Functional kleptoplasty in a limapontioidean genus: Phylogeny, food preferences and photosynthesis in Costasiella, with a focus on C. Ocellifera (Gastropoda: Sacoglossa)

Abstract

The evolution and origin of functional kleptoplasty (sequestration and retention of functional plastids) within the Sacoglossa is still controversial. While some authors have suggested that it is a synapomorphy of the parapodia-bearing Plakobranchoidea, others have suggested an earlier origin at the base of the more inclusive clade Plakobranchacea. The latter is supported by the presence of kleptoplasts in Costasiella ocellifera, a ceras-bearing member of Limapontioidea, in which they remain functional for several weeks and fix CO2. However, the phylogenetic relationships of Costasiella, especially with regard to the Plakobranchoidea, have not been satisfactorily demonstrated, and the photosynthetic ability and the importance of photosynthesis within the genus remain poorly studied. In this study we analyse the phylogenetic position, photosynthetic activity and importance of photosynthesis for survival during starvation of five Costasiella species, but focusing on C. ocellifera. We demonstrate that Costasiella is a basal member of the Limapontioidea, however a final conclusion on the origin of functional kleptoplasty within Sacoglossa is still not possible. Three Costasiella species maintain functional chloroplasts (of which C. ocellifera shows long-term retention, and both C. kuroshimae and C. sp. 1 short-term retention) and together form a monophyletic group, feeding mainly on Avrainvillea. The two nonphotosynthetic species, C. nonatoi and C. sp. 2, represent the sister clade and feed on algae other than Avrainvillea. Intriguingly, C. ocellifera survived under nonphotosynthetic conditions for a minimum of 38 d, demonstrating that photosynthates may not be essential in order to survive starvation. These findings support our previous suggestion that during starvation kleptoplasts primarily represent a sort of larder, whose function might benefit from ongoing photosynthesis.