Evolutionary History and Global Phylogeography of the Neuston.

Abstract

The neuston comprises a community of interacting species that drift at the water/atmosphere interface of the planet’s subtropical gyres and play an important role in open-ocean epipelagic food webs. The ecological base of the neuston community is an endosymbiosis involving cnidarian hosts (Porpitidae) and their dinoflagellate photosymbionts. Porpitids are preyed upon by a variety of predators, including two specialized gastropods (Janthinidae and Glaucinae). This prominent open-ocean community has been poorly studied, apart from its resident insect genus Halobates. Based on a global sampling of neuston conducted between 2005-2012, this research begins by focusing on the evolutionary history of neustonic taxa across three trophic levels (photosymbionts, porpitid hosts, predatory gastropods) and all 5 subtropical gyre systems. First, photosymbionts genotyped from exemplars of both porpitid genera are identified as the same genus, Scrippsiella (Peridiniales), in every ocean gyre. Second, a molecular phylogeny including bubble-rafting janthinids shows that they are nested within the benthic family Epitoniidae, or wentletrap snails. Using morphological and ecological data from epitoniids, the common violet snail genus Janthina, and the rare brown janthinid genus Recluzia, two hypotheses for the evolutionary origins of bubble floats are tested. The data support the evolution of the janthinid float from an epitoniid egg mass. Third, the differential distributions of the two species of glaucinin nudibranchs (Glaucus atlanticus, global; G. marginatus, Indo-Pacific) presented an opportunity to test whether the establishment of geographic vs. biological barriers is the primary speciation mechanism. Comparing genetic structuring between the two congeners shows that the global species, G. atlanticus, is panmictic whereas the Indo-Pacific G. marginatus is a complex of four overlapping cryptic species in two clades. A repeated reproductive change has occurred once in each clade: the loss of the bursa copulatrix, which is hypothesized to be a biological speciation mechanism in this clade. Finally, mitochondrial phylogeographies of three global neustonic taxa, Glaucus atlanticus (Glaucinae), Velella velella, and Porpita porpita (Porpitidae) are compared to test three hypotheses of within-species genetic structuring: global panmixis; ocean basin panmixis; within-gyre panmixis. The results show that ocean basin and ocean gyre boundaries vary by taxon as barriers to gene flow.