Systematics and Biodiversity (2015), 13(3): 278À295 Research Article Molecular taxonomy and naming of five cryptic species of Alviniconcha snails (Gastropoda: Abyssochrysoidea) from hydrothermal vents SHANNON B. JOHNSON1, ANDERS WAREN 2, VERENA TUNNICLIFFE3, CINDY VAN DOVER4, C. GEOFFREY WHEAT1, THOMAS F. SCHULTZ4 & ROBERT C. VRIJENHOEK1 1Monterey Bay Aquarium Research Institute, 7700 Sandholdt Rd., Moss Landing, CA 95039, USA 2Swedish Museum of Natural History, Box 50007, SE-10405 Stockholm, Sweden 3University of Victoria, PO Box 3020, Victoria, B.C. V8W 3N5, Canada 4Marine Laboratory, Nicholas School of the Environment, Duke University, 135 Duke Marine Lab Rd., Beaufort, NC 28516, USA (Received 5 March 2014; accepted 23 September 2014) Large symbiont-hosting snails of the genus Alviniconcha (Gastropoda: Abyssochrysidae) are among the dominant inhabitants of hydrothermal vents in the Western Pacific and Indian oceans. The genus was originally described as monotypic, but unique DNA sequences for mitochondrial genes revealed six distinct evolutionary lineages that we could not distinguish based on external morphology. Subsumed under the name Alviniconcha hessleri Okutani & Ohta, the distinct allopatric and sympatric lineages have been assigned placeholder epithets that complicate scientific communications. Based on the present multi-gene sequence data, we hereby describe five Alviniconcha species (in the order of their discovery) À A. kojimai sp. nov., A. boucheti sp. nov., A. marisindica sp. nov., A. strummeri sp. nov. and A. adamantis sp. nov. Thus, we restrict application of the name A. hessleri to specimens that are genetically similar (95% for COI) to those found at localities in the Mariana Trough. Single distinct Alviniconcha species inhabit vent fields along the Central Indian Ridge, the Mariana volcanic arc, and the Mariana back-arc basin, whereas vents in the Manus, Fiji and Lau back-arc basins may host two or three additional species. Formal recognition of these species facilitates future attempts to assess their physiological differences and symbiont associations. Furthermore, their reported distributions have significant biogeographic implications, affecting estimates of the diversity within and overlap among Indo-Pacific vent localities. http://zoobank.org/urn:lsid:zoobank.org:pub:1E4B2E71-9F1D-479E-9A9A-22A9E303AAE5 Key words: Abyssochrysoidea, cryptic species, DNA-barcode, hydrothermal vent, deep-sea Introduction invertebrate taxa inhabiting these habitats (Vrijenhoek, 2009). Failure to recognize evolutionarily distinct lineages Deep-sea organisms are woefully undersampled because results in underestimates of species diversity at local of the great depths, unpredictable oceanographic condi- scales and overestimates of species overlap at greater geo- tions and great expense associated with exploring the vast graphic scales (Matabos et al., 2011). Conversely, incom- abyssal areas that cover nearly 70% of Earth’s surface plete sampling of size series and discrete life-history (McClain & Hardy, 2010). Consequently, our understand- stages (e.g. larvae, juveniles and adults) for many deep- ings of deep-sea biodiversity and biogeography are rela- sea taxa can result in failures to link discrete developmen- tively poor, even for faunas that have received tal stages or to recognize phenotypically plastic morpho- considerable attention, such as those inhabiting hydrother- types within single species. Consequently, species mal vents and other chemosynthesis-based environments descriptions based on traits other than genetic differences (e.g. Bachraty, Legendre, & Desbruyeres, 2009; Rogers can lead to overestimates of local species diversity and et al., 2012; Sibuet & Olu, 1998; Van Dover, 2002). Cryp- underestimates of geographic overlap. Reliable assess- tic species (distinct evolutionary lineages with a common ments of diversity and reconstructions of historical bioge- morphological phenotype) frequently occur among the ography require solid foundations in taxonomy and phylogenetics that often are lacking for undersampled fau- Correspondence to: Shannon B. Johnson. Email: sjohnson@ mbari.org nas. Molecular systematic methods have helped to remedy ISSN 1477-2000 print / 1478-0933 online Ó 2014 The Author(s). Published by Taylor & Francis. This is an Open Access article. Non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly attributed, cited, and is not altered, transformed, or built upon in any way, is permitted. The moral rights of the named author(s) have been asserted. http://dx.doi.org/10.1080/14772000.2014.970673 Molecular taxonomy of five cryptic species of Alviniconcha snails 279 Table 1. Alviniconcha: prior epithets, localities, new species names, COI reference sequences and origin. Prior epithet Ref. Locality Species name GB # Authority Distr.1 A. hessleri (Okutani et al., 1988) Mariana Back-Arc A. hessleri sensu AB235216& Okutani MT, PV, FV Basin stricto AB051765-790 A. sp. "type I" (Kojima et al., 2001; Lau Basin A. kojimai AB235211& Johnson et al. MB, WR, WL, Kojima et al., 1998) sp. nov. AB051792-803 TC, TM A. sp. ‘type II’ (Kojima et al., 2001; Lau Basin A. boucheti AB235212 & Johnson et al. MB, WR, WL, Kojima et al., 1998) sp. nov. AB051804-806 MH, KM A. aff. hessleri (Okutani et al., 2004; Central Indian A. marisindica AB162121-123 & Okutani ED, KA Van Dover et al., Ridge sp. nov. AB235213 2001) A. sp. ‘Lau’ (Beinart et al., 2012; Lau Basin A. strummeri AB235215 Johnson et al. TM (= type III) Suzuki et al., 2006a) sp. nov. A. sp. ‘type IV’ This study, (Fujiwara Izu-Bonin- Mariana A. adamantis AB856040 Johnson et al. DS, SS et al., 2013) Arc sp. nov. 1 Known distributions according to the numbered localities in Figs. 1, 5.2 and Table 2. many of these problems for deep-sea faunas by exposing have proved to be indistinguishable, based on external cryptic species complexes and identifying phenotypic morphology, from A. hessleri sensu lato (Desbruyeres, plasticity in a broad range of vent molluscs and annelids Segonzac, & Bright, 2006; Hasegawa, Fujikura, & Oku- (reviewed in Vrijenhoek, 2009). Analysis of DNA sequen- tani, 1997; Kojima et al., 2001; Waren & Bouchet, 1993), ces provides an objective basis for assessing degrees of and thus remain unnamed. Efforts to identify diagnostic divergence among geographic populations of nominal morphological traits are impeded in many cases by limited species and examining the coupling (or lack thereof) samples, ontogenetic changes in conchology and apparent between distinct evolutionary lineages and morphologi- phenotypic variability. These large snails produce rela- cally defined species. tively thin shells, typically covered with a hairy periostra- The Alviniconcha hessleri species complex (Gastro- cum that is completely abraded in some cases (Fig. 2). poda: Abyssochrysoidea, previously Provannidae) pro- Because these snails often inhabit high temperature vents vides a noteworthy example of cryptic species. with low pH, the calcareous component of the shell can Alviniconcha hessleri Okutani & Ohta, 1988, was initially be severely degraded or entirely absent (Fig. 2), leaving described from the Mariana Back-arc Basin. Subsequent just a silvery organic matrix. Presently, DNA sequences collections from other Indo-Pacific locations, however, provide the most reliable diagnostic method for discrimi- revealed five additional evolutionary lineages (Table 1, nating these lineages. Fig. 1) (Kojima et al., 2001; Kojima, Suguru, Fujiwara, Informal epithets for the unnamed Alviniconcha line- Fujikura, & Hashimoto, 1998; Okutani, Hashimoto, & ages continue to proliferate through the literature, creating Sasaki, 2004; Okutani & Ohta, 1988; Suzuki et al., 2006a; instability of formal taxonomy and impediments to com- Van Dover et al., 2001). Sequencing of mitochondrial munication about the unique geographic distributions, cytochrome-c-oxidase subunit I (COI) identified a highly ecological and physiological differences and symbiont divergent lineage from the Central Indian Ridge, Alvini- associations of the species. To remedy this ‘nomenclatural concha aff. hessleri (Hashimoto et al., 2001; Van Dover housekeeping problem’ (Brower, 2010, p. 488) we used et al., 2001). Okutani and coworkers (2004) indicated that three mitochondrial (mt) markers, Cytochrome-c-oxidase the lineage warrants recognition as a distinct species, but subunit one (COI), 12S ribosomal RNA gene (12S mt morphological differences were not identified. Genetically rRNA), 16S ribosomal RNA gene (16S mt rRNA) and distinct lineages are also found at western Pacific loca- three nuclear markers, Histone-3 (H3), 18S ribosomal tions in the Manus, North Fiji and Lau basins (Kojima RNA gene (18S rRNA), and domains 1 and 6 of 28S ribo- et al., 2001; Suzuki et al., 2006b). We identified a sixth somal RNA gene (28S-D1 rRNA and 28S-D6 rRNA) for western Pacific lineage from the East Diamante Seamount species diagnoses. Genetic differentiation and phyloge- in the Mariana volcanic arc with sequence data, from the netic relationships allowed us to recognize six Alvinicon- shallowest vents known to be inhabited by Alviniconcha, cha species. We recommend that the name A. hessleri at a depth of 357 m. To date, these unnamed lineages sensu stricto is applied to snails that are genetically 280 S. B. Johnson et al. llllllllllllllll l – – 40 – – SS 35 – – 30 MT – – 25 DS – – 20 – PV – 15 – FV – 10 – MB – 5 – – 0 WL KM – WR – -5 l – TC – -10 MH – ED – TM -15 – KA – -20 – – -25 Degrees Latitude – – -30