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The Phylogeny and Diversity of the Bat-Winged Slugs

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The Phylogeny and Diversity of the Bat-Winged Slugs Zoological Journal of the Linnean Society, 2017, 180, 755–789. With 23 figures. Like a bat out of heaven: the phylogeny and diversity of Downloaded from https://academic.oup.com/zoolinnean/article-abstract/180/4/755/3782713 by University of Nevada Reno user on 11 February 2019 the bat-winged slugs (Heterobranchia: Gastropteridae) ELISE ONG1, JOSHUA M. HALLAS2,3 and TERRENCE M. GOSLINER2* 1Department of Biology, Olin-Rice Science Center, Macalester College, Saint Paul, MN 55105, USA 2Department of Invertebrate Zoology & Geology, California Academy of Sciences, San Francisco, CA 94118, USA 3Biology Department, University of Nevada, Reno, 1664 N Virginia St, Reno, NV 89557, USA Received 15 January 2016; revised 6 October 2016; accepted for publication 31 October 2016 A molecular phylogeny is presented for 25 newly sequenced specimens of Gastropteridae. The present phylogeny was estimated by analysing the nuclear fragment 28S and two mitochondrial fragments cytochrome c oxidase I (COI) and 16S using maximum likelihood and Bayesian analyses. The distinctness of eight new species of Gastropteridae is supported by the molecular phylogeny and by subsequent Automatic Barcode Gap Discovery (ABGD) analysis. Morphological data also support the distinctness of these species. The following species are described here: Gastropteron minutum Ong and Gosliner sp. nov., Gastropteron multo Ong and Gosliner sp. nov., Sagaminopteron multimaculatum Ong and Gosliner sp. nov., Siphopteron vermiculum Ong and Gosliner sp. nov., Siphopteron flavolineatum Ong and Gosliner sp. nov., Siphopteron nakakatuwa Ong and Gosliner sp. nov., Siphopteron makisig Ong and Gosliner sp. nov. and Siphopteron dumbo Ong and Gosliner sp. nov. All of these species, spanning much of the phylogenetic tree of Gastropteridae, are found in a single, highly diverse region of the Philippines, the Verde Island Passage. These data support the hypothesis that this region is an area of high species richness as well as phyletic diversity. This study also supports strong correlation between morphological characters and the molecular phylogeny within the species of Siphopteron. Molecular studies also indicate the distinctness of specimens of Siphopteron quadrispinosum from Hawaii and those from the western Pacific. Western Pacific specimens should be regarded as Siphopteron leah. Siphopteron pohnpei is transferred to Sagaminopteron based on the molecular phylogeny. Other species complexes indicating the Head1=Head2=Head1=Head2/Head1 presence of geographically separated cryptic species indicate that further detailed study of this group is warranted and Head2=Head3=Head2=Head3/Head2 that hidden diversity is likely to increase with additional study. Head3=Head4=Head3=Head4/Head3 ADDITIONAL KEYWORDS: biogeography – Cephalaspidea – coral reefs – Coral Triangle – cryptic species – molecular phylogeny – morphology – new species – species richness. INTRODUCTION capable of swimming by flapping their parapodia. This behaviour has been the basis for calling these organ- Gastropteridae is a group of fairly diverse marine isms ‘bat-winged slugs’. The nervous system is among snails with 33 described species in four genera (World the most highly cephalized of cephalaspideans and Register of Marine Species, 2015). Gastropterids are perhaps their elaborate behaviour can be attributed biologically intriguing cephalaspideans that have a to this level of ganglionic concentration. Ecologically, reduced internal shell or have lost the shell entirely as little is known about the feeding of gastropterids, with adults. They have a shortened body, a relatively small the exception that most species of Sagaminopteron body size (usually <10 mm, but always <35 mm in the Tokioka & Baba, 1964 are found and have been largest species). They have large parapodia and are observed eating sponges that lack spicules (Carlson & Hoff, 1973; Gosliner, Behrens & Valdés, 2008). Many *Corresponding author. E-mail: [email protected] [Version of Record, published on 29 April 2017; species of Siphopteron Gosliner, 1989 have complex http://zoobank.org/ urn:lsid:zoobank.org:pub:2C5B5C9E- penial morphology, with elaborate rows of spines and 63D3-48E8-9EA2-27ABA776B687] more than a single papilla. Lange, Wermkinghausen & © 2017 The Linnean Society of London, Zoological Journal of the Linnean Society, 2017, 180, 755–789 755 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] 756 E. ONG ET AL. Anthes (2013) investigated the complex mating behav- systematics of the cephalaspidean heterobranchs and iour of Siphopteron and demonstrated that the elabora- reaffirmed the apparent monophyly of Gastropteridae tion of penial armature in several species was related and suggested its sister relationship with Colpodaspidae to the employment of hypodermic insemination. Oskars, Bouchet & Malaquias, 2015, another lineage of The overwhelming majority of species are found cephalaspideans with a reduced internal shell. Downloaded from https://academic.oup.com/zoolinnean/article-abstract/180/4/755/3782713 by University of Nevada Reno user on 11 February 2019 in the Indo-Pacific tropics or in adjacent temperate The Coral Triangle, bordered by the Philippines, regions (Gosliner et al., 2008). While this is a typical Indonesia and Papua New Guinea, has been documented pattern of diversity, the extent of distribution of many as the area of greatest diversity within the Indo-West of these tropical species is poorly understood and there Pacific (Roberts et al., 2002) and is also home to many appear to be many undescribed species inhabiting this endemic species and clades. Within the Coral Triangle, largest portion of the world’s oceans. it has been shown that the Philippine Islands support The taxonomic history of Gastropteridae clearly indi- the highest known diversity for marine shore fishes cates that the overwhelming majority of species have (Carpenter & Springer, 2005), azooxanthellate corals been described only in the last 60 years. Gastropteron (Cairns, 2007) and heterobranch mollusks (Gosliner Kosse, 1813 is the only genus that has representative et al., 2008). In order to better understand distribu- species in both the Atlantic and the Indo-Pacific. While tion of marine biodiversity within the Coral Triangle Gastropteridae was established in the early 19th cen- and specifically within the Verde Island Passage of the tury, only three species had been described up until Philippines, a series of expeditions was undertaken by 1964, when Tokioka & Baba (1964) named four new spe- an international team of systematic experts organized cies of Gastropteridae in the genera Gastropteron and by the California Academy of Sciences to investigate Sagaminopteron. The following year, Baba & Tokioka undocumented diversity and patterns of diversification (1965) added two additional species of Gastropteron to in the region. The 2014 and 2015 Verde Island Passage the family. Minichev (1967) described Enotepteron, with Expeditions provided an opportunity to collect mate- the monotypic species, Enotepteron flavum Minchev, rial of nearly 100 new species of heterobranch gastro- 1967. Carlson & Hoff (1973) described two new spe- pods, including what appear to be several new species cies of Sagaminopteron from Guam and the following of Gastropteridae. Based on the examination of the year described one new species of Sagaminopteron and morphology of living material, we estimated that there three new species of Gastropteron that were transferred are likely eight new species of Gastropteridae in three later to Siphopteron (Gosliner, 1989). A decade later, of the four distinct genera. The focus of this study is Hoff & Carlson (1983) described Gastropteron pohnpei to examine the molecular phylogeny of these taxa and Hoff & Carlson, 1983, which was transferred later to to determine morphological and molecular boundaries Siphopteron (Gosliner, 1989). Gosliner & Armes (1984) that separate these apparent new species. Also, new described Gastropteron vespertilium Gosliner & Armes taxa will be formally described and differentiated. (1984) from Florida and Gosliner (1984) documented two new species of Gastropteron from temperate south- ern Africa. These two species were later transferred MATERIAL AND METHODS to Siphopteron (Gosliner, 1989). In 1988, Gosliner & MOLECULAR WORK Williams described Gastropteron michaeli Gosliner & Williams, 1988, which was considered later to be a Taxon sampling species of Siphopteron (Gosliner 1989), while Gosliner Representatives of Cephalaspidea sampled are listed in (1988) documented Enotepteron rosewateri Gosliner, Table 1, along with their corresponding voucher num- 1988. Gosliner (1989) described the genus Siphopteron bers, GenBank accession numbers and collection sites. with three new species of Siphopteron and three new The availability of appropriately preserved specimens species of Gastropteron. Brodie, Klussmann-Kolb & has limited our ability to undertake molecular phylo- Gosliner (2001) erected Enotepteron heikae Brodie et genetic studies and many taxa have only been collected al., 2001. Klussmann-Kolb & Klussmann (2003) named once and were not preserved in a manner suitable for Siphopteron leah Klussmann-Kolb & Klussmann, 2003. molecular
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