923M/abstract.

[36] Methou, P., L. N. Michel, M. Segonzac, M. A. Cambon-Bonavita, and F. Pradillon. 2020. “Integrative Taxonomy Revisits the Ontogeny and Trophic Niches of Rimicaris Vent Shrimps.” Royal Society Open Science 7: 200837.

[37] Methou, P., V. Nye, J. T. Copley, H. K. Watanabe, Y. Nagai, and C. Chen. 2023. “Life-History Traits of Alvinocaridid Shrimps Inhabiting Chemosynthetic Ecosystems Around Japan.” Marine Biology 170: 75.

[38] Nan, F., H. Xue, and F. Yu. 2015. “Kuroshio Intrusion into the South China Sea: A Review.” Progress in Oceanography 137: 314–333.

[39] Nei, M. 1987. Molecular Evolutionary Genetics. NY, New York: Columbia University Press.

[40] Okamoto, N., S. Shiokawa, S. Kawano, N. Yamaji, H. Sakurai, and M. Kurihara. 2019. “World's First Lifting Test for Seafloor Massive Sulphides in the Okinawa Trough in the EEZ of Japan.” In Proceedings of the Twenty-ninth (2019) International Ocean and Polar Engineering Conference, ISOPE–I, Honolulu, Hawaii, USA, June 2019.

[41] Pereira, O. S., M. Shimabukuro, A. F. Bernardino, and P. Y. Sumida. 2020. “Molecular Affinity of Southwest Atlantic Alvinocaris muricola with Atlantic Equatorial Belt Populations.” Deep Sea Research Part I: Oceanographic Research Papers 163: 103343.

[42] Pineda, J., J. A. Hare, and S. U. Sponaugle. 2007. “Larval Transport and Dispersal in the Coastal Ocean and Consequences for Population Connectivity.” Oceanography 20: 22–39.

[43] Plouviez, S., T. M. Shank, B. Faure, et al. 2009. “Comparative Phylogeography Among Hydrothermal Vent Species Along the East Pacific Rise Reveals Vicariant Processes and Population Expansion in the South.” Molecular Ecology 18: 3903–3917.

[44] Pritchard, J. K., M. Stephens, and P. Donnelly. 2000. “Inference of Population Structure Using Multilocus Genotype Data.” Genetics 155: 945–959.

[45] Qu, T., Y. T. Song, and T. Yamagata. 2009. “An Introduction to the South China Sea Throughflow: Its Dynamics, Variability, and Application for Climate.” Dynamics of Atmospheres and Oceans 47: 3–14.

[46] Rambaut, A., A. J. Drummond, D. Xie, G. Baele, and M. A. Suchard. 2018. “Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7.” Systematic Biology 67: 901–904.

[47] Ramirez-Llodra, E., and M Segonzac. 2006. “Reproductive Biology of Alvinocaris muricola (Decapoda: Caridea: Alvinocarididae) from Cold Seeps in the Congo Basin.” Journal of the Marine Biological Association of the United Kingdom 86: 1347–1356.

[48] Ramos-Onsins, S. E., and J. Rozas. 2002. “Statistical Properties of New Neutrality Tests Against Population Growth.” Molecular Biology and Evolution 19: 2092–2100.

[49] Rosenberg, N. A. 2004. “DISTRUCT: A Program for the Graphical Display of Population Structure.” Molecular Ecology Notes 4: 137–138.

[50] Rozas, J., A. Ferrer-Mata, J. C. Sánchez-DelBarrio, et al. 2017. “DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets.” Molecular Biology and Evolution 34: 3299–3302.

[51] Stevens, C. J., H. Limén, D. W. Pond, Y. Gélinas, and S. K. Juniper. 2008. “Ontogenetic Shifts in the Trophic Ecology of Two Alvinocaridid Shrimp Species at Hydrothermal Vents on the Mariana Arc, Western Pacific Ocean.” Marine Ecology Progress Series 356: 225–237.

[52] Su, J. L., B. X. Guan, and J. Z. Jiang. 1990. “The Kuroshio. Part I. Physical Features.” In Oceanography and Marine Biology, vol. 28, edited by H. Barnes, 11–71. London: CRC Press.

[53] Suess, E. 2014. “Marine Cold Seeps and Their Manifestations: Geological Control, Biogeochemical Criteria and Environmental Conditions.” International Journal of Earth Sciences 103: 1889–1916.

[54] Tajima, F. 1989. “Statistical Method for Testing the Neutral Mutation Hypothesis by DNA Polymorphism.” Genetics 123: 585–595.

[55] Tamura, K., G. Stecher, and S. Kumar. 2021. “MEGA11: Molecular Evolutionary Genetics Analysis Version 11.” Molecular Biology and Evolution 38: 3022–3027.

[56] Teixeira, S., M. A. Cambon-Bonavita, E. A. Serrão, D. Desbruyéres, and S. Arnaud-Haond. 2011. “Recent Population Expansion and Connectivity in the Hydrothermal Shrimp Rimicaris Exoculata Along the Mid-Atlantic Ridge.” Journal of Biogeography 38: 564–574.

[57] Teixeira, S., K. Olu, C. Decker, et al. 2013. “High Connectivity Across the Fragmented Chemosynthetic Ecosystems of the Deep Atlantic Equatorial Belt: Efficient Dispersal Mechanisms or Questionable Endemism?” Molecular Ecology 22: 4663–4680.

[58] Thomas, E. A., R. Liu, D. Amon, et al. 2020. “Chiridota heheva—The Cosmopolitan Holothurian.” Marine Biodiversity 50: 110.

[59] Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. “CLUSTAL W: Improving the Sensitivity of Progressive Multiple Sequence Alignment Through Sequence Weighting, Position-Specific Gap Penalties and Weight Matrix Choice.” Nucleic Acids Research 22: 4673–4680.

[60] Tran Lu, Y. A., S. Ruault, C. Daguin-Thiébaut, et al. 2022. “Subtle Limits to Connectivity Revealed by Outlier Loci Within Two Divergent Metapopulations of the Deep-Sea Hydrothermal Gastropod Ifremeria nautilei.” Molecular Ecology 31: 2796–2813.

[61] Tunnicliffe, V., A. G. McArthur, and D. A. McHugh. 1998. “A Biogeographical Perspective of the Deep-Sea Hydrothermal Vent Fauna.” Advances in Marine Biology 34: 353–442.

[62] Van Audenhaege, L., A. Fariñas-Bermejo, T. Schultz, and C. L. Van Dover. 2019. “An Environmental Baseline for Food Webs at Deep-Sea Hydrothermal Vents in Manus Basin (Papua New Guinea).” Deep Sea Research Part I: Oceanographic Research Papers 148: 88–99.

[63] Van Dover, C. L., C. R. German, K. G. Speer, L. M. Parson, and R. C. Vrijenhoek. 2002. “Evolution and Biogeography of Deep-Sea Vent and Seep Invertebrates.” Science 295: 1253–1257.

[64] Vrijenhoek, R. C. 2010. “Genetic Diversity and Connectivity of Deep-Sea Hydrothermal Vent Metapopulations.” Molecular Ecology 19: 4391–4411.

[65] Wang, Y. R., and Z. L. Sha. 2017. “A New Species of the Genus Alvinocaris Williams and Chace, 1982 (Crustacea: Decapoda: Caridea: Alvinocarididae) from the Manus Basin Hydrothermal Vents, Southwest Pacific.” Zootaxa 4226: 126–136.

[66] Watanabe, H., T. Yahagi, Y. Nagai, et al. 2016. “Different Thermal Preferences for Brooding and Larval Dispersal of Two Neighboring Shrimps in Deep-Sea Hydrothermal Vent Fields.” Marine Ecology 37: 1282–1289.

[67] Weersing, K., and R. Toonen. 2009. “Population Genetics, Larval Dispersal, and Connectivity in Marine Systems.” Marine Ecology Progress Series 393: 1–12.

[68] Wiedicke, M., H. Sahling, G. Delisle, et al. 2002. “Characteristics of an Active Vent in the Fore-Arc Basin of the Sunda Arc, Indonesia.” Marine Geology 184: 121–141.

[69] Xi, L., Y. Sun, T. Xu, et al. 2023. “Phylogenetic Divergence and Population Genetics of the Hydrothermal Vent Annelid Genus Hesiolyra Along the East Pacific Rise: Reappraisal Using Multi-Locus Data.” Diversity and Distributions 29: 184–198.

[70] Xu, T., X. Chai, C. Chen, et al. 2024. “Genetic Divergence and Migration Patterns of a Galatheoid Squat Lobster Highlight the Need for Deep-Sea Conservation.” Molecular Ecology 33: e17200.

[71] Xu, T., J. Sun, H. K. Watanabe, et al. 2018. “Population Genetic Structure of the Deep-Sea Mussel Bathymodiolus platifrons (Bivalvia: Mytilidae) in the Northwest Pacific.” Evolutionary Applications 11: 1915–1930.

[72] Xu, T., Y. Wang, J. Sun, et al. 2021. “Hidden Historical Habitat-Linked Population Divergence and Contemporary Gene Flow of a Deep-Sea Patellogastropod Limpet.” Molecular Biology and Evolution 38: 5640–5654.

[73] Yahagi, T., H. Kayama Watanabe, S. Kojima, and Y. Kano. 2017. “Do Larvae from Deep-Sea Hydrothermal Vents Disperse in Surface Waters?” Ecology 98: 1524–1534.

[74] Yahagi, T., H. Watanabe, J. Ishibashi, and S. Kojima. 2015. “Genetic Population Structure of Four Hydrothermal Vent Shrimp Species (Alvinocarididae) in the Okinawa Trough, Northwest Pacific.” Marine Ecology Progress Series 529: 159–169.

[75] You, Y., C. S. Chern, Y. Yang, C. T. Liu, K. K. Liu, and S. C. Pai. 2005. “The South China Sea, a Cul-de-Sac of North Pacific Intermediate Water.” Journal of Oceanography 61: 509–527.

[76] Zelnio, K. A., and S. Hourdez. 2009. “A New Species of Alvinocaris (Crustacea: Decapoda: Caridea: Alvinocarididae) from Hydrothermal Vents at the Lau Basin, Southwest Pacific, and a Key to the Species of Alvinocarididae.” Proceedings of the Biological Society of Washington 122: 52–71.

[77] Zhang, W., J. Liang, Q. Liang, et al. 2021. “Gas Hydrate Accumulation and Occurrence Associated with Cold Seep Systems in the Northern South China Sea: An Overview.” Geofluids 2021: 5571150.

[78] Zhang, Y. G., M. Pagani, and Z. Liu. 2014. “A 12-Million-Year Temperature History of the Tropical Pacific Ocean.” Science 344: 84–87.

[79] Zhao, Y., T. Xu, Y. S. Law, et al. 2020. “Ecological Characterization of Cold-Seep Epifauna in the South China Sea.” Deep Sea Research Part I: Oceanographic Research Papers 163: 103361.

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