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Phylogenetic Relationships of Terrestrial Australo-Papuan Elapid Snakes (Subfamily Hydrophiinae) Based on Cytochrome B and 16S Rrna Sequences J

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Phylogenetic Relationships of Terrestrial Australo-Papuan Elapid Snakes (Subfamily Hydrophiinae) Based on Cytochrome B and 16S Rrna Sequences J MOLECULAR PHYLOGENETICS AND EVOLUTION Vol. 10, No. 1, August, pp. 67–81, 1998 ARTICLE NO. FY970471 Phylogenetic Relationships of Terrestrial Australo-Papuan Elapid Snakes (Subfamily Hydrophiinae) Based on Cytochrome b and 16S rRNA Sequences J. Scott Keogh,*,†,1 Richard Shine,* and Steve Donnellan† *School of Biological Sciences A08, University of Sydney, Sydney, New South Wales 2006, Australia; and †Evolutionary Biology Unit, South Australian Museum, North Terrace, Adelaide, South Australia 5000, Australia Received April 24, 1997; revised September 4, 1997 quence data support many of the conclusions reached Phylogenetic relationships among the venomous Aus- by earlier studies using other types of data, but addi- tralo-Papuan elapid snake radiation remain poorly tional information will be needed before the phylog- resolved, despite the application of diverse data sets. eny of the Australian elapids can be fully resolved. To examine phylogenetic relationships among this ௠ 1998 Academic Press enigmatic group, portions of the cytochrome b and 16S Key Words: mitochondrial DNA; cytochrome b; 16S rRNA mitochondrial DNA genes were sequenced from rRNA; reptile; snake; elapid; sea snake; Australia; New 19 of the 20 terrestrial Australian genera and 6 of the 7 Guinea; Pacific; Asia; biogeography. terrestrial Melanesian genera, plus a sea krait (Lati- cauda) and a true sea snake (Hydrelaps). These data clarify several significant issues in elapid phylogeny. First, Melanesian elapids form sister groups to Austra- INTRODUCTION lian species, indicating that the ancestors of the Austra- lian radiation came via Asia, rather than representing The diverse, cosmopolitan, and medically important a relict Gondwanan radiation. Second, the two major elapid snakes are a monophyletic clade of approxi- groups of sea snakes (sea kraits and true sea snakes) mately 300 species and 61 genera (Golay et al., 1993) represent independent invasions of the marine envi- primarily defined by their unique venom delivery sys- ronment. Third, the radiation of viviparous Australian tem (two permanently erect canaliculate fangs at the elapids is much older than has been suggested from end of the maxilla; McDowell, 1968; McCarthy, 1985). immunological data. Parsimony analyses were unable Relationships both among and within major elapid to resolve relationships among the Australian radia- clades have been the subject of much debate, but most tion, a problem previously encountered with analyses authorities divide the elapid snakes into two major of other (morphological, electrophoretic, karyotypic, lineages based on morphological characters associated immunological) data sets on these species. These data with cranial kinesis (McDowell, 1970): the ‘‘palatine suggest that the reason for this continued difficulty erectors’’ (Afro-Asian cobras, Asian kraits, Asian and lies in the timing of speciation events: the elapids American coral snakes, the sea krait Laticauda, and apparently underwent a spectacular adaptive radia- the Bougainville Island Parapistocalamus) and the tion soon after reaching Australia, such that diver- ‘‘palatine draggers’’ (terrestrial Australo-Papuan elap- gences are ancient even within genera. Indeed, intrage- ids except Parapistocalamus, plus hydrophiid sea neric divergences are almost as large as intergeneric snakes). This division largely corresponds to the com- divergences. Although this timing means that our se- monly used families Elapidae and Hydrophiidae (or quence data cannot fully resolve phylogenetic relation- subfamilies Elapinae and Hydrophiinae) for ‘‘elapines’’ ships among the Australian elapids, the data suggest a and ‘‘hydrophiines’’ (Smith et al., 1977), except that close relationship of the following clades: Pseudonaja with Oxyuranus; Ogmodon with Toxicocalamus; Deman- recent studies have supported the affinity of Laticauda sia with Aspidomorphus; Echiopsis with Denisonia; the with hydrophiines (Cadle and Gorman, 1981; Mao et ‘‘Notechis’’ lineage with Drysdalia coronoides; and Rhi- al., 1983; Schwaner et al., 1985; Slowinski et al., 1997; noplocephalus and Suta with Drysdalia coronata. At Keogh, 1997, 1998a). These phylogenetic conclusions least two of the Australian genera (Drysdalia and have been based on an array of data sets involving Simoselaps) appear to be paraphyletic. These se- external and internal morphology, immunological dis- tances, and biochemical traits. Recently, Keogh (1998a) 1 Present address: Division of Botany and Zoology, Australian examined relationships among representatives of the National University, Canberra, ACT 0200, Australia. major elapid clades based on mitochondrial DNA se- 67 1055-7903/98 $25.00 Copyright ௠ 1998 by Academic Press All rights of reproduction in any form reserved. 68 KEOGH, SHINE, AND DONNELLAN quences. In this paper these data plus homologous TABLE 1 sequences gathered from representatives of the major List of Terrestrial Hydrophiine Genera with Com- hydrophiine lineages are used to present a more de- mon Names, Number of Species (Primarily after tailed analysis of phylogenetic relationships among Hutchinson, 1990), and Whether They Are Oviparous hydrophiine snakes. or Viviparous McDowell’s (1970) strong evidence for hydrophiine monophyly has been accepted in recent elapid classifica- Ovi- tions (Smith et al., 1977; Golay et al., 1993). With the Number parous/ of vivi- addition of Laticauda, hydrophiine monophyly has Genus Common name species parous been well supported by other diverse data sets includ- ing immunological distance (Cadle and Gorman, 1981), Australian elapids venom protein sequences (Slowinski et al., 1997), and Acanthophis Death adders 31 V Austrelaps Copperheads 3 V mitochondrial DNA sequences (Keogh, 1998a). The Cacophis Crowned snakes 4 O terrestrial hydrophiine radiation is entirely distributed Demansia Whip snakes 6 O in the Australo-Papuan region and comprises 27 genera Denisonia Ornamental snakes 2 V and 102 species (Table 1). The radiation includes a Drysdalia White-lipped snakes 4 V number of medically important groups such as the Echiopsis Bardick 2 V Elapognathus Little brown snake 1 V viviparous tiger snakes, copperheads, rough-scaled Furina Naped snakes 5 O snake, and death adders and the oviparous brown Hemiaspis Swamp snakes 2 V snakes, black snakes, taipans, whip snakes, and New Hoplocephalus Broad-headed snakes 3 V Guinea small-eyed snake. However, most of the radia- Notechis Tiger snakes 2 V tion is composed of relatively small, primarily fossorial, Oxyuranus Taipans 2 O Pseudechis Black snakes 6 O and innocuous species. Pseudonaja Brown snakes 7 O Much of the work devoted to terrestrial hydrophiine Rhinoplocephalus Small-eyed snake 6 V relationships has been concerned only with the Austra- Simoselaps Coral snakes 12 O lian species, in an attempt to address the high degree of Suta Black-headed snakes 10 V Tropidechis Rough-scaled snake 1 V taxonomic instability which has dominated the group Vermicella Bandy-bandy snakes 5 O (reviewed in Mengden, 1983), despite broad consensus Melanesian elapids that the endemic Melanesian genera (with the possible Aspidomorphus NG crowned snakes 3 O exception of Parapistocalamus) and 20 Australian gen- Loveridgelaps Solomons small-eyed snake 1 O? era are members of a single clade (McDowell, 1967, Micropechis NG small-eyed snake 1 O Ogmodon Fijian bola 1 O 1969a, 1969b, 1970; Schwaner et al., 1985; Keogh, Parapistocalamus Hediger’s coral snake 1 O? 1998a). McDowell (1967, 1969a, 1969b, 1970) was the Salomonelaps Solomons coral snake 1 O first to address the problem within an evolutionary Toxicocalamus NG forest snakes 9 O framework; he identified a number of putative ‘‘natural Note. All terrestrial hydrophiine genera were sampled except groups’’ through the descriptive study of cranial osteol- Elapognathus and Parapistocalamus for which no tissue samples ogy, myology, and hemipenis anatomy. McDowell’s phy- were available. The division between Australian and Melanesian logenetic hypotheses stimulated a series of studies that genera presented here simply represents major geographic distribu- addressed relationships among Australian elapids with tions. Some ‘‘Australian’’ species also occur in New Guinea (NG). diverse data sets, including (i) soft anatomy and other primarily morphological characters (Wallach, 1985, hemipenis morphology (Keogh, 1998b). Further, most Fig. 1a); (ii) karyotypes and allozyme electrophoresis authorities accept that true sea snakes evolved from (Mengden, 1985a, Fig. 1b); (iii) immunological distance within this viviparous lineage (McDowell, 1969b, 1972; (Schwaner et al., 1985); (iv) ecology and morphology Minton and da Costa, 1975; Cadle and Gorman, 1981; (Shine, 1985); and (v) hemipenis anatomy (Keogh, Minton, 1981; Schwaner et al., 1985; Gopalakrishna- 1998b, Fig. 1c). The 1985 studies culminated in a kone and Kochva, 1990; Slowinski et al., 1997; Keogh, well-accepted generic-level classification of Australian 1998a). Nonetheless, a number of conflicts remain, elapids (Hutchinson, 1990). stimulating us to gather sequence data in an attempt to Although the conclusions of these studies differed in clarify phylogenetic relationships among the Austra- several respects, their authors were in broad agree- lian and Melanesian proteroglyphs and their marine ment on some significant points. For example, Shine’s relatives. (1985) suggestion that the viviparous Australian elap- ids comprise a monophyletic lineage (with the excep- MATERIALS AND METHODS tion of Pseudechis porphyriacus) was supported by evidence
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