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Mitochondrial Gene Trees Support Persistence of Cold Tolerant Fairy Shrimp Throughout the Pleistocene Glaciations in Both Southern and More Northerly Refugia

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Mitochondrial Gene Trees Support Persistence of Cold Tolerant Fairy Shrimp Throughout the Pleistocene Glaciations in Both Southern and More Northerly Refugia Hydrobiologia DOI 10.1007/s10750-013-1533-6 PRIMARY RESEARCH PAPER Mitochondrial gene trees support persistence of cold tolerant fairy shrimp throughout the Pleistocene glaciations in both southern and more northerly refugia Jane Reniers • Bram Vanschoenwinkel • Nicolas Rabet • Luc Brendonck Received: 25 October 2012 / Revised: 16 April 2013 / Accepted: 28 April 2013 Ó Springer Science+Business Media Dordrecht 2013 Abstract Fairy shrimp (Crustacea: Anostraca) are data, the Eastern European subspecies C. diaphanus specialist inhabitants of temporary aquatic habitats. In romanicus deserves species status while the species many parts of the world and particularly in Western status of two Italian chirocephalids, C. salinus and C. Europe, however, populations are declining while the ruffoi is questionable. Results indicate European C. development of adequate conservation strategies is diaphanus lineages diverged well before the last impeded by a poor knowledge of the genetic structure glacial maximum and survived the Pleistocene glaci- and taxonomic status of remaining lineages. We ations in multiple (sub)refugia along the Iberian, reconstructed a phylogeography of the species Chiro- Italian, and Balkan peninsula. Northern Europe was cephalus diaphanus Pre´vost, 1803 using partial subsequently recolonized from Southern France, sequences of the mitochondrial COI gene and discuss resulting in high levels of cryptic diversity around the importance of different Pleistocene refugia to glacial refugia but also in more widespread haplotypes explain current diversity patterns. In addition to 20 C. in mainland Europe. diaphanus populations, we also included populations of six presumably closely related chirocephalids to Keywords C. diaphanus Á Cryptic diversity Á Long evaluate their taxonomic status. Based on molecular distance dispersal Á Temporary pools Á Zooplankton Á Refugia Jane Reniers and Bram Vanschoenwinkel contributed equally to this manuscript. Introduction Handling editor: Diego Fontaneto Members of the crustacean order Anostraca, which Electronic supplementary material The online version of includes fairy shrimps and brine shrimps, are charac- this article (doi:10.1007/s10750-013-1533-6) contains teristic inhabitants of temporary aquatic systems supplementary material, which is available to authorized users. worldwide (Brendonck et al., 2008). Most anostracans are omnivorous filter feeders that are characterized by J. Reniers (&) Á B. Vanschoenwinkel Á L. Brendonck Laboratory of Aquatic Ecology and Evolutionary Biology, obligate sexual reproduction. They produce resistant KULeuven, 3000 Leuven, Belgium resting eggs that ensure survival of populations when e-mail: [email protected] the habitat dries out or freezes solid (Brendonck & De Meester, 2003). In addition, these eggs represent the N. Rabet UMR BOREA, MNHN-UPMC-CNRS-IRD, dominant life stage that is passively dispersed by wind, 43 rue Cuvier, 75005 Paris, France water, and animal vectors (Sanchez et al., 2007; 123 Hydrobiologia Vanschoenwinkel et al., 2008a, b). Chirocephalus is with a lack of clear geographical structure—on the the second largest genus within the Anostraca and is other hand, is explained in terms of a rapid range distributed throughout the Palearctic region (Brtek & expansion after the last glacial maximum (LGM) (e.g., Mura, 2000). Within this genus, Chirocephalus di- in the water flea Daphnia magna; De Gelas & De aphanus is the most widespread and most common Meester, 2005). Little is known, however, about the European anostracan (Brtek & Thie´ry, 1995). C. exact location of glacial refugia in European freshwa- diaphanus is a eurytopic species (Fonseca et al., ter zooplankton (but see Go´mez et al., 2000, 2007;Xu 2008) occurring in a wide range of freshwater habitats et al., 2009). For anostracans, phylogeographic studies in both lowland and highland areas up to 2,300 m are either restricted to halophilic species and fresh- above sea-level (Alonso, 1996; Defaye et al., 1998; water species of the subtropics, Mediterranean or Mura, 1999; Demeter & Stoicescu, 2008). Its habitat North America which often occupy relatively small includes flooded fields, temporary ponds, ditches and geographic areas, or only consider subfragments of occasionally permanent waters in alpine areas that species ranges (Ketmaier et al., 2008, 2012; Mun˜oz freeze solid in winter, excluding fish predators. The et al., 2008; Aguilar, 2011; Vanschoenwinkel et al., species has even been observed living under ice sheets 2011; Pinceel et al., 2012, but see Ketmaier et al., in late winter in lowland areas (Brtek & Thie´ry, 1995; 2005). Czeczuga & Czeczuga-Semeniuk, 1998; Zarattini & The anostracan genus Chirocephalus is character- Mura, 2007; own observation). ized by substantial intraspecific morphological varia- Studies of the genetic structure of different organ- tion. Consequently, species are often not clearly isms in Western Europe typically report important delineated what prevents reliable demarcation of effects of the Pleistocene glaciations with extant taxonomic units based on external traits (Brtek & northern populations representing relatively recent Thie´ry, 1995; Mura et al., 2002). Hitherto, only one colonization events from at least one of the southern phylogenetic study and one phylogeographic study refugia in the Apennine peninsula (Italy), Anatolia, the have attempted to clarify the evolutionary relation- Balkans, and Iberia (Taberlet et al., 1998—review; ships within the genus; they consider one population Hewitt, 1999—review; Beebee & Rowe, 2000—frog; of each of the six nominal species that inhabit of the Habel et al., 2005—butterfly; Mun˜oz et al., 2008— Apennine peninsula (Ketmaier et al., 2003) and all brine shrimp). The relative contribution of these seven extant populations of C. kerkyrensis (Ketmaier refugia to the postglacial colonization often varies, et al., 2012). Within the widespread C. diaphanus however, even among closely related species (Weider some authors recognize several subspecies based on et al., 1999; Micheaux et al., 2005). In addition, recent morphological differences (Daday, 1913; Pesta, 1921; evidence indicates that more northerly regions, Stoicescu, 1992). Thus far, however, no consensus has including areas in central and eastern Europe, also been reached about the taxonomic status of these taxa supported small populations of cold tolerant plants and due to substantial intraspecific morphological vari- animals (Bhagwat & Willis, 2008; Sommer & Zachos, ability and a lack of sequence data from populations 2009) throughout the glaciations (Willis & Whittaker, across subspecies ranges (Brtek & Thie´ry, 1995; 2000; Stewart et al., 2010; Schmitt & Varga, 2012). Marincˇek & Petrov, 1995; Brtek, 1997; Mura, 2001; Phylogeographic studies on freshwater crustaceans Mura et al., 2002). Given the fact that many anostracan in the Western Palearctic (De Gelas & De Meester, lineages are rare and declining (Eng et al., 1990; 2005;Go´mez et al., 2007; Zierold et al., 2007; Petrov & Petrov, 1997; Damgaard & Olesen, 1998; Vanschoenwinkel et al., 2012) generally reveal two Mura, 1999; Eder & Ho¨dl, 2002), molecular markers non-mutually exclusive (e.g., Zierold et al., 2007) can present an important complementary source of patterns. The first pattern—a relatively high degree of information which may not only aid to further resolve genetic differentiation and local endemism of extant the taxonomy and delineate evolutionary significant lineages—is generally attributed to isolation and units (ESU’s) (Moritz, 1994), but also allows recon- persistence in glacial refugia leading to a long structing the impact of the Pleistocene glaciations and independent evolutionary history (e.g., in the rotifer explain the current distribution of genetic lineages. Brachionus manjavacas,Go´mez et al., 2007). The The main goal of this article is to investigate the second pattern—low genetic diversity in combination genetic structure of the Western Palearctic 123 Hydrobiologia Chirocephalus diaphanus lineages based on the mito- are provided in Table 1 and Fig. 1c. The number of chondrial cytochrome oxidase subunit I gene (COI) sequences varied per population, ranging from one up using model based phylogenetic methods. To be able to a maximum of 10 individuals. Sequences of one C. to reliably delineate meaningful taxonomic units and diaphanus (AY188996) and five additional Chiro- assess genetic distances indicative of species level cephalus species were retrieved from Genbank: C. differentiation, six presumably closely related Wes- kerkyrensis (AY188997; JN246503–JN246529; hap- tern Palearctic Chirocephalus lineages were included lotype codes for C. kerkyrensis used in this article and in the analyses: C. shadini, C. kerkyrensis, C. ruffoi, C. corresponding haplotype codes in Ketmaier et al., marchesonii, C. salinus, and C. sybillae. Based on tree 2012 are given in the Appendix—Supplementary topologies and sequence divergence based methods material), C. marchesonii (AY188998, JN246530), we first of all discuss molecular support for the C. sibyllae (AY189001), C. salinus (AY198000), C. taxonomic status of different nominal species and ruffoi (AY188999). lineages, and define conservation units. This allows us to assess whether current nominal species adequately DNA extraction, gene amplification, reflect genetic diversity in this group or whether and sequencing representatives could be considered part of a larger species complex. In addition, using a molecular clock Genomic DNA was extracted
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