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ARS Home » Northeast Area » Beltsville, Maryland (BARC) » Beltsville Agricultural Research Center » Animal Parasitic Diseases Laboratory » Research » Publications at this Location » Publication #299420

Title: A monogenean without clamps

Author
item JUSTINE, JL - Muséum National D’Histoire Naturelle
item RAHMOUNI, C - Muséum National D’Histoire Naturelle
item GEY, D - Muséum National D’Histoire Naturelle
item Hoberg, Eric

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/25/2013
Publication Date: 11/22/2013
Citation: Justine, J., Rahmouni, C., Gey, D., Hoberg, E.P. 2013. A monogenean without clamps. PLoS One. 8(11):e79155 DOI:10.1371/journal.pone.0079155.

Interpretive Summary: Ectoparasites face a daily challenge: to remain attached to their host. Polyopisthocotylean monogeneans (ectoparasitic flatworms of fishes) attach to the surface of fish gills by highly specialized structures, the sclerotized clamps. Understanding the evolution of these complex structures is provide insights to processes involved in development of host associations and in general adaptations to parasitism. In some parasites in this large and diverse group (the Protomicrocotylidae), the clamps are replaced by other specialized attachment organs such as flaps and striations which are unknown in other members of the monogenean flat worms. We hypothesized that the clamps in protomicrocotylids were progressively lost during evolution, coinciding with the development of these other attachment structures. Testing this hypothesis, we examined the relative size of clamps with relation to the body, and discovered that the ration of clamp:body surface was lowest among the protomicrocotylids. Observations thus supported the contention that clamps in protomicrocotylids are vestigial organs, and that occurrence of simple clamps within the same family are steps in regressive evolution, leading to the absence of these attributes in some species. The conclusions are important as a model for exploring evolutionary processes that lead to major modifications in organs systems in parasites. Insights are pertinent to parasitologists and developmental biologists in basis studies of parasites and parasitism.

Technical Abstract: Ectoparasites face a daily challenge: to remain attached to their host. Polyopisthocotylean monogeneans attach to the surface of fish gills by highly specialized structures, the sclerotized clamps. In the original description of the protomicrocotylid species Lethacotyle fijiensis, described 50 years ago, the clamp was considered to be absent but few specimens were available and this observation was later questioned. In addition, genera within the family Protomicrocotylidae have either clamps of the “gastrocotylid type” and of the more simple “microcotylid type”; this puzzled systematists because these clamp types are characteristic of distinct, major groups. Discovery of another, new, species of the genus Lethacotyle, prompted comparisons with other members of the family Protomicrocotylidae and has allowed us to explore the nature of the attachment organs in these mongeneans. Lethacotyle vera n. sp. is described from the gills of the carangid Caranx papuensis off New Caledonia. It is distinguished from Lethacotyle fijiensis, the only other species of the genus, by the length of the male copulatory spines. Sequences of 28S rDNA were used to build a tree, in which Lethacotyle vera grouped with other protomicrocotylids. The identity of the host fish was determined with COI barcodes. We observed that protomicrocotylids have specialized structures associated with their attachment organ, such as lateral flaps and transverse striations, which are not known in other monogeneans. We thus hypothesized that the clamps in protomicrocotylids were progressively lost during evolution, coinciding with the development of other attachment structures. To test the hypothesis, we calculated the surfaces of clamps and body in 120 species of gastrocotylinean monogeneans, based on published descriptions. The ratio of clamp surface: body surface was the lowest in protomicrocotylids. We conclude that clamps in protomicrocotylids are vestigial organs, and that occurrence of “gastrocotylid” and simpler “microcotylid” clamps within the same family are steps in regressive evolution, leading to the absence of these attributes in species of Lethacotyle.