Phylogenetic evidence for multiple independent origins of functional kleptoplasty in Sacoglossa (Heterobranchia, Gastrop
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ORIGINAL ARTICLE
Phylogenetic evidence for multiple independent origins of functional kleptoplasty in Sacoglossa (Heterobranchia, Gastropoda) Gregor Christa & Katharina Händeler & Patrick Kück & Manja Vleugels & Johanna Franken & Dario Karmeinski & Heike Wägele
Received: 27 February 2014 / Accepted: 29 October 2014 # Gesellschaft für Biologische Systematik 2014
Abstract Sacoglossa is a rather small taxon of marine slugs with about 300 described species, yet it is quite fascinating scientists for decades. This is mainly because of the ability of certain species to incorporate photosynthetically active plastids of their algae prey, a phenomenon known as functional kleptoplasty. With the stolen plastids, these slugs endure weeks (short-term retention) or months (long-term retention) of starvation, though contribution of the plastids to the survival and factors enhancing plastid longevity are unknown. Likewise, contrasting hypotheses on evolution of functional kleptoplasty exist and the phylogenetic relationship of Sacoglossa taxa is still under debate. We analyzed the phylogenetic relationship of 105 sacoglossan species to address the question of the origin of functional kleptoplasty. Based on our phylogenetic analysis and the ancestral character state reconstruction, we conclude that functional short-term retention most likely originated two times and long-term retention at least five times. Previous suggestions that functional longterm kleptoplasty is established with specific plastids are supported by our food analyses in Elysia clarki that finally harbors only plastids of certain algae species over a prolonged starvation period.
Electronic supplementary material The online version of this article (doi:10.1007/s13127-014-0189-z) contains supplementary material, which is available to authorized users. G. Christa : K. Händeler : P. Kück : M. Vleugels : J. Franken : D. Karmeinski : H. Wägele Zoological Research Museum Alexander Koenig, Center for Molecular Biodiversity (zmb), 53113 Bonn, Germany G. Christa (*) : K. Händeler Institute for Molecular Evolution, Heinrich-Heine-University, 40225 Düsseldorf, Germany e-mail: [email protected]
Keywords Chlorophyta . Barcoding . Kleptoplasty . Sacoglossa . Sea slugs
Introduction Sacoglossan sea slugs, a small but famous group of marine gastropods, feed upon siphonous green algae by piercing the cell wall, sucking out the cell content, and sequestering the plastids in cells of the digestive glands (Händeler et al. 2009; Jensen 1980). The plastids of the algal food are then maintained by the slug, for which the term functional kleptoplasty was established (Rumpho et al. 2006; Waugh and Clark 1986; Wägele and Martin 2013). How the slugs benefit from the kleptoplasts, e.g., via transfer of photosynthates from plastids into the cell lumen (Gallop 1974; Trench and Gooday 1973), is still unknown, and despite results of former studies (Giménez-Casalduero and Muniain 2008; Hinde and Smith 1975; Trench 1975), there is nowadays evidence that the slugs are not photoautotrophic (
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