Fuels for development: evolution of maternal provisioning in asterinid sea stars
For marine invertebrates, larval developmental mode is inseparably linked to the nutritional content of the egg. Within the asterinid family of sea stars there have been multiple, independent, evolutionary transitions to lecithotrophic development from the ancestral, planktotrophic state. To investigate the evolution of maternal investment and development within the Asterinidae, we quantified individual lipid classes and total protein for eggs and larval stages of closely related species representing three developmental modes (planktotrophy, planktonic lecithotrophy and benthic lecithotrophy). Within species, maternal provisioning differed between females indicating that egg quality varied with parentage. Maternal investment was related to egg size but, after correcting for egg volume, we identified two major oogenic modifications associated with the evolution of lecithotrophic development: (1) a reduction in protein deposition that probably reflects the reduced structural requirements of nonfeeding larvae, (2) an increase in deposition of a single class of energetic lipid, triglyceride (TG). The exception was Parvulastra exigua, which has benthic, lecithotrophic development and lays eggs with a lipid to protein ratio close to that of planktotrophs. This oogenic strategy may provide P. exigua larvae with a protein “weight-belt” that assists in maintaining a benthic existence. Asterinids with planktotrophic development used a significant portion of egg TG to build a feeding bipinnaria larva. For Meridiastra mortenseni, female-specific differences in egg TG were still evident at the bipinnaria stage indicating that egg quality has flow-on effects for larval fitness. In lecithotrophic asterinids, TG reserves were not depleted in development to the larval stage whereas protein stores may help fuel early larval development. Available data indicate that there may be two evolutionarily stable egg lipid profiles for free-spawning, temperate echinoderms.
KeywordsLipid Class Maternal Investment Lecithotrophic Larva Methyl Dodecanoate Lecithotrophic Development
Thanks to Inke Falkner for specimen and sample collection, Silver Bishop for help with lipid analyses, and Dr Kirsten Benkendorff for laboratory space. The Bosch Institute (University of Sydney) provided facilities for protein analyses. This manuscript benefited from the comments of three anonymous reviewers. This research was funded by a grant to MB from the Australian Research Council and complied with current laws regarding experimental science conducted in Australia and New Zealand.
- Bosch I, Colwell SJ, Pearse JS, Pearse VB (1991) Nutritional flexibility in yolk-rich planktotrophic larvae of an Antarctic echinoderm. Antarct J US 26:168–170Google Scholar
- Byrne M, Selvakumaraswamy P, Cisternas P, Villinski JC, Raff RA (2003) Evolution of maternal provisioning in ophiuroids, asteroids and echinoids. In: Feral JP, David B (eds) Echinoderm research 2001. AA Balkema, Lisse, pp 171–175Google Scholar
- Cellario C, George SB (1990) Second generation of Paracentrotus lividus reared in the laboratory: egg quality tested. In: de Ridder C, Dubois P, Lahaye MC, Jangoux M (eds) Echinoderm research. AA Balkema, Rotterdam, pp 65–69Google Scholar
- Emlet RB, McEdward LR, Strathmann MF (1987) Echinoderm larval ecology viewed from the egg. In: Jangoux M, Lawrence JM (eds) Echinoderm studies. AA Balkema, Rotterdam, pp 55–136Google Scholar
- George SB (1996) Echinoderm egg and larval quality as a function of adult nutritional state. Oceanol Acta 19:297–308Google Scholar
- Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Coral reefs. Elsevier, Amsterdam, pp 133–207Google Scholar
- Jaeckle WB (1995) Variation in the size, energy content, and biochemical composition of invertebrate eggs: correlates to the mode of larval development. In: McEdward LR (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 49–77Google Scholar
- Podolsky RD, Virtue P, Hamilton T, Vavra J, Manahan DT (1994) Energy metabolism during development of the antarctic sea urchin Sterechinus neumayeri. Antarct J US 29:157–158Google Scholar
- Watts SA, Boettger SA, McClintock JB, Lawrence JM (1998) Gonad production in the sea urchin Lytechinus variegatus (Lamarck) fed prepared diets. J Shellfish Res 17:1591–1595Google Scholar
- Wray GA (1995) Evolution of larvae and developmental modes. In: McEdward LR (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 413–448Google Scholar
- Yokota Y, Kato KH, Mita M (1993) Morphological and biochemical studies on yolk degradation in the sea urchin, Hemicentrotus pulcherrimus. Zool Sci 10:661–670Google Scholar