Evolution of maternal lipid provisioning strategies in echinoids with non-feeding larvae: selection for high-quality juveniles

In marine invertebrates where larval planktotrophy is the ancestral life history, the evolutionary switch to lecithotrophy depended on modifications of oogenesis to produce energy-rich eggs that support development to the juvenile stage. In echinoderms, this involved a change from small eggs dominated by readily metabolised triacylglycerol (TAG) to large eggs containing various types of energetic storage lipids. We characterised lipid provisioning in the large (400 mu m diameter) eggs of the echinometrid sea urchin Heliocidaris erythrogramma which has lecithotrophic larvae to compare with the small (90 mu m diameter) eggs of the planktotroph H. tuberculata. We also investigated egg lipids in temnopleurids with contrasting modes of development: Temnopleurus alexandri and Holopneustes purpurascens (egg diameter: 125 and 600 mu m, respectively). In the planktotrophs, TAG was the major energetic lipid. Egg energetic lipids in the lecithotrophs were largely diacylglycerol ether (DAGE) with TAG and wax ester also present. We used rapid juvenile development in H. erythrogramma to characterise lipid depletion through metamorphosis to the 14 d old juvenile. Larval development did not significantly deplete energetic lipids, with 70% of the DAGE remaining for the juvenile. TAG supported larval development with a 20-30% decrease by Day 3 with no further depletion to Day 14. DAGE levels decreased around metamorphosis, followed by a gradual depletion, but 49% of these reserves remained on Day 14. Thus, DAGE provisioning provides a significant nutritive buffer for a considerable time post settlement. Selection to produce a high-quality juvenile has driven egg evolution in echinoids with lecithotrophic development.