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      Functional chloroplasts in metazoan cells - a unique evolutionary strategy in animal life

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          Abstract

          Background

          Among 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.

          Results

          Three 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.

          Conclusion

          We 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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          Most cited references60

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          Plant-Animal Mutualistic Networks: The Architecture of Biodiversity

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            The Maximum Likelihood Approach to Reconstructing Ancestral Character States of Discrete Characters on Phylogenies

            Mark Page (1999)
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              Insects on plants: macroevolutionary chemical trends in host use.

              Determining the macroevolutionary importance of plant chemistry on herbivore host shifts is critical to understanding the evolution of insect-plant interactions. Molecular phylogenies of the ancient and speciose Blepharida (Coleoptera)-Bursera (Burseraceae) system were reconstructed and terpenoid chemical profiles for the plant species obtained. Statistical analyses show that the historical patterns of host shifts strongly correspond to the patterns of host chemical similarity, indicating that plant chemistry has played a significant role in the evolution of host shifts by phytophagous insects.
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                Author and article information

                Journal
                Front Zool
                Frontiers in Zoology
                BioMed Central
                1742-9994
                2009
                1 December 2009
                : 6
                : 28
                Affiliations
                [1 ]Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany
                [2 ]Department of Biological Sciences, California State University, Los Angeles, California, 90032-8201, USA
                Article
                1742-9994-6-28
                10.1186/1742-9994-6-28
                2790442
                19951407
                45aada0e-b9a4-416b-87b3-7aa04c35947c
                Copyright ©2009 Händeler et al; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 26 June 2009
                : 1 December 2009
                Categories
                Research

                Animal science & Zoology
                Animal science & Zoology

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