The distribution of Oxyrrhis marina: a global disperser or poorly characterized endemic?

JOURNAL OF PLANKTON RESEARCH j VOLUME 33 j NUMBER 4 j PAGES 579 – 589 j 2011 The distribution of Oxyrrhis marina: a global disperser or poorly characterized endemic? PHILLIP C. WATTS 1*, LAURA E. MARTIN 1, SUSAN A. KIMMANCE 2, DAVID J. S. MONTAGNES 1 AND CHRIS D. LOWE 1 1 2 SCHOOL OF BIOLOGICAL SCIENCES, BIOSCIENCES BUILDING, UNIVERSITY OF LIVERPOOL, LIVERPOOL L69 7ZB, UK AND PLYMOUTH MARINE LABORATORY, PROSPECT PLACE, PLYMOUTH PL1 3DH, UK *CORRESPONDING AUTHOR: Received May 13, 2010; accepted in principle September 16, 2010; accepted for publication October 16, 2010 It is often argued that microscopic organisms typically have cosmopolitan distributions. This argument has been criticized as it fails to acknowledge the many protists that have limited geographic distributions. Oxyrrhis marina, a common heterotrophic dinoflagellate in many intertidal and coastal habitats, is regarded as globally distributed, yet despite its prominent role as an experimental planktonic organism there are few explicit studies of this species’ geographic range. An analysis of 846 water samples globally confirmed the wide geographic distribution of O. marina and extends this morphospecies’ range into the southern hemisphere. We did not find O. marina beyond 638N latitude, implying that it is rare, or even absent, in Polar seas. Despite being rare in open water, O. marina inhabits the coastal waters of remote islands, such as Hawaii and the Azores. Beneath the apparent broad spatial range are some emerging patterns on the distribution of distinct genetic clades that form two divergent lineages that may represent different species. Two of the clades have discrete, non-overlapping distributions (one in the European Atlantic and western Mediterranean, and the second in the eastern Mediterranean Sea): one has a broad distribution (both coasts of North America and also in the eastern Mediterranean Sea), and one is limited to culture collections from the Baltic Sea and Red Sea. Thus, the Mediterranean Basin appears to be a diversity hotspot for Oxyrrhis, and there is a mixture of wide distributions and endemicity. These issues are discussed with respect to protist biogeography. KEYWORDS: dispersal; speciation; cosmopolitan species; biogeography I N T RO D U C T I O N Oxyrrhis marina, a common heterotrophic dinoflagellate in many intertidal and coastal habitats, is typically regarded as cosmopolitan or globally distributed (e.g. see AlgaeBase—http://www.algaebase.org/—date accessed 15 October 2009). It is surprising, therefore, that despite extensive research using O. marina as a model marine protist (Montagnes et al., 2011a), there are few explicit studies of this species’ natural distribution. Thus, the apparent global occurrence of O. marina is poorly characterized. As a consequence, we lack the basic data that underpin an understanding of the ecological and evolutionary processes that generate present patterns of diversity, and this inevitably creates problems when studies attempt to interpret patterns of divergence (e.g. functional or genetic) between isolates of O. marina. doi:10.1093/plankt/fbq148, available online at www.plankt.oxfordjournals.org. Advance Access publication November 24, 2010 # The Author 2010. Published by Oxford University Press. All rights reserved. For permissions, please email: Corresponding editor: John Dolan JOURNAL OF PLANKTON RESEARCH j VOLUME 33 j NUMBER 4 j PAGES 579 – 589 j 2011 Below, we first provide an indication of why it is important to assess model-species distributions in marine environments. We then indicate the scope of knowledge regarding the distribution of O. marina, indicate why this species can act as a model, in this respect, and finally suggest which data are required to improve our use of O. marina as a model. DISTRIBUTIONS OF MARINE SPECIES M I C RO B I A L D I S T R I B U T I O N S For microbial species, in contrast, controversy has developed with conflicting theories and predictions about the extent and distribution of (free-living) microbial diversity, and ultimately whether microbial biogeography is fundamentally different to that of macroorganisms. On the one hand it has been argued that microscopic or “small” organisms (,1 mm) typically have a cosmopolitan distribution in terrestrial, freshwater and marine environments (Finlay and Clarke, 1999; Finlay, 2002; Fenchel and Finlay, 2003, 2004; Finlay and Fenchel, 2004). These authors argue that wide geographic ranges are a consequence of huge absolute population sizes (rather than inherent properties of certain taxa), which drive wide dispersal potential and maintain a low probability of local population extinction. Since endemism largely generates patterns of species diversity of large organisms, there is an apparent effect of scale, with the diversity of small species exceeding that of larger organisms at local scales, whereas the feature is reversed at larger scales (e.g. global at the extreme). The corollary is that the distribution of small organisms is less dependent on historical contingency and that free-living microbial species are less likely to have biogeographies. Clearly, the above arguments are relative, being based on the size of the organism, its dispersal rate, and the 580 Most macroscopic species (defined here as organisms .10 mm in size) have relatively restricted geographic distributions that presumably reflect a combination of their ecological requirements, evolution and historical contingency (see Finlay and Fenchel, 2004). The relative influences of these processes depend upon the taxon, but there remains some debate about the general importance of such processes in generating observed biogeographic patterns. For example, a contrast may be made between (i) taxa that evolve at a point and subsequently disperse outwards to realize their geographic distribution and (ii) species whose evolution is driven by vicariance or allopatry are characterized by no obvious centre of origin (Heads, 2005). An issue that remains central to any debate about biogeographic patterns is a species’ ability to disperse across heterogeneous landscapes and, therefore, its potential to colonize and exploit new habitats, and to maintain gene flow over wide areas. As an extreme biogeographic pattern, cosmopolitanism (organisms that occur globally or quasi-globally) nonetheless has been described for a substantial number of large species, particularly marine taxa which may be distributed by currents or allowed to disperse due to the connectivity of the oceans (e.g. Graves, 1998; Watts et al., 1998). On the one hand, the pelagic marine environment is perceived to be relatively more stable and typically lacking in barriers to dispersal, when compared with terrestrial landscapes or even benthic marine systems (Palumbi, 1994; Graves, 1998; Sexton and Norris, 2008). For species with life-history traits suitable for wide dispersal, particularly free-living pelagic species, such unifor (...truncated)