Annelid Distal-less/Dlx duplications reveal varied post-duplication fates

Abstract

BackgroundDlx (Distal-less) genes have various developmental roles and are widespread throughout the animal kingdom, usually occurring as single copy genes in non-chordates and as multiple copies in most chordate genomes. While the genomic arrangement and function of these genes is well known in vertebrates and arthropods, information about Dlx genes in other organisms is scarce. We investigate the presence of Dlx genes in several annelid species and examine Dlx gene expression in the polychaete Pomatoceros lamarckii.ResultsTwo Dlx genes are present in P. lamarckii, Capitella teleta and Helobdella robusta. The C. teleta Dlx genes are closely linked in an inverted tail-to-tail orientation, reminiscent of the arrangement of vertebrate Dlx pairs, and gene conversion appears to have had a role in their evolution. The H. robusta Dlx genes, however, are not on the same genomic scaffold and display divergent sequences, while, if the P. lamarckii genes are linked in a tail-to-tail orientation they are a minimum of 41 kilobases apart and show no sign of gene conversion. No expression in P. lamarckii appendage development has been observed, which conflicts with the supposed conserved role of these genes in animal appendage development. These Dlx duplications do not appear to be annelid-wide, as the polychaete Platynereis dumerilii likely possesses only one Dlx gene.ConclusionsOn the basis of the currently accepted annelid phylogeny, we hypothesise that one Dlx duplication occurred in the annelid lineage after the divergence of P. dumerilii from the other lineages and these duplicates then had varied evolutionary fates in different species. We also propose that the ancestral role of Dlx genes is not related to appendage development.

Possible co-option ofengrailedduring brachiopod and mollusc shell development

“…However, en and dlx have diverse functions in animals, suggesting that shell formation is probably not the ancestral role of these genes. For example, in annelids, en and dlx may have roles in segmentation and neurogenesis, respectively, rather than shell formation [11,12] (electronic supplementary material, table S3). In arthropods, en and dlx are required for segmentation and limb formation [11,13].…”

Heterogeneous Conservation of Dlx Paralog Co-Expression in Jawed Vertebrates

“…Within the gnathostome sister group (cyclostomes), Dlx genes from the lamprey and hagfish have been identified but could not be strictly designated as members of the gnathostome Dlx1 to Dlx6 orthology groups ( Petromyzon marinus 4 genes [1]; Lampetra japonica , 6 genes [33], Eptatretus burgeri , 6 genes [34]). Outside the vertebrates, three Dlx genes have been identified in the urochordate Ciona , two organized as a bigene tandem cluster [35], while a single gene is found in amphioxus ( AmphiDll [36]) and most protostomes ( Drosophila melanogaster [37], but see [38] for exceptions). The current hypothesis is therefore that there was an ancestral tandem duplication after the divergence of the cephalochordates and before the common ancestor of the urochordates and vertebrates (Figure 1), making this gene family a chordate gene family which expanded from two ancestral genes in vertebrates.…”

Evolutionary crossroads in developmental biology: annelids

“…Development 139 (15) PRIMER Development 139 (15) et al, 2004), gut (Arendt et al, 2001;Boyle and Seaver, 2008;Saudemont et al, 2008;Hui et al, 2009;Boyle and Seaver, 2010), appendages (Panganiban et al, 1997;Winchell et al, 2010;McDougall et al, 2011), mesoderm (Kerner et al, 2006;Dill et al, 2007;Saudemont et al, 2008;Kerner et al, 2009) and more. The prominent role of annelids in evolutionary developmental biology is now clear, and this is likely to be extended in the future.…”