A “chimera” theory on the origin of dicyemid mesozoans: evolution driven by frequent lateral gene transfer from host to parasite

The phylogenetic status of the enigmatic dicyemid mesozoans is still uncertain. Are they primitive multicellular organisms or degenerate triploblastic animals? Presently, the latter view is accepted. A phylogenetic analysis of 18S rDNA sequences placed dicyemids within the animal clade, and this was supported by the discovery of a Hox-type gene with a lophotrochozoan signature sequence. This molecular information suggests that dicyemid mesozoans evolved from an ancestral animal degenerately. Considering their extreme simplicity, which is probably due to parasitism, they might have come from an early embryo via a radical transformation, i.e. neoteny. Irrespective of this molecular information, dicyemid mesozoans retain many protistan-like or extremely primitive features, such as tubular mitochondrial cristae, endocytic ability from the outer surface, and the absence of collagenous tissue, while they do not share noticeable synapomorphy with animals. In addition, the 5S rRNA phylogeny suggests a somewhat closer kinship with protozoan ciliates than with animals. If we accept this clear contradiction, dicyemids should be regarded as a chimera of animals and protistans. Here, we discuss the traditional theory of extreme degeneration via parasitism, and then propose a new “chimera” theory in which dicyemid mesozoans are exposed to a continual flow of genetic information via eating host tissues from the outer surface by endocytosis. Consequently, many of their intrinsic genes have been replaced by host-derived genes through lateral gene transfer (LGT), implying that LGT is a key driving force in the evolution of dicyemid mesozoans.