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Life History Diversity and Molecular Phylogeny in the Australian Sea Star Genus Patiriella

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Life History Diversity and Molecular Phylogeny in the Australian Sea Star Genus Patiriella Life history diversity and molecular phylogeny in the Australian sea star genus Patiriella Maria Byrne,' Anna Cerra,' Mike W. Hart^^ and Mike J. Smith^ 'Department of Anatomy and Histology, F13, University of Sydney, New South Wales 2006 ^Institute of Molecular Biology and Biochemistry, Simon Fraser University, Burnaby, BC, Canada 'Biology Department, Dalhousie University, Halifax, Nova Scotia, Canada B3H 4JI The sea star genus Patiriella in Australia lias tlie greatest diversity of life histories known for the Asteroidea. While the adults have similar phenotypes and life styles, their larvae are highly divergent. Patiriella includes species with unmodified development through typical feeding bipinnaria and brachiolaria larvae and several patterns of modified development through non- feeding planktonic, benthic or intragonadal brachiolaria. Comparative embryology and molecular phylogeny indicate that divergence of Patiriella was closely tied to developmental change. Phylogenetic analysis divided the Patiriella species into two clades. With feeding larvae representing the ancestral state for these sea stars, one clade exhibited one identifiable change Downloaded from http://meridian.allenpress.com/rrimo/book/chapter-pdf/2643123/rzsnsw_1999_031.pdf by guest on 28 September 2021 in larval form, while the other clade exhibited four changes in larval form. Life history traits in Patiriella appear to have evolved freely, contrary to the widely assumed evolutionary conservatism of early development. The range of life histories exhibited by Patiriella'appears unique to these sea stars and is an important resource for investigation of the evolution of development. INTRODUCTION gonad dissection. P. regularis, a native of New Zealand, was collected from populations The diversity of the asteroid genus Patiriella established in the Derwent River Estuary, is an unusual feature of Australia's echinoderm Tasmania. P. gunnii, P. calcar and P. exigua fauna with at least eight species distributed were collected from Sydney. P. gunnii occurs around the coast from Western Australia from northern New South Wales to the south to north Queensland (Dartnall 1971; Keough coast of Western Australia (Fig. 1). P. calcar and Dartnall 1978). These sea stars are occurs from southern Queensland to the south a conspicuous and numerically important coast of Western Australia. P. exigua occurs component of many marine communities. The from northern New South Wales to the Eyre genus exhibits a striking diversity of life Peninsula. P. brevispina was collected from histories spanning the range of developmental Mornington, Victoria and is distributed from patterns seen in the Asteroidea (Keough Victoria to south-west Western Australia. and Dartnall 1978; Byrne and Barker 1991; P. vivipara, P. parvivipara and P. pseudoexigua Byrne 1995, 1996; Byrne and Cerra 1996). were collected from south-east Tasmania, With the planktotrophic larvae of P. regularis the Eyre Peninsula and central Queensland, representing the ancestral state (Byrne and respectively. The former two species have Barker 1991), the larvae of the lecithotrophic highly restricted distributions (Figs 4 and 5), developers present what appears to be the while the latter species occurs from central to sequential series of developmental change as northern Queensland. predicted by life history theory. Patiriella presents an ideal model with which to examine We analysed phylogenetic relationships hypotheses on the evolution of life history among species of Patiriella as detailed in Hart traits (Hart et al. 1997; Palumbi 1997). Here et al. (1997). Specimens of P. pseudoexigua were we present an overview of the developmental obtained from Taiwan. P. gunnii and P. brevispina diversity and phylogenetic relationships in from eastern and western Australia were also Patiriella. The phylogeny detailed in Hart included. We also include P. pseudoexigua et al. (1997) is extended with inclusion of pacifica from the north Pacific, a viviparous P. pseudoexigua from central Queensland. The species (Komatsu et al. 1990). Analyses were relationships among the Australian Patiriella based on complete sequences for a indicated by molecular data are compared with mitochondrial protein coding gene cytochrome those originally suggested by Dartnall (1971) oxidase I (CGI) and five mitochondrial tRNA based in systematic characters. genes (1923 bp total). We produced phylogenetic hypotheses using maximum parsimony in PAUP 3.1.1, neighbour joining in MATERIALS AND METHODS MEGA 1.02 and maximum likelihood in Development of eight species was docu- PHYLIP 3.5c. All three methods converged on mented in laboratory culture or through similar tree topologies (see Hart et al. 1997). Pp. 188-96 in The Other 99%. The Conservation and Biodiversity of Invertebrates ed by Winston Ponder and Daniel Lunney, 1999. Transactions of the Royal Zoological Society of New South Wales, Mosman 2088. h H 500km Downloaded from http://meridian.allenpress.com/rrimo/book/chapter-pdf/2643123/rzsnsw_1999_031.pdf by guest on 28 September 2021 F gunnii Q R brevispina P. Calcar [3 P- pseudoexigua TASMANIA P. regularis S p. exigua P. vivipara Figure 1. Distribution o{ Patiriella species in Australia. RESULTS brachiolaria (Fig. 2C). They have similar ontogenies and their larvae are indistinguish- Life History Patterns able. At the anterior end of the larvae the Planktotrophy. The broadcast spawner P. attachment complex comprises a large arm regularis (Fig. 3A) has a small egg (150/itm flanked by two smaller arms and a central diameter) and planktotrophic development adhesive disc. through typical feeding bipinnaria and Patiriella exigua (Fig. 3E) deposits large brachiolaria larvae (Figs 2A,B). The attach- eggs (390/xm diameter) on the shore and ment complex, required for settlement prior has a highly modified benthic brachiolaria to metamorphosis, develops at the brachiolaria (Fig. 2D). The eggs adhere to the substratum stage. This structure comprises one long and development proceeds without parental central arm with an adhesive disc at its base care. The larvae remain attached to the flanked on either side by short lateral arms. substratum by their hypertrophied attachment Development of the brachiolar complex complex comprised of three arms equal in reflects the larval habitat and extent of benthic length (Fig. 2D). attachment and thus provides a useful com- The intragonadal brooders Patiriella vivipara, parative landmark illustrating the evolution of P. parvivipara and P. pseudoexigua have the larval form in Patiriella (Figs 2B-F). most derived mode of development seen in Lecithotrophy. All the other Patiriella species the Asteroidea. Development occurs in the (Figs 3B-H) have lecithotrophic development, gonad and the juveniles emerge through i.e., development through yolky non-feeding the gonopore. P. vivipara and P. parvivipara larvae (Figs 2C-F). P calcar, P gunnii and have small eggs (130-150 ^tm diameter) and P brevispina spav/n large eggs (380-430/^m the larva has a vestigial attachment complex diameter) and develop through a planktonic (Fig. 2F). These species give birth to large June 1999 The Other 99%. The Conservation and Biodiversity of Invertebrates 189 Downloaded from http://meridian.allenpress.com/rrimo/book/chapter-pdf/2643123/rzsnsw_1999_031.pdf by guest on 28 September 2021 Figure 2. Larvae of Patiriella, ventral viev^f. B-F illustrate the differing morphology of the brachioiar attachment complex. A.B. P. regularis has planktotrophic bipinnaria (A) and brachiolaria (B) larvae. A from Byrne and Barker (1991). C. P. gunnii has a planktonic lecithotrophic brachiolaria. D. P exigua has a lecithotrophic benthic brachiolaria with a well developed brachioiar complex which serves as a tenacious attachment device for permanent benthic attachment. E. P pseudoexigua has a lecithotrophic intragonadal brachiolaria with a well-developed attachment complex. F. P. vivipara has a lecithotrophic intragonadal reduced brachiolaria with a vestigial attachment complex. From Byrne and Cerra (1996). A, adhesive disc; B, brachioiar arm, C, ciliated band. Scale bars: a-e 100/xm, f. 50/xm. 190 The Other 99%. The Conservation and Biodiversity of Invertebrates June 1999 1.0-5.0 mm diameter juveniles that remain 1997). At this stage it is not possible to close to the parent, a development mode discern between polyphyly or paraphyly for probably associated with their restricted these genus names. Recent morphological distributions (Figs 4 and 5). Post-metamorphic studies indicate that the name Asterina should growth is supported by intragonadal be restricted to Atlantic members of the cannibalism. By contrast P. pseudoexigua has Asterinidae (Rowe and Gates 1995). The need large 440 /xm eggs and a larva similar to the for several taxonomic changes is indicated planktonic lecithotrophic developers (Fig. 2E). by the phylogeny. As suggested in Hart et al. The juveniles exit from the gonopores at (1997) these include a revision of P. gunnii, 800/i,m diameter. splitting the east and western forms. The combination Patiriella pseudoexigua pacifica Molecular phylogeny (Hayashi) is listed as "new comb" by Clark Phylogenetic analysis divided the Patiriella (1993) and so this species need not be species into two clades (Fig. 6). One included referred to Asterina, a change supported by the the type species for the genus, R regularis. molecular data. A further recommendation This clade also included P. exigua, P. from the present study is a reassignment of pseudoexigua, P. vivipara and P.
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