Hox genes in brachiopods and priapulids and protostome evolution

Abstract

Understanding the early evolution of animal body plans requires knowledge both of metazoan phylogeny and of the genetic and developmental changes involved in the emergence of particular forms. Recent 18S ribosomal RNA phylogenies suggest a three-branched tree for the Bilateria comprising the deuterostomes and two great protostome clades, the lophotrochozoans and ecdysozoans. Here, we show that the complement of Hox genes in critical protostome phyla reflects these phylogenetic relationships and reveals the early evolution of developmental regulatory potential in bilaterians. We have identified Hox genes that are shared by subsets of protostome phyla. These include a diverged pair of posterior (Abdominal-B-like) genes in both a brachiopod and a polychaete annelid, which supports the lophotrochozoan assemblage, and a distinct posterior Hox gene shared by a priapulid, a nematode and the arthropods, which supports the ecdysozoan clade. The ancestors of each of these two major protostome lineages had a minimum of eight to ten Hox genes. The major period of Hox gene expansion and diversification thus occurred before the radiation of each of the three great bilaterian clades.

Annelids in evolutionary developmental biology and comparative genomics

“…Another way that gene sequences can be used for phylogenetic purposes is as presence/ absence characters, rather than building phylogenetic trees from sequence alignments. One of the clearest examples of this is found with the Hox genes in lophotrochozoans such as the annelids Nereis virens, Helobdella robusta and Hirudo medicinalis (de Rosa et al, 1999). Lophotrochozoans, such as these annelids, have Posterior Hox genes (Post1 and Post2) that are distinct from the Posterior Hox genes of deuterostomes and ecdysozoans, and which presumably arose via independent tandem duplications from those that generated the deuterostome and ecdysozoan Posterior Hox genes.…”

“…The presence of Post1 and Post2, as distinct from ecdysozoan AbdB or deuterostome Hox9-15 sequences, can be taken as a character that unites the lophotrochozoans. Similarly the lophotrochozoans are distinguished by diagnostic central Hox gene sequences as well, such as Lox2, Lox4 and Lox5 (de Rosa et al, 1999;Balavoine et al, 2002). The Hox cluster genes pattern the development of the anterior-posterior axis of bilaterian embryos (Lemons & McGinnis, 2006).…”

“…For example the retention of many developmental control genes after the whole genome duplications at the origin of the vertebrates is hypothesized to have contributed to the evolution of the complexity of vertebrates (Shimeld & Holland, 2000). Duplication of Hox genes is certainly not restricted to the vertebrate lineage (Schwager et al, 2007;Cartwright et al, 1993;de Rosa et al, 1999). Leeches are reported as having duplications of some Hox genes, although as yet there is no evidence for whole cluster duplications in these annelids.…”

“…al de Rosa et al, 1999). Although the precise membership of each of these three super-clades is still being refined their existence seems well supported and justifiable.…”

Lophotrochozoan relationships and parasites. A snap-shot

“…However, Lophotrochozoa is consistently recovered in molecular phylogenetic analyses using different markers: combined multigene/EST data (Philippe et al, 2005, Baurain et al, 2007, mitochondrial gene order and sequence data (Helfenbein & Boore 2004;Larget et al, 2004), ATPase a-subunit (Anderson et al, 2004), hox genes (de Rosa et al, 1999;Passamaneck & Halanych, 2004), intermediate filament sequence data (Erber et al, 1998), myosin II heavy chain (Ruiz-Trillo et al, 2002), 28S rRNA (Mallatt & Winchell, 2002;Passamaneck & Halanych, 2006), and 18S rRNA (e.g. Halanych et al, 1995).…”