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The Noncosmopolitanism Paradigm of Freshwater Zooplankton

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The Noncosmopolitanism Paradigm of Freshwater Zooplankton Molecular Ecology (2009) 18, 5161–5179 doi: 10.1111/j.1365-294X.2009.04422.x The noncosmopolitanism paradigm of freshwater zooplankton: insights from the global phylogeography of the predatory cladoceran Polyphemus pediculus (Linnaeus, 1761) (Crustacea, Onychopoda) S. XU,* P. D. N. HEBERT,† A. A. KOTOV‡ and M. E. CRISTESCU* *Great Lakes Institute for Environmental Research, University of Windsor, Windsor, ON, Canada N9B 3P4, †Biodiversity Institute of Ontario, University of Guelph, Guelph, ON, Canada N1G 2W1, ‡A. N. Severtsov Institute of Ecology and Evolution, Leninsky Prospect 33, Moscow 119071, Russia Abstract A major question in our understanding of eukaryotic biodiversity is whether small bodied taxa have cosmopolitan distributions or consist of geographically localized cryptic taxa. Here, we explore the global phylogeography of the freshwater cladoceran Polyphemus pediculus (Linnaeus, 1761) (Crustacea, Onychopoda) using two mitochon- drial genes, cytochrome c oxidase subunit I and 16s ribosomal RNA, and one nuclear marker, 18s ribosomal RNA. The results of neighbour-joining and Bayesian phylogenetic analyses reveal an exceptionally pronounced genetic structure at both inter- and intra- continental scales. The presence of well-supported, deeply divergent phylogroups across the Holarctic suggests that P. pediculus represents an assemblage of at least nine, largely allopatric cryptic species. Interestingly, all phylogenetic analyses support the reciprocal paraphyly of Nearctic and Palaearctic clades. Bayesian inference of ancestral distribu- tions suggests that P. pediculus originated in North America or East Asia and that European lineages of Polyphemus were established by subsequent intercontinental dispersal events from North America. Japan and the Russian Far East harbour exceptionally high levels of genetic diversity at both regional and local scales. In contrast, little genetic subdivision is apparent across the formerly glaciated regions of Europe and North America, areas that historical demographic analyses suggest that were recolonized just 5500–24 000 years ago. Keywords: Cladocera, endemism, glacial refugia, intercontinental dispersal, speciation, zoo- plankton Received 7 August 2009; revision received 25 September 2009; accepted 6 October 2009 sizes and strong dispersal abilities of micro-eukaryotes Introduction maintain genetic homogeneity across their broad distri- A major uncertainty in our understanding of biodiver- butions. The freshwater zooplankton represents one sity is whether unicellular and small-bodied taxa have group that was historically thought to be dominated by cosmopolitan distributions or consist of geographically cosmopolitan species. This paradigm of cosmopolitanism structured cryptic taxa. Even less clear is the scale of stemmed from the assumption that the dispersal of these geographic structure, when it exists. The classical cosmo- organisms via the passive transport of resting stages politanism view, the ‘everything is everywhere’ hypoth- through vectors such as waterfowl, wind and water esis (Baas-Becking 1934), holds that the large population currents mediated extensive gene flow (Mayr 1963). Furthermore, the cosmopolitan nature of freshwater Correspondence: Sen Xu, Fax: (519) 971-3616; zooplankton is supported by the observed morphologi- E-mail: [email protected] cal homogeneity among widely separated populations. Ó 2009 Blackwell Publishing Ltd 5162 S. XU ET AL. Recently, the classical view of cosmopolitanism has climatic and geologic histories, and to hierarchically been challenged by detailed morphological and genetic explore the evolutionary forces that have shaped pat- studies (e.g. Frey 1982; Hebert & Wilson 1994; Forro´ terns of genetic diversity from global to continental and et al. 2008). These studies clearly show that many so- regional scales. Moreover, due to the limited taxonomic called conspecific populations of zooplankton species scope of previous studies on taxa such as rotifers and including rotifers and cladocerans display strong Daphnia, our understanding of the phylogeography for genetic divergence not only at global geographic scales, freshwater zooplankton with dissimilar biological and but even at regional levels (Gomez et al. 2000; Hebert ecological attributes appear to be limited (but see Cox et al. 2003; Penton et al. 2004). In fact, many widely dis- & Hebert 2001; Petrusek et al. 2004; Dooh et al. 2006; tributed species have now been recognized as cryptic Rowe et al. 2007). species assemblages, which appear to be tens of mil- In this study, we examine the phylogeography of the lions of years old (Colbourne & Hebert 1996; Colbourne predatory cladoceran, Polyphemus pediculus (Linnaeus, et al. 1998; Taylor et al. 1998; Gomez et al. 2002; Ishida 1761) (Crustacea, Onychopoda) across the entirety of its et al. 2006). Holarctic range (Rivier 1998; Korovchinsky 2006). Poly- The replacement of cosmopolitanism by continen- phemus pediculus is well known for its exceptional eco- tal ⁄ regional endemism has greatly facilitated efforts to logical plasticity. It occupies not only ephemeral probe the evolutionary factors underlying the distribu- habitats such as small ponds but also large lakes and tion of genetic diversity in freshwater zooplankton. The brackish estuaries such as the Gulf of Finland (Butorina genetic differentiation between nearby populations has et al. 1975) where it not only occurs in the littoral zone, been proposed as a consequence of founder events fol- but also far offshore and at great depths. Polyphemus lowed by rapid local adaptation. Moreover, the pres- shares important life history attributes with other pred- ence of large, resilient resting propagule banks of local atory cladocerans of the Family Onychopoda (Rivier populations buffers against the establishment of newly 1998; Cristescu & Hebert 2002). As with all other ony- invading genotypes, thus restricting the extent of gene chopods, Polyphemus lacks the protective, ephippial case flow in the face of frequent dispersal events (Monopoli- that encapsulates the resting eggs of most Cladocera, zation Hypothesis; De Meester et al. 2002, 2006). Com- but its resting eggs can resist extensive periods of freez- parative phylogeographic analyses reveal that ing and desiccation (Butorina 1998; Rivier 1998), provid- topographic barriers to gene flow generate predictable ing a capacity for passive dispersal and persistence in patterns of population divergence in zooplankton, sug- ephemeral habitats. gesting that allopatric speciation has played an impor- In this study, we employ two mitochondrial genes, tant role (Hebert et al. 2003). For example, the cytochrome c oxidase subunit I (COI) and 16s ribosomal Appalachian mountain range in North America has RNA, and one nuclear gene, 18s ribosomal RNA (18s), been shown to act as a severe barrier to gene flow as well as an intense sampling strategy across its range between populations of Daphnia laevis (Taylor et al. in North America and Eurasia to examine the genetic 1998), Daphnia ambigua (Hebert et al. 2003) and Sida structure of P. pediculus and ultimately to test its cosmo- crystallina (Cox & Hebert 2001). Furthermore, palaeocli- politanism. Furthermore, we investigate the evolution- matic changes such as the Pleistocene glaciations have ary history underlying the Holarctic distribution of this had a significant impact on the genetic divergence and species and test the roles of intercontinental dispersal persistence of endemic populations. For example, the and habitat shifts between permanent lakes and ephem- North American Sida crystallina (Cox & Hebert 2001) eral ponds in its evolutionary diversification. Finally, and the European Daphnia magna (De Gelas & De Me- we use a combination of phylogeographic and popula- ester 2005) represent assemblages of divergent lineages tion demographic analyses to investigate the effects of that retreated to glacial refugia and recolonized recently the Pleistocene glaciations on the genetic structure and deglaciated habitats. population dynamics of the North American and Eur- Although substantial insights have been gained con- asian populations. cerning the genetic diversification of freshwater zoo- plankton, few studies have investigated their Materials and methods phylogeographic patterns on a global scale (Adamowicz et al. 2009). Yet, a global phylogeographic perspective is Sampling and DNA amplification essential for understanding the evolutionary history of freshwater zooplankton and testing the cosmopolitan- Polyphemus pediculus was sampled from 106 freshwater ism hypothesis. This approach also allows us to com- habitats across the Holarctic: 56 sites in Nearctic and 50 paratively analyse phylogeographic patterns in sites in Palaearctic (Fig. 1 and Table 1). Once collected, geographic regions characterized by dissimilar palaeo- samples were sorted, preserved in 95% ethanol and Ó 2009 Blackwell Publishing Ltd GLOBAL PHYLOGEOGRAPHY OF POLYPHEMUS PEDICULUS 5163 180° NA1 NA2 NA3 150° W 150° E NA4 PA1 PA2 PA3 PA4 PA5 120° W 120° E 90° W 90° E 60° W 60° E 30° W 30° E 0° Fig. 1 Sampling locations and geographic distribution of phylogroups for Polyphemus pediculus. Different shapes identify the nine reconstructed phylogroups (Fig. 2). stored at 4 °C. Genomic DNA was extracted from single and SSU-531 and SSU-1085R (Crease & Colbourne 1998) individuals using a modified proteinase K method (Sch- were used to amplify a 680-base pair (bp) fragment of wenk et al. 1998). the COI gene, a 513-bp fragment of the 16s gene and a A total
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