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Species discovery, evolution and kleptoplasty in marine meiofaunal flatworms Stephenson, India

Abstract

Rhabdocoel flatworms are abundant members of marine meiofaunal communities worldwide, contributing to a reservoir of biodiversity that thrives between grains of sand. However, they are relatively understudied due to bias in meiofaunal sampling techniques and a lack of taxonomic expertise. Here, five species of neodalyellid rhabdocoels were discovered from intertidal habitats in British Columbia and characterised with molecular and morphological data: Baicalellia solaris n. sp., Baicalellia daftpunka n. sp., Tamanawas kalipis n. sp., Pogaina paranygulgus and Baicalellia pusillus. A molecular phylogenetic analysis using maximum likelihood and Bayesian inference on concatenated 18S and 28S rDNA sequences provided a framework for revising neodalyellid systematics and for inferring character evolution within the group. Kleptoplasty, the phenomenon by which one organism steals plastids from another, was discovered in the “solar panel worms” B. solaris and P. paranygulgus, representing just the second case in metazoans; kleptoplasty has only been described previously in sacoglossan sea slugs. Using a combination of light and electron microscopy, I demonstrated that plastids were intracellularly sequestered in the parenchymal tissue. DNA barcoding of partial rbcL sequences demonstrated that the plastids were stolen from raphid pennate diatoms, which was consistent with plastid ultrastucture. Measurements of oxygen consumption demonstrated that kleptoplasts remain functional for at least ten days after sequestration in B. solaris cells. Photosynthetic activity was of a similar magnitude to a dense chlorophyte culture, indicating that photosynthetically-fixed carbon enhanced survival in light-treated compared with dark-treated flatworms. Kleptoplasts ultimately lose function and are digested; therefore, heterotrophy is required to replenish healthy populations of kleptoplasts within the host tissue. The kleptoplasts might serve as a food store, providing sustenance when seasonal diatom blooms collapse. It cannot be determined whether kleptoplasty arose once in the common ancestor of Pogaina and Baicalellia or has evolved twice convergently.

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