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Evidence of host-associated divergence from coral-eating snails (genus Coralliophila) in the Coral Triangle

Abstract

We studied how host-associations and geography shape the genetic structure of sister species of marine snails Coralliophila radula (A. Adams, 1853) and C. violacea (Kiener, 1836). These obligate ectoparasites prey upon corals and are sympatric throughout much of their ranges in coral reefs of the tropical and subtropical Indo-Pacific. We tested for population genetic structure of snails in relation to geography and their host corals using mtDNA (COI) sequences in minimum spanning trees and AMOVAs. We also examined the evolutionary relationships of their Porites host coral species using maximum likelihood trees of RAD-seq (restriction site-associated DNA sequencing) loci mapped to a reference transcriptome. A maximum likelihood tree of host corals revealed three distinct clades. Coralliophila radula showed a pronounced genetic break across the Sunda Shelf (ΦCT = 0.735) but exhibited no genetic structure with respect to host. C. violacea exhibited significant geographic structure (ΦCT = 0.427), with divergence among Hawaiian populations, the Coral Triangle and the Indian Ocean. Notably, C. violacea showed evidence of ecological divergence; two lineages were associated with different groups of host coral species, one widespread found at all sites, and the other restricted to the Coral Triangle. Sympatric populations of C. violacea found on different suites of coral species were highly divergent (ΦCT = 0.561, d = 5.13%), suggesting that symbiotic relationships may contribute to lineage diversification in the Coral Triangle.

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Acknowledgements

This work was supported by three National Science Foundation programs (OISE-0730256, OISE-1243541 and OCE-0349177), and a US Agency for International Development Grant (497-A-00-10-00008-00). The Lemelson Foundation Fellowship, Conchologists of America, Sigma Xi and the UCLA Department of Ecology and Evolutionary Biology provided additional funding to S. Simmonds. We acknowledge support from the Indonesia government including the Indonesian Ministry of Research and Technology (RISTEK), Indonesian Institute of Sciences (LIPI), Nature Conservation Agency (BKSDA) and the National Marine Park offices of Bunaken and Wakatobi. Sampling was covered under research permits obtained in Indonesia (RISTEK 2011, 198/SIP/FRP/SMNl/2012, 187/SIP/FRP/SM/VI/2013), Timor-Leste (Direccao nacional de Pescase Aquicultura 0042/DNPA/IOP/VII/11), Vietnam, the Philippines (Department of Agriculture-Bureau of Fisheries and Aquatic Resources), the Maldives (Ministry of Fisheries and Aquaculture Permit No. (OTHR)30-D/INDIV/2013/116) and Hawai'i (Department of Land and Natural Resources SAP 2013-11). Thanks to C. Meyer for comments that stimulated this study. Thank you to A. Fritts-Penniman, B. Stockwell, M. Weber, H. Nuetzel and D. Willette for collecting specimens. Thanks also to Z. Forsman and C. Reboton for help identifying Porites. Thank you to M. Campbell, N. Vu and D. Eardley at the Eagle Fish Genetics Laboratory (Eagle, Idaho) for sequencing the coral DNA. Thanks to those that provided advice about or assistance with fieldwork and permits: A. Fritts-Penniman, D. Cahyani, A. Wahyu, Z.A. Muchlisin, E. Rudi, A. Muhardy, F. Hadinata, P. Usef, A. Ackiss, G. Arlotti, D. Smith, M. Sweet and R. Pooley. Diving support provided by Bali Diving Academy, Critters@Lembeh, Lorenso’s Cottages, Cubadak Paradiso Village, Komodo National Park, Freddies Santai Sumurtiga, Lumba-lumba Diving Centre, Cendrawasih Bay National Park, Papua State University, Papua Diving, Kri Eco Resorts and the Korallion Lab. We also thank the Indonesian Biodiversity Research Center at Udayana University, Institute for Environmental and Marine Sciences at Silliman University, Nha Trang University and the Korallion Lab in the Maldives for institutional support.

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Simmonds, S.E., Chou, V., Cheng, S.H. et al. Evidence of host-associated divergence from coral-eating snails (genus Coralliophila) in the Coral Triangle. Coral Reefs 37, 355–371 (2018). https://doi.org/10.1007/s00338-018-1661-6

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Keywords

  • Marine gastropod
  • Parasite
  • Sister species
  • Porites
  • RAD-seq