Biogeography and Phylogeny of the New Zealand Cicada Genera (Hemiptera : Cicadidae) Based on Nuclear and Mitochondrial DNA Data
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UC Riverside UC Riverside Previously Published Works Title Biogeography and phylogeny of the New Zealand cicada genera (Hemiptera : Cicadidae) based on nuclear and mitochondrial DNA data Permalink https://escholarship.org/uc/item/9bh6k6cm Journal Journal of Biogeography, 31(4) ISSN 0305-0270 Authors Arensburger, P Buckley, T R Simon, C et al. Publication Date 2004-04-01 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Journal of Biogeography (J. Biogeogr.) (2004) 31, 557–569 ORIGINAL Biogeography and phylogeny of the New ARTICLE Zealand cicada genera (Hemiptera: Cicadidae) based on nuclear and mitochondrial DNA data Peter Arensburger1*, Thomas R. Buckley2, Chris Simon3, Max Moulds4 and Kent E. Holsinger3 1Department of Entomology, University of ABSTRACT California at Riverside, Watkins Drive, CA, Aim Determine the geographical and temporal origins of New Zealand cicadas. USA, 2Landcare Research, Mt Albert, Auckland, New Zealand, 3Department of Location New Zealand, eastern Australia and New Caledonia. Ecology and Evolutionary Biology, University of Connecticut, CT, USA, 4Entomology Methods DNA sequences from 14 species of cicadas from New Zealand, Department, Australian Museum, Sydney, Australia, and New Caledonia were examined. A total of 4628 bp were analysed NSW, Australia from whole genome extraction of four mitochondrial genes (cytochrome oxidase subunits I and II, and ribosomal 12S and 16S subunits) and one nuclear gene (elongation factor-1 alpha). These DNA sequences were aligned and analysed using standard phylogenetic methods based primarily on the maximum likelihood optimality criterion. Dates of divergences between clades were determined using several molecular clock methods. Results New Zealand cicadas form two well-defined clades. One clade groups with Australian taxa, the other with New Caledonian taxa. The molecular clock analyses indicate that New Zealand genera diverged from the Australian and New Caledonian genera within the last 11.6 Myr. Main conclusions New Zealand was likely colonized by two or more invasions. One NZ lineage has its closest relatives in Australia and the other in New Caledonia. These invasions occurred well after New Zealand became isolated *Correspondence: Peter Arensburger, from other land masses, therefore cicadas must have crossed large bodies of water Department of Entomology, University of to reach New Zealand. California at Riverside, Watkins Drive, CA 92521-0001, USA. Keywords: E-mail: [email protected] Cicada, New Zealand, phylogeny, molecular clock, dispersal. Australia, New Caledonia, New Zealand, and Africa. They are INTRODUCTION divided into five genera: Kikihia (14 species) Dugdale, While New Zealand contains many ancient ‘Gondwanan’ Maoricicada (14 species) Dugdale, Rhodopsalta (two species) elements, the presumed ancient age and origin of many New Dugdale, Notopsalta (two species) Dugdale, and Amphipsalta Zealand taxa has been challenged in recent years (Raven, 1973; (three species) Fleming. Nearly all New Zealand cicada species Dettman & Jarzen, 1990; Pole, 1994; Christidis et al., 1996; are endemic to the North and South Islands and to small Winkworth et al., 2002). Several studies have looked at the surrounding islands. The only exception is a species of Kikihia, origins of plants and vertebrates (Cooper et al., 1992; Waters & K. convicta (Distant), that is endemic to Norfolk Island Burridge, 1999; Chambers et al., 2001) but few have focused (Australia), located between New Zealand and the Australian on invertebrate taxa (e.g. Gleeson et al., 1998). We examined mainland. Such high levels of endemicity suggest that New the origins, both geographical and temporal, of a well-studied Zealand cicadas have been isolated for some time. New New Zealand insect group, the Cicadidae (order Hemiptera) Zealand separated from Gondwanaland 82 Ma and has (five genera, 36 described species + eight or more undescribed remained isolated ever since (Cooper & Millener, 1993). species). Therefore, present day New Zealand cicadas must be the New Zealand cicadas all belong to the tribe Cicadettini, a descendants of either Gondwanan species (i.e. older than cosmopolitan tribe in the southern hemisphere that is found in 82 Myr) or of species that were able to cross hundreds of ª 2004 Blackwell Publishing Ltd www.blackwellpublishing.com/jbi 557 P. Arensburger et al. kilometres of ocean to settle New Zealand; a remarkable feat literature (Dugdale, 1972) and molecular systematic studies for an insect not generally known for its dispersal abilities of Maoricicada (Buckley et al., 2001a,b) and Kikihia (Williams & Simon, 1995; de Boer & Duffels, 1996). The (P. Arensburger, pers. comm.). geographical origins of New Zealand cicadas have generally All five New Zealand genera were sampled. The single been traced to Australia or New Caledonia. Myers (1929), New Zealand species of the genus Notopsalta, N. sericea based on morphological evidence, hypothesized that all New (Walker, 1850), was sampled to represent the earliest branch Zealand cicadas were derived from a New Caledonian ancestor of the lineage leading both to Notopsalta and Amphipsalta. that invaded both New Zealand and Australia. However, This was suggested by molecular phylogenetic analyses (T.R. Dugdale (1972) believed that New Zealand cicadas were the Buckley et al., unpub. data), which show all three Amphips- result of several, perhaps as many as five (one for each genus) alta species and the one New Zealand Notopsalta species to separate invasions from Australia. Fleming (1975) believed that form a monophyletic polytomy with similar terminal branch these invasions occurred only after angiosperms had exten- lengths. sively radiated throughout New Zealand 65 Ma. To distinguish Australia contains over 100 described species within the between these hypotheses we determined the relationships tribe Cicadettini with many remaining to be described between New Zealand cicadas and potential source popula- (Moulds, 1990, M. Moulds unpub.). From the large number tions and estimated the date of arrival of cicadas into New of cicadettine species in Australia we chose a subset for this Zealand. study. Species in this subset were identified by Dugdale (1972) This study focused on possible source populations in and M.M. as likely relatives to New Zealand cicadas based on Australia and New Caledonia. While cicadas are found morphological features. In a pilot sequencing study, fragments throughout the South Pacific we limited ourselves to these (between 385 and 684 bp) of the cytochrome oxidase II (COII) two countries for a number of reasons. First, populations in gene were sequenced for eleven Australian Cicadettini (Cica- these countries had previously been suggested as possible detta arenaria (Distant), C. celis Moulds, C. denisoni (Distant), ancestors (Myers, 1929; Dugdale, 1972; Fleming, 1975). C. torrida (Erichson), C. puer (Walker, 1850), C. tristrigata Second, these are the two closest large land masses to New (Goding & Froggatt, 1904), C. labeculata (Distant), Urabunana Zealand and they share a recent geological history when all marshalli Distant, Birrima varians (Germar), Pauropsalta three were connected by the supercontinent of Gondwanaland. aktities Ewart, and P. annulata Goding & Froggatt, 1904). Third, the cicadas of New Zealand, Australia, and New As done by other systematists (e.g. Kim et al., 1999), species Caledonia are morphologically distinct from those of New with unusually long branches were eliminated in order to Guinea and other islands north-west of New Zealand (Duffels, minimize problems of long-branch attraction–uniting taxa at 1986). A distinct Australia – New Caledonia – New Zealand the tips of long branches because of parallel or convergent biogeographical region is supported by evidence in other taxa changes rather than homology–one of the most serious (Duffels, 1986). Fourth, all New Zealand cicadas belong to the problems in molecular phylogenetic analysis (Felsenstein, tribe Cicadettini and current taxonomy does not recognize 1978; Hendy & Penny, 1989; Swofford et al., 2001). Even if species of this tribe in South America. other screened Cicadettini had been more closely related to By using selected species from each country we established a New Zealand cicadas in terms of branching pattern, the large well-supported phylogeny containing all five New Zealand number of autapomorphies and shared convergent bases would genera as well as selected Australian and New Caledonian have made phylogenetic analysis difficult. Based on these genera. Furthermore, by using molecular sequence data we also sequencing results, two species (C. celis and C. puer) with short examined the timing of arrival of cicadas into New Zealand. branches (i.e. genetically less distant from the New Zealand cicadas) were chosen to represent the Australian Cicadettini. The relationships of the New Caledonian cicadas are less MATERIALS AND METHODS well understood than those of cicadas found in either New Zealand or Australia. Cicadas collected during a single Taxon sampling sampling trip in 1998 were identified by M. Boulard (Muse´um Cicadas collected in the field were either preserved in 95% d’Histoire Naturelle, Paris) and M. M. Two New Caledonian ethanol, frozen on dry ice, or both; followed by storage at cicadettine species were used in this study, Pauropsalta johanae )70 °C. Voucher specimens of each species were deposited in Boulard and Myersalna depicta (Distant), based on morpho- the entomology collection