Leech anticoagulants are ancestral and likely to be multifunctional

Abstract

Abstract Bloodfeeding leeches have powerful anticoagulants that allow them to feed for extended periods. However, many leech species are predatory rather than bloodfeeding. It is not known whether they express these proteins and whether the proteins are co-opted for other purposes. Little is known about salivary secretions of the sister groups of leeches, where blood is not part of the diet. We screened the transcriptomes of four non-bloodfeeding leeches and four leech relatives to identify major lineages of anticoagulant genes, helping to determine their evolutionary origin and maintenance. We estimated selection regimes that are expected after a change in feeding behaviour. We found widespread presence of putative anticoagulants, although our results also indicate that several of these are members of multicopy gene families. Our analyses suggest that homologues to leech anticoagulants were already present before the origin of bloodfeeding in leeches and that negative selection is the major driver of evolutionary rates even in non-bloodfeeding taxa. These results point to the retention of the original function by these molecules in non-bloodfeeding species. Ultimately, the proteins might not be involved in bloodfeeding or it seems likely that their putative pleiotropic effects are of great importance.