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. parvivipara the nominal species P. pseudoexigua from Downloaded from http://meridian.allenpress.com/rrimo/book/chapter-pdf/2643123/rzsnsw_1999_031.pdf by guest on 28 September 2021 which are considered to be sibling species Taiwan. This species has a planktonic (Dartnall 1971^ It also included P lecithotrophic larva (Chen and Chen 1992), pseudoexigua pacifica from Japan, which is whereas P. pseudoexigua from near the type viviparous (Komatsu et al. 1990). The results locality in central Queensland is viviparous. also indicated that P. pseudoexigua from With the discovery that P. pseudoexigua is Queensland and Taiwan are different species. viviparous there are now four asteroid species With feeding larvae representing the ancestral known to have intragonadal development, state, this clade exhibits four changes in the others being P. vivipara, P. parvivipara and development; planktotrophy {P. regularis), P. p. pacifica. planktonic lecithotrophy [P. pseudoexigua The tree topology placed the Australian Taiwan), benthic lecithotrophy {P. exigua), Patiriella into two clades, largely in agreement intragonadal lecithotrophy through a well- with previous systematic studies (Dartnall developed brachiolaria {P. pseudoexigua 1971). The clade with P. exigua, P. pseudoexigua, Queensland) and intragonadal lecithotrophy P. vivipara and P. parvivipara corresponds through a reduced brachiolaria {P. vivipara and to Dartnall's "exigua" group, while the P. parvivipara). clade containing P. gunnii and P. brevispina The other clade included the multi-armed corresponds to Dartnall's "gunnii" group. In species, P. calcar, P. gunnii and P. brevispina. contrast with the earlier study, a distinct The phylogeny indicated that P. gunnii from "regularis" group is not supported. eastern and western Australia are different Embryological evidence indicates that species, while P. brevispina from eastern ontogenetic processes have been modified in and western Australia are the same species. Patiriella and the molecular data indicate that This clade exhibits one change in develop- these changes occurred over a relatively short ment, from ancestral planktotrophy to evolutionary time frame (Byrne and Cerra planktonic lecithotrophy {P. calcar, P. gunnii 1996; Hart et al. 1997). It appears that life and P. brevispina). history traits in Patiriella have evolved freely, contrary to the widely assumed evolutionary DISCUSSION conservatism of early development (see Raff 1996). Patiriella is a speciose taxon in Australia and life history evolution appears to have Associated with their low dispersal life played an major role in the divergence of history, P. vivipara and P. parvivipara have the the species examined here. Divergence times most restricted distribution known for the calibrated from substitution rates measured Asteroidea. Details of the distribution of for the COI and tRNA genes in the geminate the viviparous P. pseudoexigua in Queensland Oreaster species from either side of the are not known. P. vivipara is endemic to Panamanian land bridge indicate that this southeastern Tasmania where it is recorded divergence occurred within the last 10 Mya from seven locations (Fig. 4). P. parvivipara (Hart et al. 1997). Some life history changes is restricted to the west side of the Eyre are recent, particularly the evolution of Peninsula where it is recorded from five viviparity, <2 Mya P. vivipara and P parvivipara locations (Fig. 5). Both species have a and within the last 0.5 Mya for P p. pacifica. geographic distribution of 150-300 km. This extremely limited distribution, together The phylogeny revealed that neither Asterina with their extended brood care indicate nor Patiriella are monophyletic (Hart et al.

June 1999 The Other 99%. The Conservation and Biodiversity of Invertebrates 191 Downloaded from http://meridian.allenpress.com/rrimo/book/chapter-pdf/2643123/rzsnsw_1999_031.pdf by guest on 28 September 2021 Figure 4 (left). Distribution of Patiriella vivipara, a species endemic to south- eastern Tasmania. This species is currently known to occur at the sites indicated here as solid squares. A seventh site, the Sorrell Causeway, lies immediately to the east of Midway Point. ^Tessellated Pavement

Fortescue Bay Downloaded from http://meridian.allenpress.com/rrimo/book/chapter-pdf/2643123/rzsnsw_1999_031.pdf by guest on 28 September 2021

'—M Daniefi Figure 5 (below). Distribution of Patiriella parvivipara, a species endemic to the Eyre Peninsula, South Australia. This species is currently known rsTny 20 Kilometers to occur at the five sites indicated here as solid squares, (updated from Keough and Dartnall 1978).

Ceduna 80 Kilometers Whittlebee ^Point

Figure 3 (opposite). Adults aboral view. A. P. regularis, EYRE a New Zealand native PENINSULA thought to be introduced to Tasmania in association Cape with shell fish (Dartnall Labatt 1971), has planktotrophic larvae, x 0.5 B. P. calcar, common in southeastern Australia has planktonic lecithotrophic larvae x 0.75. C. P brevispina x 0.8 and D. P. gunnii X 1.5; common around the south coast of Australia have planktonic lecithotrophic larvae. E. P. exigua, common in south- GREAT eastern Australia has benthic AUSTRALIAN lecithotrophic larvae, x 2.0, BIGHT F. P pseudoexigua x 2.0, G. P vivipara x 2.5, and H. P parvivipara x 7.0 have intragonadal lecithotrophic larvae and are endemic to north-east Queensland, south- east Tasmania and the Eyre Peninsula, respectively.

June 1999 The Other 99%. The Conservation and Biodiversity of Invertebrates 193 P, regularis

P. pseudoexigua N Downloaded from http://meridian.allenpress.com/rrimo/book/chapter-pdf/2643123/rzsnsw_1999_031.pdf by guest on 28 September 2021

— P, p. pacifica P. pseudoexigua

P. exigua

P. vivipara

P. parvivipara

P. calcar P. gunnUE

— P, gunnii W — P. brevispina E

P. brevispina W

Figure 6. Phylogenetic relationships among Patiriella modified from Hart et al. 1997 and with separation of F pseudoexigua from Queensland and P. pseudoexigua (N) from Taiwan. The brachiolaria larva of each species is also illustrated. their ranges are unlikely to increase. The Byrne, M. and Cerra, A., 1996. Evolution of intragonadal populations of P. vivipara have declined since development in the diminutive asterinid sea stars the early surveys in the 1970s. This decline Patiriella vivipara and P parvivipara with an overview appears to be associated with anthropogenic of development in the Asterinidae. Biological Bulletin 191: 17-26. influences and habitat change (Prestedge 1998). In 1998 P. vivipara was listed as Chen, B.-Y. and Chen, C.-R, 1992. Reproductive cycle, endangered under the Tasmanian Threatened larval development, juvenile growth and population Species Protection Act 1995. The important dynamics of Patiriella pseudoexigua (Echinodermata: Asteroidea) in Taiwan. Marine Biology 113: 271-80. insights on life history evolution that can be obtained from the viviparous Patiriella, and Clark, A. M., 1993. An index of names of recent the apparent decline of P. vivipara, emphasizes Asteroidea. Part 2. Valuatida. Echinoderm Studies 4: 187-366. the need for detailed surveys to determine their current population status. Efforts are Dartnall, A, J., 1969. A viviparous species of Patiriella (Asteroidea, Asterinidae) from Tasmania. Proceedings presently focused on protection of P. vivipara of the Linnean Society of New South Wales 93: 294-96. and its habitat. This effort should be extended to the other viviparous Patiriella. Dartnall, A. J., 1971. Australian sea stars of the genus Patiriella (Asteroidea, Asterinidae). Proceedings of the

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ACKNOWLEDGEMENTS Hart, M. W., Byrne, M. and Smith, M. J., 1997. Molecular Many thanks to colleagues for providing phylogenetic analysis of life-history evolution in specimens, particularly, C.-P. Chen, H. Lessios, asterinid starfish. Evolution 51: 1846-859. S. McKillup and G. Prestedge. Assistance was Keough, M. J. and Dartnall, A. J., 1978. A new species provided by G. Anderson and P. Cisternas. of viviparous asterinid asteroid from Eyre Peninsula, South Australia. Records of the South Australia Museum M. Keough is thanked for recent information 17: 407-16. on the distribution of P. parvivipara. We thank the Electron Microscope Unit of the University Komatsu M., Kano, Y. T. and Oguro, C., 1990. Develop- ment of a true ovoviviparous sea star, Asterina of Sydney for use of facihties. This research pseudoexigua pacifica Hayashi. Biological Bulletin 179: was supported by NSERC (Canada) and the 254-63. ARC (Australia). Palumbi, S., 1997. A star is born. Nature 390: 556-57.

REFERENCES Prestedge, G. K., 1998. The distribution and biology of Patiriella vivipara (Echinodermata: Asteroidea: Byrne, M., 1995. Changes in larval morphology in Asterinidae) a sea star endemic to southeast Tasmania. the evolution of benthic development by Patiriella Records of the Australian Museum 50: 161-70. exigua (Asteroidea), a comparison with the larvae of Patiriella species with planktonic development. Raff, R. A., 1996. The Shape of Life. University of Chicago Biological Bulletin 188: 293-305. Press: Chicago. Rowe, F. W. E. and Gates, J., 1995. Echinodermata. Byrne, M., 1996. Viviparity and intragonadal cannibalism Zoological Catalogue of Australia Vol. 33. Melbourne: in the diminutive sea stars Patiriella vivipara and CSIRO: Australia. P. parvivipara (family Asterinidae). Marine Biology 125: 551-67.

Byrne, M. and Barker, M. F., 1991. Embryogenesis and larval development of the asteroid Patiriella regularis viewed by light and scanning electron microscopy. Biological Bulletin 180: 332-45.

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