Atypical plant–herbivore association of algal food and a kleptoplastic sea slug (Elysia clarki) revealed by DNA barcoding and field surveys

Middlebrooks, Michael L.; Bell, Susan S.; Curtis, Nicholas E.; Pierce, Sidney K.

doi:10.1007/s00227-014-2431-9

Cited by 22 publications

(23 citation statements)

References 52 publications

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“…Our results indicate that, depending on collection locality, food sources may differ to some degree and can also differ between specimens of the same collection locality, as was previously reported for P. ocellatus, E. clarki, and E. viridis (Maeda et al 2012;Baumgartner et al 2014;Middlebrooks et al 2014). This can be based on seasonality of algae or differences in the abundance of certain algae (Marìn and Ros 1993).…”

Section: Food Sources Of Sacoglossasupporting

confidence: 45%

“…Furthermore, differences in food source identification between feeding experiments, laboratory cultures (Krug 2009), or observation and DNA barcoding occur (see also Christa et al 2014d) as in the case of E. subornata or E. zuleicae: results obtained by barcoding revealed several different putative food source; however, they were known only to feed on Caulerpa and on Udotea, respectively (Krug 2009;Händeler and Wägele 2007;Jensen 1996). This may implement that sacoglossan sea slugs are not always closely associated with their food sources, a fact that was shown, e.g., for E. clarki (Middlebrooks et al 2014), and that some species may feed occasionally on algae as well that do not comprise their usual food. Even if slugs feed upon algae under laboratory conditions, this may not happen in the natural environment, as was shown recently for E. timida (Schmitt et al 2014).…”

Section: Food Sources Of Sacoglossamentioning

confidence: 88%

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Phylogenetic evidence for multiple independent origins of functional kleptoplasty in Sacoglossa (Heterobranchia, Gastropoda)

et al. 2014

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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.

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Section: Food Sources Of Sacoglossasupporting

confidence: 45%

Section: Food Sources Of Sacoglossamentioning

confidence: 88%

Phylogenetic evidence for multiple independent origins of functional kleptoplasty in Sacoglossa (Heterobranchia, Gastropoda)

et al. 2014

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“…Uncertainty surrounds feeding ecology, but thought to be highly polyphageous for a sacoglossan. The most recent work using field and lab methods confirmed feeding on one or more species in the genera Bryopsis, Penicillus, Halimeda, Acetabularia Lamouroux, 1812, and Derbesia Solier, 1846 (Pierce et al, 2003;Curtis et al, 2004Curtis et al, , 2006Middlebrooks et al, 2014). Originally described as Elysia (Tridachia) crispata, now formally recognized as a member of the genus Elysia.…”

Section: Notesmentioning

confidence: 99%

Identification guide to the heterobranch sea slugs (Mollusca: Gastropoda) from Bocas del Toro, Panama

et al. 2016

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Background: The Bocas del Toro Archipelago is located off the Caribbean coast of Panama. Until now, only 19 species of heterobranch sea slugs have been formally reported from this area; this number constitutes a fraction of total diversity in the Caribbean region. Results: Based on newly conducted fieldwork, we increase the number of recorded heterobranch sea slug species in Bocas del Toro to 82. Descriptive information for each species is provided, including taxonomic and/or ecological notes for most taxa. The collecting effort is also described and compared with that of other field expeditions in the Caribbean and the tropical Eastern Pacific. Conclusions: This increase in known diversity strongly suggests that the distribution of species within the Caribbean is still poorly known and species ranges may need to be modified as more surveys are conducted.

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“…; Middlebrooks et al. ). There is no apparent relationship between the species of alga(e) eaten by a particular slug and the adaptations for using the plastids in the host cell.…”

Section: Different Slug Species Are Differently Adapted To Support Klmentioning

confidence: 98%

“…In these species, the chloroplasts merely photosynthesize until they burn out, using up whatever algal‐originated material was engulfed initially, so that chloroplasts must be replaced by continuous feeding by the slugs (reviewed in Middlebrooks et al. , ; Pierce & Curtis ; Curtis et al. ).…”

Section: Chloroplast Proteins Are Synthesized In the Host Cellsmentioning

confidence: 99%

Sacoglossan sea slugs make routine use of photosynthesis by a variety of species‐specific adaptations

Pierce

Curtis

Middlebrooks

2015

Invertebrate Biology

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The phenomenon of the uptake, intracellular sequestration, and subsequent usage of algal chloroplasts by the digestive cells of many species of sacoglossan sea slugs, currently called kleptoplasty, has been of considerable interest since its discovery in the 1960s. While a large body of literature reported that captured chloroplasts were photosynthetically active inside slug cells and that plastid longevity in some species might be the result of the horizontal transfer of functional algal nuclear genes into the slug genome, a few recent studies have called the older results into question. Here, we have reviewed the literature and showed that while kleptoplasty occurs in many slug species and almost all derive benefit from kleptoplast photosynthesis, the slug adaptations to maintain the chloroplasts differ from species to species. These adaptations range from behavioral to molecular, including gene transfer, in a variety of combinations.

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Atypical plant–herbivore association of algal food and a kleptoplastic sea slug (Elysia clarki) revealed by DNA barcoding and field surveys

Cited by 22 publications

References 52 publications

Phylogenetic evidence for multiple independent origins of functional kleptoplasty in Sacoglossa (Heterobranchia, Gastropoda)

Phylogenetic evidence for multiple independent origins of functional kleptoplasty in Sacoglossa (Heterobranchia, Gastropoda)

Identification guide to the heterobranch sea slugs (Mollusca: Gastropoda) from Bocas del Toro, Panama

Sacoglossan sea slugs make routine use of photosynthesis by a variety of species‐specific adaptations

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