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Phylogenetics of Planipapillus, Lawn-Headed Onychophorans of the Australian Alps, Based on Nuclear and Mitochondrial Gene Sequences Matthew V

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Phylogenetics of Planipapillus, Lawn-Headed Onychophorans of the Australian Alps, Based on Nuclear and Mitochondrial Gene Sequences Matthew V Molecular Phylogenetics and Evolution Vol. 21, No. 1, October, pp. 103–116, 2001 doi:10.1006/mpev.2001.0990, available online at http://www.idealibrary.com on Phylogenetics of Planipapillus, Lawn-Headed Onychophorans of the Australian Alps, Based on Nuclear and Mitochondrial Gene Sequences Matthew V. Rockman,*,1 David M. Rowell,* and Noel N. Tait† *Department of Botany and Zoology, Australian National University, Canberra, ACT 0200, Australia; and †Department of Biological Science, Macquarie University, Sydney, NSW 2109, Australia Received January 29, 2001; revised March 28, 2001 tide sequence studies have exposed a wealth of varia- We addressed phylogenetic relationships among tion indicative of extensive and ancient radiations of species of Planipapillus, a clade of oviparous onych- onychophorans in Australia and New Zealand (Briscoe ophorans from southeastern mainland Australia, to and Tait, 1995; Tait and Briscoe, 1995; Tait et al., 1995; create a framework for understanding the evolution of Gleeson et al., 1998; Trewick, 1998, 1999, 2000; Sun- the modified male head papillae used in mating in this nucks et al., 2000b). Rowell et al. (1995) demonstrated clade. We sequenced fragments of two mitochondrial a wide range of distinct karyotypes, with variation genes, COI and 12S rRNA, and a nuclear intron from evident even among sister species (Reid et al., 1995). the fushi tarazu gene, for individuals from 14 putative Finally, detailed studies of morphology have revealed species of Planipapillus and six outgroups. We ana- lyzed these data under both parsimony and likelihood that the molecular and karyotypic divergences are par- criteria, incorporating heterogeneous parameter fit- alleled by morphological differentiation, culminating ting guided by likelihood ratio tests. These analyses in the description of 64 species within Australia (Reid, result in strong, congruent support for many clades. 1996, 2000). One surprising result of these morpholog- We infer multiple independent origins of spikes in ical studies was the identification of a suite of modifi- Planipapillus male head structures. © 2001 Academic Press cations of the integument of the head of males, includ- ing patches of modified dermal papillae and eversible pits which, in some species, contain hardened tusks, INTRODUCTION spikes, or stylets (Tait and Briscoe, 1990; Reid, 1996, 2000). The description of mating behavior in Planipap- Onychophorans are soft-bodied terrestrial inverte- illus annae and Florelliceps stutchburyae indicate that brates with lobopodial limbs arranged segmentally these head structures function in the transfer of a along their trunks, each limb terminating in a pair of spermatophore to the posterior genital opening of fe- claws. Commonly called peripatus or velvet worms, males (Reid, 2000; Tait and Norman, 2001). they are widely distributed in southern hemisphere Given the new broad perspectives on onychophoran temperate regions and in the tropics. Onychophorans diversity, we have focused our attention on a single are vulnerable to desiccation and hence largely con- clade of closely related species belonging to Planipap- fined to moist, humid microhabitats, including leaf lit- illus Reid, 1996 to provide a better characterization of ter and the interior of decomposing logs, where they the features underlying the evolution of the Australian are predators on small invertebrates. onychophoran fauna. An understanding of the popula- Onychophorans are often considered evolutionarily tion- and species-level diversity is also critical for the static “living fossils” (Ghiselin, 1984) with affinities to conservation of these potentially threatened but poorly Cambrian forms (Ramskold and Junyuan, 1998), rela- known animals (New, 1995; Trewick, 1999). Planipap- tively unchanged in the more than 300 million years illus, a clade confined to the southeastern corner of since the Carboniferous (Thompson and Jones, 1980; mainland Australia, is of particular interest as prelim- Heyler and Poplin, 1988). Recent studies, however, inary studies indicated distinctive patterns of morpho- have revealed an extraordinary diversity among extant logical and chromosomal variation which, when ana- onychophorans at several levels. Allozyme and nucleo- lyzed together, may permit the development of an 1 inclusive model for the origin and radiation of this To whom correspondence should be addressed at present ad- dress: Department of Biology, Duke University, Box 90338, Durham, group. Planipapillus females are oviparous and pos- NC 27708. E-mail: [email protected]. sess ovipositors, features found only in some lineages 103 1055-7903/01 $35.00 Copyright © 2001 by Academic Press All rights of reproduction in any form reserved. 104 ROCKMAN, ROWELL, AND TAIT FIG. 1. Locality map for Planipapillus collection sites. confined to Australia and New Zealand (Reid, 1996). Twelve species have been described within Plani- The remaining species of Australian onychophorans papillus (Reid 1996, 2000). Whereas Planipapillus ap- are ovoviviparous with yolky eggs and give birth to pears to be monophyletic, a phylogenetic analysis active young. The evolutionary relationships among based on morphological characters did not resolve re- oviparous and ovoviviparous species are unresolved lationships within the clade (Reid, 2000). This may be (Reid, 1996; Gleeson et al., 1998), although the phylog- due to species diagnoses based largely on the male eny may be interpreted as implying that ovoviviparity modified head papillae, which by themselves are insuf- is the ancestral state in the Onychophora, with derived ficiently informative. Here we use an independent data oviparity having arisen on a number of occasions (Reid, set of nucleotide sequences to formulate hypotheses 1996). about the evolution of the head structure within Pla- Planipapillus males have a patch of reduced papillae nipapillus. These analyses also include species display- on the dorsal surface of their heads, just posterior to ing a variety of head structure types and female repro- the eyes. In some species, these patches are elaborated ductive strategies as outgroups. by the presence of spines on the posterior margin (Tait and Briscoe, 1990; Reid, 1996). The relationships MATERIALS AND METHODS among Planipapillus and other Australian genera pos- sessing head structures are uncertain. Reid (1996) con- Specimens sidered eversible head structures to be homologous to Specimens of Planipapillus were hand-collected modified papillae anterior to the eyes; such modified from 14 localities in New South Wales and Victoria, papillae are absent in Planipapillus. Thus, Reid’s anal- Australia (Fig. 1, Table 1). All specimens were collected ysis treated modified papillae posterior to the eyes (as from within or under rotting logs. Specimens from 5 of in Planipapillus) and anterior to the eyes (as in some the populations are referable to described Planipapil- other species and including eversible structures) as lus species on the basis of head structure morphology nonhomologous features. One of our goals is to place and locality as in Reid (1996, 2000). Others did not these head structures in a phylogenetic context as a conform to a species diagnosis or their identity is un- first step to understanding their homologies and evo- certain as they were collected from a locality previously lutionary histories. unsampled by Reid. All of these undiagnosed popula- Planipapillus PHYLOGENY 105 TABLE 1 Collection Data Species Locality Coordinates Modified papillae P. biacinaces Howman Gap, Vic 36° 51ЈS 147° 15ЈE Class 4 P. cyclus Combienbar, Vic 37° 28ЈS 148° 55ЈE Class 3 P. impacris Coolangubra, NSW 37° 01ЈS 149° 23ЈE Class 3 P. mundus Penderlea, NSW 36° 26ЈS 148° 30ЈE Class 1 P. taylori Brown Mt., NSW 36° 37ЈS 149° 21ЈE Class 2 P. sp. 1 Grassy Flat, NSW 36° 29ЈS 148° 08ЈE Class 1 P. sp. 2 Tom Groggin, NSW 36° 33ЈS 148° 08ЈE Class 1 P. sp. 3 Playground Rd, Vic 37° 35ЈS 147° 53ЈE Class 1 P. sp. 4 Bennison’s Lookout, Vic 37° 30ЈS 146° 41ЈE Class 1 P. sp. 5 Mt. Useful, Vic 37° 43ЈS 146° 32ЈE Class 6 P. sp. 6 Shannonvale, Vic 36° 55ЈS 147° 25ЈE Class 5 P. sp. 7 Bendoc, Vic 37° 09ЈS 148° 53ЈE Class 3 P. sp. 8 Dinner Plain, NSW 37° 01ЈS 147° 15ЈE Class 4 P. sp. 9 Bemm River, Vic 37° 40ЈS 148° 54ЈE Unknown tions differed chromosomally from otherwise morpho- Scanning Electron Microscopy logically similar species (D. M. Rowell et al., in press). Specimens were prepared for SEM according to Tait These populations are here designated by numerals and Briscoe (1990). following Rowell et al. (in press) as shown in Table 1 and by locality names. DNA Extractions, Primers, PCR, and Sequencing Reid (1996) described P. bulgensis from Tarra–Bulga Whole genomic DNA was extracted from body seg- National Park, but in approximately 6 person-days of ments after removal of the gut. Tissue was repeat- searching we were unable to collect any Planipapillus edly soaked in TE9 buffer (Shiozawa et al., 1992) for at this site, and we were thus unable to include this several hours to leach pigments, which may act as species in our sequencing efforts. Additionally, our col- PCR inhibitors (Sunnucks and Wilson, 1999). Tis- lection from Planipapillus sp. 9, Bemm River, included sues were then homogenized in 250 ␮l TE9 and in- no males, and so we were unable to characterize the cubated overnight at 65°C after the addition of 30 ␮l male head structure of this population. 20% SDS and 5 ␮l 10 mg/ml proteinase K. Protein The techniques of DNA preparation and scanning was precipitated with ammonium acetate, and
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