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Afro-Eurasia and the Americas present barriers to gene flow for the cosmopolitan neustonic nudibranch Glaucus atlanticus

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Abstract

Pelagic species have been traditionally thought to occupy vast, genetically interconnected, geographic ranges in an essentially homogeneous environment. Although this view has been challenged recently for some mesopelagic planktonic taxa, the population structure of hyponeustonic (surface-drifting) species remains unknown. Here, we test the hypothesis of panmixis in Glaucus atlanticus, a cosmopolitan neustonic nudibranch, by assessing the genetic differentiation of multiple representatives from a global neustonic sampling effort. Specimens were collected from all subtropical oceanic gyre systems (North Atlantic, South Atlantic, North Pacific, South Pacific, and Indian Ocean). We sequenced a fragment of the mitochondrial cytochrome oxidase I gene for 98 individuals and performed population structure, differentiation (analysis of molecular variance, spatial analysis of molecular variance, F ST, Jost’s D), and molecular clock analyses. Our results indicate that G. atlanticus is not globally panmictic, but that populations appear to be panmictic within ocean basins. We detected several topologically ectopic haplotypes in the Atlantic Ocean, but the molecular clock analysis indicates that these have diverged from closely related Indo-Pacific haplotypes over 1.2 MYA, coinciding with cooling in waters around in the southern tip of Africa and resulting oceanographic changes. These data and the fact that G. atlanticus is not known from polar latitudes suggest that gene flow between ocean basins is hindered by physical barriers (supercontinents) and water temperatures in the Arctic and Southern Oceans.

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Acknowledgments

We thank the following for their assistance: USA: J. Lyczkowski-Shultz (Southeast Area Monitoring and Assessment Program) and R. Humphreys (Pacific Islands Fisheries Science Center) of the National Oceanographic and Atmospheric Administration, the students and crew of SEA Semester (www.sea.edu), T. Lee (University of Michigan Museum of Zoology); Australia: P. Colman (Australian Museum), L. Beckley (Murdoch University), S. Slack-Smith and C. Whisson (Western Australian Museum); South Africa: R. van der Elst (Oceanographic Research Institute), D. Herbert (Natal Museum), Mark Gibbons (University of the Western Cape), W. Florence and E. Hoenson (Iziko Museums of Cape Town). D. Riek photographed live glaucinins. Funding for this research comes from NSF award OCE 0850625 and National Geographic Society award 8601-09 to D.ÓF.

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  1. Celia K. C. Churchill

    Present address: Marine Science Institute, University of California, Santa Barbara, Santa Barbara, CA, 93106, USA

Authors and Affiliations

  1. Museum of Zoology and Department of Ecology and Evolutionary Biology, University of Michigan, 1109 Geddes Avenue, Ann Arbor, MI, 48109-1079, USA

    Celia K. C. Churchill & Diarmaid Ó Foighil

  2. Department of Biological Sciences, California State Polytechnic University, 3801 West Temple Avenue, Pomona, CA, 91768, USA

    Ángel Valdés

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  1. Celia K. C. Churchill
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Correspondence to Ángel Valdés.

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Communicated by T. Reusch.

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Appendix S1 Bayesian maximum credibility tree (DOCX 343 kb)

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Churchill, C.K.C., Valdés, Á. & Ó Foighil, D. Afro-Eurasia and the Americas present barriers to gene flow for the cosmopolitan neustonic nudibranch Glaucus atlanticus . Mar Biol 161, 899–910 (2014). https://doi.org/10.1007/s00227-014-2389-7

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