Rotiferan Hox genes give new insights into the evolution of metazoan bodyplans

Abstract

The phylum Rotifera consists of minuscule, nonsegmented animals with a unique body plan and an unresolved phylogenetic position. The presence of pharyngeal articulated jaws supports an inclusion in Gnathifera nested in the Spiralia. Comparison of Hox genes, involved in animal body plan patterning, can be used to infer phylogenetic relationships. Here, we report the expression of five Hox genes during embryogenesis of the rotifer Brachionus manjavacas and show how these genes define different functional components of the nervous system and not the usual bilaterian staggered expression along the anteroposterior axis. Sequence analysis revealed that the lox5-parapeptide, a key signature in lophotrochozoan and platyhelminthean Hox6/lox5 genes, is absent and replaced by different signatures in Rotifera and Chaetognatha, and that the MedPost gene, until now unique to Chaetognatha, is also present in rotifers. Collectively, our results support an inclusion of chaetognaths in gnathiferans and Gnathifera as sister group to the remaining spiralians.

Identification and characterization of homeobox (Hox) genes and conservation of the single Hox cluster (324.6 kb) in the water flea Daphnia magna

“…The lophotrochozoan Hox cluster is likely to have undergone a lineage-specific gene duplication and diversification event (Fröbius & Funch, 2017 Figure 3). For example, in D. melanogaster, three copies of Hox3 genes (Bcd, Zen, Zen2) are reported (Stauber, Jäckle, & Schmidt-Ott, 1999), while the insect Tribolium castaneum has two copies of Hox3 genes including Zen1 and Zen2 (van der Zee, Berns, & Roth, 2005).…”

“…The lophotrochozoan Hox cluster is likely to have undergone a lineage‐specific gene duplication and diversification event (Fröbius & Funch, ). In ecdysozoans, lineage‐specific gene duplication events and a change in transcriptional orientation in Hox genes have been identified (Figure ).…”

Hox gene expression during the development of the phoronidPhoronopsis harmeri

“…Consequently, both phoronid species lack an orthologue of lox2, the absence, which is apparently shared by Phoronida with other Lophophorata (16,89,90,95) as well as with some other Spiralia -i.e. Rotifera (34,97) and Platyhelminthes (42,98 ) and possibly kamptozoans(107) (however, in the latter the lox2-like sequence lacks most of the residues considered as lox2 signature, Additional File 1: Fig. S2).…”

“…nervous system) and their ectodermal expression is often considered as an ancestral feature(14,28,34), in various spiralian species certain Hox genes are also expressed in mesoderm, endoderm and clade-specific structures like chaetal sacs or shell fields (e.g (16,23,24,27,29,31,35,36,(39)(40)(41)46)…”

Morphology of the nervous system of monogonont rotiferEpiphanes sentawith focus on sexual dimorphism between feeding females and dwarfed males

“…(12-33)). Further, gene expression in the developing and juvenile nervous system of monogonont rotifers has recently been studied(34, 35). However, most of these studies focused on the nervous system of feeding females, whereas neuroanatomy of dwarfed males remains poorly examined.…”