Afro-Eurasia and the Americas present barriers to gene flow for the cosmopolitan neustonic nudibranch Glaucus atlanticus
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.
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.
- Alvarado Bremer JR, Viñas J, Mejuto J, Ely B, Pla C (2005) Comparative phylogeography of Atlantic bluefin tuna and swordfish: the combined effects of vicariance, secondary contact, introgression, and population expansion on the regional phylogenies of two highly migratory pelagic fishes. Mol Phylogenet Evol 36:169–187CrossRefGoogle Scholar
- Bucklin A, Frost BW, Bradford-Grieve J, Allen LD, Copley NJ (2003) Molecular systematic and phylogenetic assessment of 34 calanoid copepod species of the Calanidae and Clausocalanidae. Mar Biol 142:333–343Google Scholar
- Coates AG, Obando JA (1996) The geologic evolution of the Central American Isthmus. In: Jackson JBC, Budd AF, Coates AG (eds) Evolution and environment in tropical America. University of Chicago Press, Chicago, pp 21–56Google Scholar
- Day JH (1963) The complexity of the biotic environment. In: Harding JP, Tebble N (eds) Speciation in the sea. Systematics Associates, London, pp 31–49Google Scholar
- Ely B, Viñas J, Alvarado Bremer JR, Black D, Lucas L, Covello K, Labrie AV, Thelen E (2005) Consequences of the historical demography on the global population structure of two highly migratory cosmopolitan marine fishes: the yellowfin tuna (Thunnus albacares) and the skipjack tuna (Katsuwonus pelamis). BMC Evol Biol 22:19CrossRefGoogle Scholar
- Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3:294–299Google Scholar
- Goetze E (2005) Global population genetic structure and biogeography of the oceanic copepods Eucalanus hyalinus and E. spinifer. Evolution 59:2378–2398Google Scholar
- Lalli CM, Gilmer RW (1989) Pelagic snails. The biology of holoplanktonic gastropod mollusks. Stanford University Press, Stanford, CAGoogle Scholar
- McGowan JA (1971) Oceanic biogeography of the Pacific. In: Funnell BM, Riedel WR (eds) The micropaleontology of the oceans. Cambridge University Press, Cambridge, pp 3–74Google Scholar
- Rambaut A, Drummond AJ (2009) Tracer v1.5. http://beast.bio.ed.ac.uk/Tracer. Accessed 1 December 2009
- Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089Google Scholar
- Shields CC (2009) Nudibranchs of the Ross Sea, Antarctica: Phylogeny, diversity, and divergence. Masters Dissertation, Clemson UniversityGoogle Scholar
- Walker ND (1989) Sea surface temperature-rainfall relationships and associated ocean-atmosphere coupling mechanisms in the southern Africa region. Ph.D. Dissertation, University of Cape TownGoogle Scholar