Review: The Origin of Digenetic Trematodes: Did the Story Begin with the Blood Flukes?

Building on other scholars' relatively recent insights of the relationships of polyopisthocotyleans and trematodes, here for the first time it is hypothesized that this relationship favors the view that blood flukes are the primordial digeneans, and blood feeding per se was a factor facilitating the transition to endoparasitism. In contrast to other hypotheses of digenean origins that are "mollusc first" and then suggest acquisition of the vertebrate host secondarily, this is a "vertebrate first" hypothesis that features later capture of molluscan or annelid hosts. Capture of molluscan or annelid hosts may have been facilitated by their possession of hemoglobin. This hypothesis is also distinctive in suggesting that the 2-host blood fluke life cycle is not secondarily truncated but in fact represents the basal condition and, furthermore, provides a platform from which 3-host life cycles could emerge. The hypothesis is supported by long-standing observations that early diverging blood flukes tend to appear in early diverging vertebrate host lineages, blood fluke intermediate hosts and intramolluscan larval stages are exceptionally diverse, and blood flukes exhibit cercariae with tails ranging from simple buds to complex forked swimming structures. These ideas have nonetheless heretofore never been gathered into an explicit statement hypothesizing the early divergence of blood flukes, manifested today in definitive hosts ranging from early diverging fish lineages to birds and mammals, a host breadth unparalleled among other digenean groups. This hypothesis supports the sister group relationships of aspidogastreans and digeneans, but unlike others it does not posit a major role for aspidogastrean-like organisms giving rise to primordial digeneans. It also points out problems in concluding that some digenean groups such as brachylaimids or transversotrematids are basal digeneans. This review also considers how the complex intramolluscan asexual reproduction program of digeneans may have arisen, based on new insights from functional genomics.