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Molecular Phylogeny of Nemadactylus and Acantholatris (Perciformes: Cirrhitoidea: Cheilodactylidae), with Implications for Taxonomy and Biogeography C

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Molecular Phylogeny of Nemadactylus and Acantholatris (Perciformes: Cirrhitoidea: Cheilodactylidae), with Implications for Taxonomy and Biogeography C Molecular Phylogenetics and Evolution Vol. 13, No. 1, October, pp. 93–109, 1999 Article ID mpev.1999.0622, available online at http://www.idealibrary.com on Molecular Phylogeny of Nemadactylus and Acantholatris (Perciformes: Cirrhitoidea: Cheilodactylidae), with Implications for Taxonomy and Biogeography C. P. Burridge School of Zoology, University of Tasmania, GPO Box 252-05, Hobart, Tasmania 7001, Australia Received July 21, 1998; revised November 6, 1998 There are five recognized species of Nemadactylus. The species of Nemadactylus and Acantholatris are Four of these are restricted to the waters of Australia perciform fishes with representatives in each ocean of and New Zealand, and the remaining species occur the Southern Hemisphere. Mitochondrial DNA se- along the east coast of South America (Fig. 1). One quences were obtained from all five species of Nema- species, commonly called ‘‘king tarakihi,’’ has only dactylus, two of the three Acantholatris species, and recently been proposed (Roberts, 1993; Smith et al., several outgroup taxa. Analysis of cytochrome b se- 1996). The record of N. macropterus at Saint Paul and quences placed A. monodactylus and A. gayi within an Amsterdam Island by Agnot (1951) was a misidentifica- otherwise entirely Nemadactylus clade, suggesting that these genera are synonymous. The Acantholatris se- tion according to Duhamel (1989). Acantholatris is not quences were also very similar to those from three of represented in the waters of Australia or New Zealand. the Nemadactylus species, despite their geographic Instead, its three members occur around isolated is- separation. Analysis of D-loop sequences paralleled lands and seamounts such as Juan Ferna´ndez and the the cytochrome b results, but provided greater resolu- Desventuradas in the southeastern Pacific, and those tion of species relationships. Nemadactylus sp. and A. which form a loose chain from Tristan da Cunha and gayi are transoceanic sister taxa. Polytypic clades Gough Island in the South Atlantic, to Saint Paul and observed for N. macropterus and A. monodactylus most Amsterdam Islands in the Indian Ocean (Fig. 1). likely reflect incomplete sorting of mitochondrial DNA The taxonomy of these species as based on external lineages. It is proposed that this group dispersed and characteristics has been problematic. Although Allen radiated during the last 0.6–2.6 million years, and the and Heemstra (1976) synonymized Acantholatris with possible mechanisms of this process are Cheilodactylus, the characters described by Gill (1862) discussed. ௠ 1999 Academic Press and Smith (1980), particularly the presence of a rela- tively long and narrow anal fin, distinguish Acanthola- tris from the cheilodactylid genera Cheilodactylus, Chi- INTRODUCTION rodactylus, and Dactylophora (Lamb, 1990). While the The species of Nemadactylus Richardson, 1839, and remaining cheilodactylid genus Nemadactylus shares Acantholatris Gill, 1862, are marine perciforms which the majority of characteristics which define Acanthola- occur in subtropical to cool-temperate waters through- tris, including the long narrow anal fin, these genera out the Southern Hemisphere (Fig. 1). Juveniles and have been separated primarily on the number of anal adults occur demersally over sand or reef substrates, at fin rays, with the former having 14–19 and the latter depths of 1–350 m (Annala, 1987; Wo¨hler and Sa´nchez, 10–12 (Gill, 1862; Lamb, 1990). 1994; Andrew et al., 1995). Movements of juveniles and Nemadactylus bergi and A. gayi have been called adults appear limited, with a gradual migration into Cheilodactylus in recent nonsystematic literature (e.g., deeper waters with age (Annala, 1987; Andrew et al., Mele´ndez and Villalba, 1992; Wo¨hler and Sa´nchez, 1995). However, a common trait of these and related 1994) and were also indexed as Acantholatris in the taxa is an offshore pelagic larval phase of 7–12 months systematic work by Greenwood (1995). These species in duration, which implies high dispersal capabilities are obviously not members of Cheilodactylus, given (Annala, 1987; Andrew et al., 1995). These species their relatively long and narrow anal fins, and since mature at 2–6 years and serially spawn large numbers they have anal fin ray counts of 14–15 and 12 they of small eggs (Annala, 1987; Andrew et al., 1995; should be referred to as Nemadactylus and Acanthola- Jordan, 1997); maximum ages exceed 25 years (Andrew tris, respectively (Lamb, 1990). et al., 1995; Jordan, 1997). N. bergi and N. macropterus are morphologically 93 1055-7903/99 $30.00 Copyright ௠ 1999 by Academic Press All rights of reproduction in any form reserved. 94 C. P. BURRIDGE FIG. 1. Distribution of Nemadactylus and Acantholatris species. Ns, Nemadactylus sp.; Nm, N. macropterus; Nb, N. bergi; Nd, N. douglasii; Nv, N. valenciennesi; Am, A. monodactylus; Av, A. vemae; Ag, A. gayi; ?, possible records of A. gayi (R. Mele´ndez C., Museo Nacional de Historia Natural, Santiago, Chile, 1998, pers. comm.). similar, but have been distinguished by the width of the and the external characteristics listed above. The famil- supra-cleithrum relative to the diameter of the eye, the ial allocation of these genera does not influence this relative lengths of their thickened pectoral fin rays, and study, and they are referred to as cheilodactylids pend- lateral line scale counts (Norman, 1937; Lamb, 1990). ing familial revision. However, two of these differences are not consistent In addition to their taxonomic uncertainties, the among the holotype and paratypes of N. bergi (R. W. G. distribution patterns and potentially high dispersal White, University of Tasmania, Australia, 1995, pers. capabilities of Nemadactylus and Acantholatris make comm.), and the separate status of this species requires them interesting subjects for a molecular phylogenetic justification. study. The biogeography and radiation of these and Nemadactylus and Acantholatris are usually allo- similarly distributed fishes has attracted some atten- cated to the Family Cheilodactylidae (Allen and Heem- tion (Eschmeyer and Hureau, 1971; Briggs, 1974; Wil- stra, 1976; Smith, 1980; Lamb, 1990). However, a son and Kaufmann, 1987; Collette and Parin, 1991; recent systematic study based on urohyal morphology Andrew et al., 1995), but no molecular studies have suggested that these genera should be reallocated to a been conducted. Members of the rock lobster genus cirrhitoid sister family, the Latridae (Greenwood, 1995). Jasus have distributions and dispersal capabilities Nemadactylus and Acantholatris are clearly distin- similar to Nemadactylus and Acantholatris, and their guished from all other cheilodactylid and latrid genera radiation, together with that of the related genus by both preliminary molecular data (Burridge, unpubl.) Panulirus, have received much attention (Pollock, MOLECULAR PHYLOGENY OF Nemadactylus AND Acantholatris 95 1990, 1992, 1993; George, 1997), including two molecu- material. Symmetric PCR amplifications were con- lar phylogenetic studies (Brasher et al., 1992; Ovenden ducted in 50-µL volumes, containing 1.0 units of Taq et al., 1997). The theories regarding the radiation of DNA polymerase (Promega), 5 µL of 10ϫ reaction these rock lobsters may well be applicable to much of buffer (Promega), 200 µM dNTPs, 0.5 µM each oligo- the Southern Hemisphere marine fauna with similar nucleotide primer, 1.5–2.5 mM MgCl2, and 25–100 ng species distributions and dispersal capabilities. genomic DNA. The oligonucleotide primers employed The aim of this study was to obtain molecular data were L14841 and H15149 for a 307-bp region of cyto- from species of Nemadactylus and Acantholatris that chrome b (Kocher et al., 1989) and proline-light (5Ј would clarify their taxonomy and provide phylogenetic AACTC TCACC CCTAR CTCCC AAAG 3Ј) and D-loop- information about their radiation with respect to biogeo- heavy (5Ј GGCCC TGAAR TAGGA ACCAR ATG 3Ј) for graphic processes and events. Mitochondrial DNA se- the left domain of the D-loop. Primer L14724 (Pa¨a¨bo, quences were chosen as the type of data to be collected, 1990) was required to obtain clean cytochrome b se- for reasons of resolving power and accessibility (Meyer, quences in some instances. 1994). Thermal cycling conditions for the amplification of cytochrome b were 10 cycles of 94°C/30 s, 45°C/30 s, and MATERIALS AND METHODS 72°C/60 s, followed by 30 cycles of 94°C/30 s, 55°C/30 s, and 72°C/60 s. Conditions for the amplification of Frozen or ethanol-preserved muscle and liver tissues D-loop sequences were identical with the exception of were obtained from all species of Nemadactylus and annealing being conducted at 60°C. An initial denatur- Acantholatris with the exception of A. vemae, for which ation of 94°C/5 min and a final extension of 72°C/10 min only formalin-fixed material was easily accessible (Table were employed for both templates. The results of PCR 1). Material from representatives of the remaining were assessed by 1.0% agarose gel electrophoresis, with cheilodactylid genera and Cirrhitus splendens (Cirrhiti- visualization under UV radiation after ethidium bro- dae) were also obtained for use as outgroups. The mide staining. Cirrhitidae is considered the most plesiomorphic of the Templates were gel purified using the QIAquick Gel five cirrhitoid families (Greenwood, 1995). Extraction Kit (Qiagen). DNA sequences were deter- Total DNA was extracted from approximately 40 mg mined using either the fmol DNA sequencing system of tissue following a standard CTAB phenol-chloroform (Promega) with [␥33P]ATP end-labeled primers, or the procedure (Hillis et al., 1990). The technique of Shed- ABI PRISM BigDye Terminator Cycle Sequencing lock et al. (1997) was employed for the A. vemae Ready Reaction Kit (Applied Biosystems Inc.). Both light and heavy strands were sequenced for each tem- TABLE 1 plate, enabling the verification of character states. D-loop sequences were aligned using CLUSTALW 1.7 Collection Details of Nemadactylus and Acantholatris (Thompson et al., 1994). Individuals Analyzed To test for the presence of certain character states, PCR-amplified D-loop fragments were digested with Indi- Species Collection site Month/year viduals Dpn II and Hinc II restriction endonucleases.
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