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Oogenic strategies in the evolution ofdevelopment in Patiriella (Echinodermata:Asteroidea)MARIA BYRNE a , ANNA CERRA b & JEFFREY T. VILLINSKI ba Department of Anatomy and Histology, F13 , University of Sydney , NSW, 2006,Australia Phone: +61 (2) 9351-5611 Fax: +61 (2) 9351-5611 E-mail:b Molecular Biology Institute and Department of Biology, Indiana University ,Bloomington, IN, 47405, USAPublished online: 01 Dec 2010.

To cite this article: MARIA BYRNE , ANNA CERRA & JEFFREY T. VILLINSKI (1999) Oogenic strategies in the evolution ofdevelopment in Patiriella (Echinodermata: Asteroidea), Invertebrate Reproduction & Development, 36:1-3, 195-202,DOI: 10.1080/07924259.1999.9652700

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Invertebrate Reproduction and Development, 36:l-3 (1999) 195-202 Balaban, Philadelphia/Rehovot 0168-8170/99/$05.00 0 1999 Balaban

Oogenic strategies in the evolution of development in Patiriella (Echinodermata: Asteroidea)

MARIA BYRNEI*, ANNA CERRA~ and JEFFREY T. VILLINSKI~ l ~ e ~ a r t m e n t of Anatomy and Histology, F13, University of Sydney, NSW 2006, Australia Tel. + 61 (2) 9351 -561 I; Fax +61(2) 9351 -281 3; email: mbryne@anatomy. usyd edu. au

2~olecular Biology Institute and Department ofBiology, Indiana Universiy, Bloomington, IN 47405, USA

Summary

The sea star genus Patiriella has the greatest diversity of life histories known for the Asteroidea. P. regularis has small eggs (150 pm diameter) and the ancestral planktotrophic larvae. P. calcar, P. gunnii, P. exigua and P. pseudoexigua have large eggs (390-440 pm diameter) and non-feeding lecithotrophic larvae. Two species with lecithotrophic larvae P. vivipara and P. parvivipara have secondarily evolved a small egg (135-150 pm diameter). We examined the oogenic strategies involved with evolution of egg size in these sea stars. Comparison of protein profiles, histochemistry and ultrastructure of the eggs of Patiriella indicated that the major changes underlying acquisition of a large egg involved enhanced deposition of lipid in some species and an increase in yolk reserves in others. The eggs of the planktotroph, P. regularis, and the benthic lecithotroph, P. exigua, contained an abundance of major yolk protein MYP. By contrast, the eggs of the planktonic lecithotrophs P. gunnii and P. calcar were dominated by lipid and the MYP appeared to be greatly reduced. The eggs of P. calcar contained an abundant protein which may be a truncated form of vitellogen. The small eggs of the viviparous species P. vivipara and P. parvivipara appear to be miniature versions of the eggs of the closely related P. exigua. Comparison of the eggs of Patiriella species with lecithotrophic development revealed among species variation in oogenesis. Depending on the species, the evolutionary modification of oogenesis appeared to be influenced by phylogenetic history and selection for egg characteristics with respect to the planktonic or benthic location of development.

Key words: Patiriella, oogenesis, asteroid, evolution, development

Introduction considered to represent the ancestral condition For many marine invertebrates the dispersive life (Strathrnann, 1993). Although there is increasing

history which involves release of small eggs and evidence that this is not the case for several taxa development through planktotrophic larvae is [review by McHugh and Rouse (1998)], the absence of

*corresponding author.

Proceedings of the 8th International Congress on Invertebrate Reproduction andDevelopment, Amsterdam, The Netherlunch, I &I 4 August 1998.

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homoplasious feeding larvae in the Echinodermata indicates that this paradigm still holds for this phylum (Wray, 1996; Hart et al., 1997). For echinoderms acquisition of a large egg and the associated increase in maternal investment is suggested to have freed larvae from the need to feed, resulting in the loss of feeding structures and a simplification in larval form (Mortensen, 192 1 ; Strathmann, 1993).

Although the evolution of development in echinoderms was inextricably linked to alterations in maternal provisioning, the oogenic mechanisms involved with increased egg size are not well- understood. Maternal nutrients provided to support embryogenesis are generally considered in terms of egg yolk protein and lipid. In most animals an increase in egg size is accomplished by enhanced deposition of yolk proteins (Wahli, 1988; del Pino, 1989). In echinoderms, however, increase in oocyte size is often accomplished by enhanced deposition of lipid reserves (Jaeckle, 1995). The egg cytoplasm is often dominated by large lipid droplets (Byme, 1999; Byme et al., 1999a) and, as a result, many of these eggs are positively buoyant. This trend has been taken to suggest the presence of selection for a positively buoyant egg in species with planktonic development to enhance fertilization success and to retain larvae in shallow water (Emlet et al., 1987). In contrast, echinoderms with benthic lecithotrophic development in egg masses or in association with parental care

asteroid genus Patiriella with different patterns of development (Fig. 1). These species diverged within the last 10 Mya yet present a full range of life histories (Fig. 1) (Hart et al., 1997; Byme et al., 1999b). The small eggs and planktotrophic larvae of P. regularis represent the ancestral life history (Byme and Barker, 1991). Several Patiriella species have large eggs and lecithotrophic development. For this study we included P. calcar, P. gunnii, P. exigua and P. pseudoexigua which have planktonic, benthic or intragonadal lecithotrophic brachiolaria larvae (Fig. 1). The species with the most derived life history, P. vivipara and P. parvivipara, have reduced intragonadal lecithotrophic brachiolaria that develop from small eggs. These eggs are secondarily reduced in size (Byme, 1996; Byme and Cerra, 1996; Hart et al., 1997). We examined yolk protein content and lipid deposition associated with evolution of oogenesis in these sea stars. The eggs of P. calcar, P. gunnii, P. exigua and P. pseudoexigua were examined to determine the oogenic strategies used to increase egg size whereas those of P. vivipara and P. parvivipara were examined to determine the strategies used to decrease egg size. If evolution of lecithotrophy in Patiriella with planktonic and benthic larvae was associated with selection for a positively and negatively buoyant eggs, respectively we expected this trend would be reflected in the lipid and protein profiles of the eggs.

would be expected to have negatively buoyant eggs with less emphasis on lipid. It appears that the extra Materials and Methods lipid reserves in some echinoid eggs are not used for embryogenesis and reflect selection for enhanced juvenile performance (Emlet and Hoegh-Guldberg, All specimens were collected from the intertidal 1997). Clearly, there are many possible selective forces zone. P. regularis and P. vivipara were collected in that may influence the size and composition of Hobart, Tasmania. P. exigua, P. calcar and P. gunnii echinoderm eggs. were collected from Sydney, NSW, and P.

In this study we describe the ultrastructure and pseudoexigua were collected from Rockhampton, Qld. protein composition of oocytes in species of the P. parvivipara were collected from the Eyre Peninsula,

I P. regularis - P

P. pseudoexigua - IL

P. psmiax igua - w - r r I P. exigua -EL

IJ. gunnii - PL

Fig. 1. Phylogenetic relationships among eight species of Patiriella (redrawn from Hart et al., 1997). The taxonomic status of P. pseudoexigua from Taiwan, needs to be revised [see Byme et al. (1999b)l. Symbols at the right indicate develop- mental mode. BL, benthic lecithotroph; IL, intragonadal lecithotroph; P, planktotroph; PL, planktonic lecithotroph.

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SA. The ovaries of P. regularis, P. exigua, P. gunnii and P. calcar were removed and treated with lo-' M I-methyladenine in filtered seawater to obtain mature oocytes (Kanatani, 1969). Advanced and mature oocytes of the species with intragonadal development, P. pseudoexigua, P. vivipara and P. parvivipara were obtained by dissection of the gonads or were examined in ovary sections.

Protein gel Spawned eggs obtained from several specimens of

P. regularis, P. exigua, P. calcar and P. gunnii were pooled and frozen at -70°C for protein analysis. The egg samples were homogenized in SDS sample buffer (Laemmli, 1970). Proteins were size separated by SDS- PAGE and the gel was stained with Coomassie Blue.

Light and electron microscopy For oocyte histochemistry (data not illustrated) the

ovaries of each of the seven Patiriella species were fixed in Bouin's fluid overnight, transferred through a graded ethanol series, followed by two changes in histoclear and transfer to paraffin. Sections (6 ym thick) were stained with the periodic-acid Shiff's (PAS) method which stains echinoderm yolk (Armant et al., 1986; Byme, 1989).

The spawned eggs or ovaries of P. regularis, P. calcar, P. exigua, P. pseudoexigua and P. vivipara were processed for transmission electron microscopy (TEM). Two fixation methods were used: seawater buffered glutaraldehyde and cacodylate buffered glutaraldehyde. In the first method, dissected gonads, spawned eggs or embryos were fixed in 2.5% glutaraldehyde in filtered seawater for 1 h at room temperature, rinsed several times in 2.5% NaHCO, (pH 7.2) and postfixed in 2% osmium tetroxide in 1.25% NaHCO, for 1 h at room temperature. The specimens were then washed in distilled water, dehydrated in graded ethanols and embedded in Spurr's resin. For the cacodylate method, specimens were fixed in 3% glutaraldehyde in 0.2M cacodylate buffer, for 2 h at 4OC with NaCl (30mg/ml) added to the primary fixative. They were then rinsed four times in 0.2M cacodylate buffer with reduced amounts of NaCl added to each rinse, with the final rinse containing no NaCl. This was followed by postfixation in 1% osmium tetroxide in 0.2M cacodylate buffer for 2h at 4°C. The specimens were finally washed in 0.2M cacodylate and distilled water, dehydrated in, graded ethanols and embedded in Spurr's resin.

To compare lipid inclusions the diameters of the largest lipid droplets in the eggs of P. regularis, P. calcar, P. exigua, P. pseudoexigua and P. parvivipara were compared by one factor analysis of variance (ANOVA). The data were square root transformed to achieve homogeneity of variance. Student-Neuman Keul's test were used for post hoc comparison of the lipid data. Significance heterogeneity of variance in the yolk granule data (Cochrans' test C= 0.5376,~ < 0.05) precluded analysis of these data by ANOVA.

Results

P. regularis had small (150pm diameter) negatively buoyant eggs. Several of the lecithotrophic developers had negatively buoyant eggs including the benthic eggs of P. exigua (390pm diameter) and the intragonadal eggs of P. vivipara and P. parvivipara (1 35 pm and 150 pm diameter, respectively). The planktonic eggs of P. calcar and P. gunnii (41 5 pm and 400pm diameter, respectively) were neutral to negatively buoyant. If disturbed, these eggs remained in the water column, but eventually sank. By contrast, the intragonadal eggs of P. pseudoexigua (440pm diameter) were positively buoyant and on removal from the gonad floated up to the water surface.

Egg protein gels A large molecular weight protein (-1 80 kD), the

major yolk protein (MYP) was very abundant in eggs of P. regularis and P. exigua. The abundance of MYP was greatly reduced in eggs of P. gunnii and was virtually undetectable in eggs of P. calcar (Fig. 2). P. calcar had a smaller abundant protein (-160 kD) which was less prevalent in the eggs of the other species. This protein may be a truncated form of vitellogen.

Yolk protein histochemistry In ovary sections stained with PAS, yolk granules

first appeared in early oocytes as red dots scattered in the cytoplasm. The PAS response of fully grown oocytes depended on the density of the yolk granules with respect to other egg constituents, particularly lipid. The eggs of P. regularis, P. calcar, P. gunnii, P. exigua, P. vivipara and P. parvivipara were uniformly PAS+. This reflected the abundance and relatively homogeneous distribution of yolk granules in the cytoplasm. The large benthic eggs of P. exigua produced a particularly intense PAS+ reaction

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Fig. 2. SDS-PAGE gel showing that the -180 kD MYP is abundant in eggs of P. regularis (Pr) and P. exigua (Pe), less abundant in eggs of P. gunnii (Pg) and virtually undetectable in eggs of P. calcar (PC). P. calcar has an abundant protein migrating at -160 kD which is less prevalent in the other species. The lanes are relatively equally loaded, as seen by comparing many of the protein bands across lanes (e.g., 47 kD, 73 kD and 109 kD).

indicating the presence of substantial yolk protein stores. In contrast, the eggs of P. pseudoexigua were weakly PAS+ staining a pale pink. This more diffuse staining response was due to the abundance of large lipid droplets in the cytoplasm which resulted in dis- persion of the yolk granules, largely to the egg cortex.

Ultrastructure of lipid and yolk reserves in the oocytes

Fully grown oocytes contained numerous organelles, including yolk granules, lipid droplets, cortical granules, vesicles and mitochondria (Fig. 3a-e). Yolk granules were electron-dense and membrane-bound, whereas lipid droplets were paler and lacked a limiting membrane. Across all the Patiriella species examined, the yolk granules and lipid droplets in these eggs ranged in diameter between 0.8-2.3 pm and 0.4-8.2 pm, respectively (Fig. 4). Yolk granules were abundant in the eggs of P. regularis and were distributed relatively uniformly (Fig. 3a), correlating with the uniform cytoplasmic PAS+ reaction of these oocytes. Although lipid droplets were also present in the eggs of P. regularis, they were small (0.4 pm diameter) and infrequent. The eggs of P. exigua and P. vivipara also contained abundant yolk granules (Fig. 3c,d). Lipid droplets were

also abundant in the eggs of these two species and had a mean diameter of 2.6 pm and 1.7 pm, respectively (Fig. 4). The oocytes of P. calcar and P. pseudoexigua were dominated by large lipid droplets (mean diameter 5.1 pm and 8.2 pm, respectively) which dwarfed the yolk granules dispersed among them (Fig. 3b,e).

ANOVA indicated that the size of the lipid droplets differed significantly (F= 86 1.0 1, p < 0.0 1) among Patiriella species (Fig. 4). Student-Neuman-Keul's test @ < 0.05) indicated the following trend in lipid droplet size: P. pseudoexigua > P. calcar > P. exigua > P. vivipara > P. regularis (Fig. 4).

Discussion

In general, egg size is a reliable predictor of developmental mode in echinoderms with a large egg typically associated with lecithotrophic development (Emlet et al., 1987; Strathmann, 1993). This relationship holds for Patiriella with the exception of the viviparous lecithotrophs, P. vivipara and P. vivipara, which had small eggs similar in size to those of the planktotrophic species P. regularis. Several of the lecithotrophic developers had large eggs which were similar in size, but which differed greatly in composition. The differences in the eggs of these recently diverged Patiriella species indicates that changes in egg size and maternal provisioning can occur over a relatively short evolutionary time frame (Hart et al., 1997). These changes include alterations in vitellogenic and lipogenic processes.

A common feature of vitellogen in many animal systems is its high molecular weight and abundance in eggs (Wahli, 1988; Li et al., 1998). As yet, the vitellogen in asteroid eggs has not been characterized. In echinoid eggs, this protein is so large (1 80 kD) and abundant that it is the single most conspicuous protein on Coomassie stained gels (Shyu et al., 1986; Scott et al., 1990; Byrne et al., 1999a). By analogy, due to its size (-1 80 kD) and prevalence, the MYP identified in the eggs of the planktotroph P. regularis and the benthic lecithotroph P. exigua is likely to be vitellogen. The PAS+ reaction of these oocytes is also

Fig. 3 (opposite). TEM of Patiriella eggs. A-C. Spawned eggs of P. regularis (A) , P. calcar ( B ) and P. exigua (C). D. Advanced oocyte in the ovary of P. vivipara. E. Ovum dissected from the ovary of P. pseudoexigua. C, cortical granules; L, lipid droplets; Y, yolk granules. Scale: 2.0pm.

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-.- Pr PC Pe Ppe Pv

Fig. 4. Egg size and diameter of yolk granules and lipid droplets in ~"atiriella eggs. The eggs are to scale. All shaded eggs sink or are negatively of neutrally bouyant, whereas the open circle indicates that only the eggs of P. pseudoexigua float. Bars are standard error.

characteristic of echinoderm eggs with abundant vitellogen (Armant et al., 1986; Byme, 1989). In contrast, the eggs of the planktonic lecithotrophs P. calcar and P. gunnii appeared to have a lower MYP content. Their PAS+ reaction, however, indicates that yolk is present in these eggs and yolk granules were seen in sections of P. calcar eggs. As reported for the large eggs of the echinoid Heliocidaris erythrogramma (Byme et al., 1999a), the increase in egg size of P. calcar and P. gunnii may result in a proportionate decrease in MYP relative to other egg proteins, but not an absolute reduction with respect to the ancestral state indicated by the eggs of P. regularis. Immuno- cytochemical verification of the identity of the MYP in Patiriella eggs was, not possible because an anti- vitellogenin antibody for asteroid vitellogenin is not available. Antibodies raised against echinoid

vitellogenin do not cross-react with the MYP of Patiriella (unpublished data).

The prevalence of MYP and the abundance of yolk granules in the eggs of P. regularis are characteristic of echinoderms with planktotrophic development (Armant et al., 1986; Reimer and Crawford, 1995). Like P. regularis, small echinoderm eggs also tend to have low lipid reserves (Jaeckle, 1995). The abundance of MYP in the large eggs of the benthic lecithotroph P. exigua was unexpected. In parallel with this result, yolk granules were conspicuous in these eggs. It appears that increased egg size in P. exigua involved enhanced vitellogenesis in addition to an increase in lipid stores. The abundance of MYP in the eggs P. exigua contrasts with the lower level of this protein in the eggs of the planktonic lecithotrophs P. calcar and P. gunnii. This difference may reflect selection for a strongly negatively buoyant egg in P. exigua which lays benthic egg masses (Byme, 1995).

In P. calcar acquisition of a large egg involved a change from production ofa yolk-dominated to a lipid- rich egg, a trend seen in many asteroids with planktonic lecithotrophic development (Jaeckle, 1995). The extensive lipid reserves in P. pseudoexigua, however, were not be expected in a species with non- dispersive intragonadal larvae. Evolution of this mode of development is unlikely to have been associated with selection for a positively buoyant egg. Insights into this apparent conflict can be obtained from the phylogenetic relationships among Patiriella (Hart et al., 1997). It appears that evolution of intragonadal development in P. pseudoexigua occurred through retention and internal fertilization of a large egg by an ancestor that had a lipid-rich egg and planktonic development similar to that seen in the closely related species from Taiwan (Fig. 1, Chen and Chen, 1992; Byrne et a]., 1999b). In contrast, evolution of intragonadal development in P. vivipara and P. parvivipara appears to have occurred through a P. exigua-like ancestor which had benthic egg masses (Hart et al., 1997). As might be expected from this relationship, the eggs of P. vivipara and P. parvivipara appear ultrastructurally to be a miniature version of the eggs of P. exigua.

The increase in maternal investment associated with lecithotrophic development in echinoderms was considered to reflect the requirement to sustain development to metamorphosis without feeding (Mortensen, 192 1). Counter to this suggestion, the small reduced eggs of the intragonadal lecithotrophs, P. vivipara and P. parvivipara support development to the juvenile stage (Byme, 1996; Byme and Cerra,

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1996). The metamorphic juveniles of these species are among the smallest known for asteroids and the additional reserves required to achieve independence of the parent are obtained by brood cannibalism. By inference, much of the extra nutrients in the large eggs of the other lecithotrophic Patiriella may not be required for embryogenesis. Indeed, comparison of the energy content of eggs and metamorphosed juveniles of lecithotrophic echinoderms and the energy use pattern in feeding and non-feeding development indicates that most of the provisions in large eggs are reserved for the post-metamorphic juvenile (Lawrence et al., 1984; Hoegh-Guldberg and Emlet, 1997). This phenomenon is readily observed in the embryos of P. pseudoexigua which extrude their maternally derived lipid reserves into the blastocoel where they are stored for the juvenile stage (Byme, unpub. obs). A similar phenomenon occurs in Heliocidaris erythrogramma and is suggested to be a strategy to enhance juvenile performance (Emlet and Hoegh-Guldberg, 1997).

In conclusion, although oogenesis in some Patiriella species appears to reflect the presence of selection forces associated with the benthic and planktonic environments in which the eggs are deposited, oogenesis in other species appears to largely reflect their phylogenetic history.

Acknowledgments

Assistance was provided by R. Smith and the staff of the Electron Microscope UnitiUniversity of Sydney. Dr. S. McKillup and H. and S. Sowden are thanked for collecting specimens. C. King is thanked for help with statistics. Prof. R. Raff is thanked for providing facilities. The research was supported by a grant from the Australian Research Council (MB) and a Training Grant from the National Institutes of Health (JTV).

References

Armant, D.R., Carson, D.D., Decker, G.L., Welply, J.K. and Lennarz, W.J., Characterization ofyolk platelets isolated from developing embryos of Arbacia punctulata. Dev. Biol., 113 (1986) 342-355.

Byrne, M., Ultrastructure of the ovary and oogenesis in the ovoviviparous brittlestar Ophiolepispaucispina (Echino- dermata: Ophiuroidea). Biol. Bull., 176 (1989) 79-95.

Byrne, M., Changes in larval morphology in the evolution of benthic development Patiriella exigua (Asteroidea: Asterinidae), a comparison with the larvae of Patiriella species with planktonic development. Biol. Bull., 188 (1995) 293-305.

Byrne, M., Viviparity and intragonadal cannibalism in the diminutive asterinid sea stars Patiriella vivipara and P. parvivipara. Mar. Biol., 125 (1996) 551-567.

Byrne, M., Echinodermata. In: Encyclopedia of Repro- duction, Vol. 1, E. Knobil and J.D. Neil (eds.), Academic Press, New York, 1999, pp. 940-954.

Byrne, M. and Barker, M.F., Embryogenesis and larval development of the asteroid Patiriella regularis viewed by light and electron microscopy. Biol. Bull., 180 (1991) 332-345.

Byrne, M. and Cerra, A., Evolution of intragonadal development in the asterinid sea stars Patiriella vivipara and P. parvivipara with an overview of development in the Asterinidae. Biol. Bull., 191 (1996) 17-26.

Byrne, M., Villinski, J.T., Cisternas, P., Seigel, R.K., Popodi, E. and Raff, R.A., Maternal factors and the evolution of developmental mode: Evolution of oogenesis in Heliocidaris erythrogramrna. Genes Dev. and Evol., (1 999a) 275-283.

Byme M., Cerra, A., Hart, M.W. and Smith M.J., Life history diversity and molecular phylogeny in the Australian sea star genus Patiriella. The Conservation and Biodiversity of Invertebrates, W. Ponder and D. Lunney (eds.), Trans. Royal Soc. New South Wales. 1999b, pp. 1-8.

Chen, B.-Y and Chen, C.P., Reproductive cycle, larval development, juvenile growth &d populatioh dynamics in Patiriella pseudoexigua (Echinodermata: Asteroidea) in Taiwan. Mar. Biol., 113 (1992) 271-280.

Del Pino, E.M., Modifications of oogenesis and develop- ment in marsupial frogs. Development, 107 (1989) 169-1 87.

Emlet R.B. and Hoegh-Guldberg, O., The effects of egg size on post-larval performance: experimental evidence from a sea urchin. Evolution, 51 (1997) 141-152.

Emlet R.B., McEdward L.R. and Strathmann, R.R., Echinoderm larval ecology viewed from the egg. In: Echinoderm Studies, Vol. 2, M. Jangoux and J.M. Lawrence (eds.), Balkema, Rotterdam, 1987, pp. 55-1 36.

Hart, M.W., Byrne M. and Smith, M.J., Molecular phylogenetic analysis of life-history evolution in asterinid starfish. Evolution, 5 1 (1997) 1848-1861.

Hoegh-Guldberg, 0. and Emlet, R.B., Energy use during the development of a lecithotrophic and a planktotrophic echinoid. Biol. Bull., 192 (1997) 2740 .

Jaeckle, W.B., Variation in the size, energy content, and biochemical composition of invertebrate eggs: correlates to the mode of larval development. In: Ecology of Marine Invertebrate Larvae, L. McEdward (ed.), CRC Press, New York, 1995, pp. 49-77.

Kanatani, H., Induction of spawning and oocyte maturation by 1-methyladenine in starfishes. Exp. Cell Res., 57 (1969) 333-337.

Laemmli, U.K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227 (1970) 680-685.

Lawrence, J.M., McClintock, J.B. and Guille, A., Organic level and caloric content of eggs of brooding asteroids and an echinoid (Echinodermata) from Kerguelen (South

Dow

nloa

ded

by [

Uni

vers

ity o

f W

ater

loo]

at 0

8:07

20

Nov

embe

r 20

14

202 M.Byrne et al. / IRD 36 (1999) 195-202

Indian Ocean). Invert. Reprod. Develop., 7 (1984) 249- 257.

Li, Q., Osada, M., Suzuki, T., Sato, M. and Mori, K., Degradation of vitellin during embryonic and larval development in the Pacific oyster Crassostrea gigas. Invert. Reprod. Develop., 33 (1998) 1-9.

McHugh, D. and Rouse, G.W., Life history evolution of marine invertebrates: new views from phylogenetic systematics. TREE, 13 (1998) 182-1 86.

Mortensen, T., Studies on the development and larval forms of echinoderms. GED GAD, Copenhagen, 1921.

Reimer, C.L. and Crawford, B.J., Identification and partial characterisation of yolk and cortical granule proteins in eggs and embryos of the starfish, Pisaster ochraceus. Dev. Biol., 167 (1995) 439-457.

Shyu, A.-B., Raff, R.A. and Blumenthal, T., Expression of the vitellogenin gene in female and male sea urchins. Proc. Natl. Acad. Sci. USA, 83 (1986) 3865-3869.

Scott, L.B., Leahy, P.S., Decker, G.L. and Lennarz, W.J., Loss of yolk platelets and yolk glycoproteins during larval development of the sea urchin embryo. Dev. Biol., 137 (1990) 368-377.

Strathmann, R.R., Hypotheses on the origins of marine larvae. Ann. Rev. Ecol. Syst., 24 (1993) 89-1 17.

Wahli, W., Evolution and expression of vitellogenin genes. Trends in Genetics, 4 (1988) 227-232.

Wray, G.A., Parallel evolution of nonfeeding larvae in echinoids. Syst. Biol., 45 (1996) 308-322.

Dow

nloa

ded

by [

Uni

vers

ity o

f W

ater

loo]

at 0

8:07

20

Nov

embe

r 20

14