Short circuit co-evolution by the perfect parasites : antifreeze glycoproteins in Antarctic fish leeches (Hirudinea, Piscicolidae) : a thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Zoology at Massey University

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Antifreeze glycoproteins (AFGPs) play an important role in biochemical adaptation to supercooled waters and hence in the survival of notothenioid fish in Antarctica. These fishes have a well developed parasitic epifauna, which in turn is also exposed to freezing conditions. In order to retain their association with Antarctic fishes as the environment progressively cooled during the Miocene, leeches as fish-associated ectoparasites had either (i) to evolve a short circuit mechanism to acquire the necessary life-saving chemical compounds from their host, (ii) to adapt their own genome to confer protection from freezing, or (iii) to develop a combined tactic unique to their parasitic life strategy according to requirements during ontogenesis. I have found that Antarctic leeches (Hirudinea, Piscicolidae), that feed on a variety of notothenioid fish species, contain antifreeze compounds at the cellular level. I present evidence that strongly indicates an absorption pathway of AFGPs in the parasitic organisms from the fish blood as source. The physiological processes of AFGPs uptake from the intestine and circulatory distribution by haemolymph would be analogous to those enabling the fish hosts to distribute these peptides by blood within their bodies, as fish absorb AFGPs through the gut after production in the pancreas. The analysis of protein chemical structures in leech material revealed characteristics typical of fish AFGPs. Further, there are high capacities for freezing point suppression in vivo, thus biological activity of antifreeze proteins in the leech parasites Cryobdella antarctica and Cryobdella levigata. A combination of this thermal hysteresis (TH) with a specific bi-pyramidal ice crystal growth has been observed, which is typical for fish AFGPs. This confirms the presence not only of functional antifreeze macromolecules but also of true AFGPs in these parasite species. Finally, to trace the potential origin of these proteins to leech genomic information, mRNA molecules were successfully detected in C. levigata, as the intermediate step necessary for any de novo AFGP biosynthesis. These results suggest the possibility of a vi horizontal gene transfer (HGT) event in this host-parasite system and if proven would mark a further record of such a gene transfer for antifreeze molecules in Antarctica but for the first time outside the surface sea ice zone. I conclude that Antarctic fish leeches have developed a novel means of an evolutionary shortcut by co-opting mechanisms for survival in supercooled waters from their hosts in the form of biochemical exploitation and possibly in addition by HGT. To the best of my knowledge, the use of functional AFGPs after digestive absorption would represent the first example in the animal kingdom of an instantly effective adaptive advantage provided by another species under natural conditions in a quasi short circuit co-evolution. I also present results from a first survey on the leech fauna in the Ross Sea across nine species of Antarctic fishes and report one new host record for C. antarctica and three new leech-host associations for C. levigata. Finally, one new species belonging to the Piscicolidae is described, Megapodibdella kirsteni, gen. et sp. nov., from the Antarctic eelpout Lycodichthys dearborni.
Antifreeze proteins, Leeches, Antarctica, Fish parasites