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Molecular Data Reveal a Highly Diverse Species Flock Within the Munnopsoid Deep-Sea Isopod Betamorpha Fusiformis (Barnard, 1920)

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Molecular Data Reveal a Highly Diverse Species Flock Within the Munnopsoid Deep-Sea Isopod Betamorpha Fusiformis (Barnard, 1920) ARTICLE IN PRESS Deep-Sea Research II 54 (2007) 1820–1830 www.elsevier.com/locate/dsr2 Molecular data reveal a highly diverse species flock within the munnopsoid deep-sea isopod Betamorpha fusiformis (Barnard, 1920) (Crustacea: Isopoda: Asellota) in the Southern Ocean Michael J. Raupacha,Ã, Marina Malyutinab, Angelika Brandtc, Johann-Wolfgang Wa¨ gelea aZoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, D-53113 Bonn, Germany bInstitute of Marine Biology, FEB RAS, Palchevskogo, 17, Vladivostok 690041, Russia cUniversita¨t Hamburg, Zoologisches Institut und Museum, Martin-Luther-King Platz 3, D-20146 Hamburg, Germany Accepted 5 July 2007 Available online 3 August 2007 Abstract Based on our current knowledge about population genetics, phylogeography and speciation, we begin to understand that the deep sea harbours more species than suggested in the past. Deep-sea soft-sediment environment in particular hosts a diverse and highly endemic invertebrate fauna. Very little is known about evolutionary processes that generate this remarkable species richness, the genetic variability and spatial distribution of deep-sea animals. In this study, phylogeographic patterns and the genetic variability among eight populations of the abundant and widespread deep-sea isopod morphospecies Betamorpha fusiformis [Barnard, K.H., 1920. Contributions to the crustacean fauna of South Africa. 6. Further additions to the list of marine isopods. Annals of the South African Museum 17, 319–438] were examined. A fragment of the mitochondrial 16S rRNA gene of 50 specimens and the complete nuclear 18S rRNA gene of 7 specimens were sequenced. The molecular data reveal high levels of genetic variability of both genes between populations, giving evidence for distinct monophyletic groups of haplotypes with average p-distances ranging from 0.0470 to 0.1440 (d-distances: 0.0592–0.2850) of the 16S rDNA, and 18S rDNA p-distances ranging between 0.0032 and 0.0174 (d-distances: 0.0033–0.0195). Intermediate values are absent. Our results show that widely distributed benthic deep-sea organisms of a homogeneous phenotype can be differentiated into genetically highly divergent populations. Sympatry of some genotypes indicates the existence of cryptic speciation. Flocks of closely related but genetically distinct species probably exist in other widespread benthic deep-sea asellotes and other Peracarida. Based on existing data we hypothesize that many widespread morphospecies are complexes of cryptic biological species (patchwork hypothesis). r 2007 Elsevier Ltd. All rights reserved. Keywords: Biogeography; Cryptic species; Patchwork hypothesis; Phylogeography; 16S rDNA; 18S rDNA ÃCorresponding author. Tel.: +49 228 9122 242; fax: +49 228 9122 295. E-mail address: [email protected] (M.J. Raupach). 0967-0645/$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr2.2007.07.009 ARTICLE IN PRESS M.J. Raupach et al. / Deep-Sea Research II 54 (2007) 1820–1830 1821 1. Introduction Peek et al., 2000; Quattro et al., 2001), the decapod Chaceon quinquedon (Weinberg et al., 2003) and Two-thirds of the Earth’s surface is covered by some corals (France et al., 1996; Le Goff-Vitry, oceans, with the majority lying deeper than 1000 m. 2004a, b). However, more detailed studies have Nevertheless, our knowledge about the phylogeny, focused on the invertebrate fauna of hydrothermal speciation, radiation and evolution of the animals vents, including tube worms (Vestimentifera) (e.g., inhabiting the deep sea is poor. Although large Halanych et al., 2001; Goffredi et al., 2003; Hurtado number of specimens have been brought back from et al., 2004) molluscs (e.g., Schwarzpaul and Beck, many deep-sea expeditions, it has often been 2002; Won et al., 2003; Smith et al., 2004; Johnson assumed that the deep-sea environment is homo- et al., 2006) and bresiliid shrimps (Shank et al., genous, with communities largely comprised of 1999; Tokuda et al., 2006). opportunistic habitat generalists (Wolff, 1970; Despite the fact that asellote isopods are one of Menzies et al., 1973; Vinogradowa, 1997). During the most abundant taxons of the deep-sea fauna the 1960s and 1970s it became apparent that species (Hessler and Wilson, 1983; Paterson and Lambs- diversity was much greater than originally expected head, 1995; Howell et al., 2002), only two studies (Sanders et al., 1965; Hessler and Sanders, 1967; analysing the genetic variability within deep-sea Rex, 1981; Rex et al., 1993; Gray, 2002). Grassle asellotes exist until now (Raupach and Wa¨ gele, and Maciolek (1992) estimated the total species pool 2006; Bro¨ keland and Raupach, 2007). However, of benthic deep-sea organisms at 10 million, while both studies give striking evidence for high genetic Lambshead (1993) suggested that such number variability and the existence of cryptic species. might account only for the benthic macrofaunal Asellote isopods are morphologically diverse small species and would increase if meiofaunal taxa were animals (less than 10 mm length) of reduced included. While such estimates of deep-sea diversity mobility, that have colonized the deep sea in several are contentious (Briggs, 1991), it is clear that the lineages (Wa¨ gele, 1989; Raupach et al., 2004). Even deep-sea benthos harbours many more species than though munnopsoid species can swim temporarily previously thought and may compare to other (Hessler and Stro¨ mberg, 1989; Marshall and Diebel, species-rich habitats such as coral reefs and tropical 1995), Asellota are benthic animals. Their dispersal rain forest. capacities may be restricted since isopods possess a Today, we know that the biodiversity of the deep marsupium (brood pouch) where the embryos sea can vary regionally and locally (Grassle and undergo their entire larval development to juveniles Maciolek, 1992). Since the mid-1970s, numerous (mancas). All these aspects probably reduce gene studies have been undertaken to determine the flow and increase the probability of speciation genetic population structure of deep-sea animals events. using a variety of biochemical and molecular Within the deep-sea Asellota, Betamorpha fusi- techniques, especially allozymes electrophoreses formis (Barnard, 1920) represents an abundant and and DNA sequencing. However, most studies have widespread munnopsoid of the deep Atlantic and been carried out on vertebrates, especially Teleostei Southern Oceans (Thistle and Hessler, 1977). (e.g., Creasey and Rogers, 1999; Rogers, 2003; Currently 10 different species of Betamorpha are Aboim et al., 2005), and only a few studies known, which show subtle variations on a few analysing DNA sequences of invertebrates exist. features: the shape of the body, head and mouth- For example, molecular studies on amphipods of field are nearly identical, but the species are clearly the species Eurythenes gryllus reveal two distinct separable on subtle differences of vertex shape, the populations at different depths (France and Kocher, position of uropod insertion and orientation of 1996). Chase et al. (1998) analysed specimens of the tergite margins (Thistle and Hessler, 1977). How- deep-sea protobranch bivalve Deminucula atacella- ever, in spite of minor or subtle morphological na of the North Atlantic, showing that continental traits, the identification of phenotypic plasticity and slope (o2500 m) and rise (42500 m) populations species-specific morphological traits will remain are genetically distinct. The same is true for difficult. In this study mitochondrial 16S rDNA of populations of different deep-sea basins (Zardus 50 specimens of B. fusiformis were analysed to et al., 2006). High degrees of genetic differentiation investigate the genetic variability within an abun- also have been observed between abyssal popula- dant deep-sea munnopsoid morphospecies of the tions of other molluscs (Etter et al., 1999, 2005; Southern Ocean. Beside this we analysed the ARTICLE IN PRESS 1822 M.J. Raupach et al. / Deep-Sea Research II 54 (2007) 1820–1830 Table 1 Individual codes, haplotype codes, GenBank accession numbers for DNA sequences and sample locality of the analysed Betamorpha fusiformis specimens of this study Individual Haplotype Accession Accession Sample locality codes group no.16S rDNA no.18S rDNA BF7 A EF116524 Cape Basin (16-10): 411070S/91540E; 4687–4669 m BF9 A EF116525 Cape Basin (16-10): 411070S/91540E; 4687–4669 m BF10 A EF116526 Cape Basin (16-10): 411070S/91540E; 4687–4669 m BF11 A EF116527EF116546 Cape Basin (16-10): 411070S/91540E; 4687–4669 m BF12 A EF116528 Cape Basin (16-10): 411070S/91540E; 4687–4669 m BF138 C EF116535 Cape Basin (16-10): 411070S/91540E; 4687–4669 m BF139 F EF116523 Cape Basin (16-10): 411070S/91540E; 4687–4669 m BF20 F EF116520 Angulhas Basin (21-7): 471380S/41150E; 4555–4552 m BF21 F EF116521EF116542 Angulhas Basin (21-7): 471380S/41150E; 4555–4552 m BF22 F EF116522 Angulhas Basin (21-7): 471380S/41150E; 4555–4552 m BF57 B EF116529 Kapp Norvegia (74-6): 711180S/131570W; 1030–1040 m BF58 B EF116530 Kapp Norvegia (74-6): 711180S/131570W; 1030–1040 m BF59 B EF116531EF116547 Kapp Norvegia (74-6): 711180S/131570W; 1030–1040 m BF60 B EF116532 Kapp Norvegia (74-6): 711180S/131570W; 1030–1040 m BF91 D EF116533 Explora Esc. (80-9): 701390S/141430W; 3103–3102 m BF94 D EF116534EF116548 Explora Esc. (80-9): 701390S/141430W; 3103–3102 m BF81 E EF116541 Weddell Sea (94-11): 661380S/271050W; 4893–4894 m BF160 G EF116501 Weddell Sea (94-11): 661380S/271050W; 4893–4894 m BF162 G EF116502 Weddell Sea (94-11): 661380S/271050W; 4893–4894 m BF163
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