BackgroundAmong metazoans, retention of functional diet-derived chloroplasts (kleptoplasty) is known only from the sea slug taxon Sacoglossa (Gastropoda: Opisthobranchia). Intracellular maintenance of plastids in the slug's digestive epithelium has long attracted interest given its implications for understanding the evolution of endosymbiosis. However, photosynthetic ability varies widely among sacoglossans; some species have no plastid retention while others survive for months solely on photosynthesis. We present a molecular phylogenetic hypothesis for the Sacoglossa and a survey of kleptoplasty from representatives of all major clades. We sought to quantify variation in photosynthetic ability among lineages, identify phylogenetic origins of plastid retention, and assess whether kleptoplasty was a key character in the radiation of the Sacoglossa.ResultsThree levels of photosynthetic activity were detected: (1) no functional retention; (2) short-term retention lasting about one week; and (3) long-term retention for over a month. Phylogenetic analysis of one nuclear and two mitochondrial loci revealed reciprocal monophyly of the shelled Oxynoacea and shell-less Plakobranchacea, the latter comprising a monophyletic Plakobranchoidea and paraphyletic Limapontioidea. Only species in the Plakobranchoidea expressed short- or long-term kleptoplasty, most belonging to a speciose clade of slugs bearing parapodia (lateral flaps covering the dorsum). Bayesian ancestral character state reconstructions indicated that functional short-term retention arose once in the last common ancestor of Plakobranchoidea, and independently evolved into long-term retention in four derived species.ConclusionWe propose a sequential progression from short- to long-term kleptoplasty, with different adaptations involved in each step. Short-term kleptoplasty likely arose as a deficiency in plastid digestion, yielding additional energy via the release of fixed carbon. Functional short-term retention was an apomorphy of the Plakobranchoidea, but the subsequent evolution of parapodia enabled slugs to protect kleptoplasts against high irradiance and further prolong plastid survival. We conclude that functional short-term retention was necessary but not sufficient for an adaptive radiation in the Plakobranchoidea, especially in the genus Elysia which comprises a third of all sacoglossan species. The adaptations necessary for long-term chloroplast survival arose independently in species feeding on different algal hosts, providing a valuable study system for examining the parallel evolution of this unique trophic strategy.

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A new sacoglossan species, belonging to the genus Ercolania Trinchese, 1872 is described.  E. kencolesi sp. nov. has a similar biology as E. endophytophaga Jensen, 1999. Both are living within syncytial algal tubes of members of the Siphonocladales, E. kencolesi sp. nov. in Boergesenia forbesii and E. endophytophaga in Struvea plumosa. Assignment to the genus Ercolania is possible on the base of the cerata, which are round in cross-section, the digitiform rhinophores, sabot-shaped teeth and the presence of a penial stylet. The new species can be easily distinguished from E. endophyto-phaga, by the teeth with a prominent cusp, as well as other Ercolania species, by its unique colouration and its peculiar association to the food alga Boergesenia. Feeding, copulation, egg masses and development are noted. Differences in development further strengthen the distinction of E. kencolesi to E. endophytophaga. Measurement of photosynthetic activity of incorporated chloroplasts during several days clearly shows that chloroplasts are digested.