Chemical defense and evolutionary trends in biosynthetic capacity among dorid nudibranchs (Mollusca: Gastropoda: Opisthobranchia)

Abstract

An evolutionary scenario incorporating recent advances in phylogenetic research begins with an opisthobranch-pulmonate common ancestor that was herbivorous and had some diet-derived chemical defense. The Nudibranchia and their closest relatives, the Notaspidea, form a lineage the ancestors of which had switched to feeding upon sponges and deriving protection from metabolites contained in them. Subsequently there have been repeated shifts in food and defensive metabolites, and trends are evident in the ability to detoxify, sequester and utilize metabolites from food, as well as to synthesize defensive compounds de no6o. The Notaspidea display a minor adaptive radiation that foreshadows a more extensive one in the various lineages of nudibranchs. This review emphasizes changes that have occurred within the Holohepatica, or dorid nudibranchs (order Doridacea). Their sister-group, the Cladohepatica, consists of three other orders, Dendronotacea, Arminacea, and Aeolidiacea, in which there has been a shift from sponges to Cnidaria as food. The Dendronotacea often feed upon Octocorallia, which combine spicules, chemical defense, and stinging capsules and thereby suggest a transition from feeding on sponges. A previous diet of Octocorallia is suggested by the defensive use of prostaglandins in the dendronotacean Tethys fimbria, which eats crustaceans. A shift to bryozoans in some Arminacea is accompanied by use of different metabolites. Dorid nudibranchs evidently began as sponge-feeders, but some lineages have shifted to a variety of other food organisms, and others have specialized in the kind of sponges they feed on and how they do it. There have been shifts to bryozoans (Ectoprocta) and ascidians (Chordata: Urochordata) that track metabolites rather than the taxonomy of the food. There is a crude correlation between the genealogy and the defensive metabolites of the sponge-feeding dorids.De no6o synthesis is well documented in this order and the metabolites are appropriately positioned so as to have an adaptive effect. The hypothesis that the capacity for de no6o synthesis was acquired by gene transfer across lineages is rejected, partly on the basis of different chirality of metabolites in the nudibranchs and their food organisms. Instead it is proposed that there has been a preadaptive phase followed by evolution in a retrosynthetic mode, with selection favoring enzymes that enhance the yield of end products that are already present in the food.

Endobacteria in the tentacles of selected cnidarian species and in the cerata of their nudibranch predators

“…Cimino and Ghiselin (1999) reported diet switch in species of nudibranch orders Dendronotaceae, Arminaceae, and Aeolidiaceae from sponges to cnidaria. Indeed, diet shifts may be regarded as a smart survival strategy of sea slugs.…”

“…Overviews of their phylogeny, diet, sophisticated defence strategies and the chemical structures of their feeding deterrents were provided by Faulkner and Ghiselin (1983), Mebs (1985), Cimino and Ghiselin (1999) and Wägele and Klussmann-Kolb (2004). McDonald and Nybakken (1996) compiled the available information on the diet of nudibranch species from all over the world.…”

Factors promoting marine invasions: A chemoecological approach

“…1-5 and references therein). Chemical defense is now understood as the driving force behind the evolution of the group, preceding the regression of the shell and the abandonment of mechanical defense (6)(7)(8)(9). Adaptive radiation, with switches from one chemically defended food source to another, has been documented by means of comparative techniques.…”

Endobacterial morphotypes in nudibranch cerata tips: a SEM analysis

“…The observed difference in endobacteria may be due to variations in diet, for example the spindle-like bacteria in Coryphella lineata and the two different oval forms in Berghia caerulescens and in Janolus cristatus. For the latter, nudibranch species (member of the family Zephyrinidae) Cimino and Ghiselin (1999) reported a possible diet switch from sponges to cnidaria. Further, major evidence supports the probability of bacterial transfer from cnidaria to nudibranchia: the uptake of the many unfired kleptocnides and their path through the complex nudibranch gut system to cnidosacks, their final destination in the tip region of cerata.…”