Wnt evolution and function shuffling in liberal and conservative chordate genomes

Abstract

BackgroundWhat impact gene loss has on the evolution of developmental processes, and how function shuffling has affected retained genes driving essential biological processes, remain open questions in the fields of genome evolution and EvoDevo. To investigate these problems, we have analyzed the evolution of the Wnt ligand repertoire in the chordate phylum as a case study.ResultsWe conduct an exhaustive survey of Wnt genes in genomic databases, identifying 156 Wnt genes in 13 non-vertebrate chordates. This represents the most complete Wnt gene catalog of the chordate subphyla and has allowed us to resolve previous ambiguities about the orthology of many Wnt genes, including the identification of WntA for the first time in chordates. Moreover, we create the first complete expression atlas for the Wnt family during amphioxus development, providing a useful resource to investigate the evolution of Wnt expression throughout the radiation of chordates.ConclusionsOur data underscore extraordinary genomic stasis in cephalochordates, which contrasts with the liberal and dynamic evolutionary patterns of gene loss and duplication in urochordate genomes. Our analysis has allowed us to infer ancestral Wnt functions shared among all chordates, several cases of function shuffling among Wnt paralogs, as well as unique expression domains for Wnt genes that likely reflect functional innovations in each chordate lineage. Finally, we propose a potential relationship between the evolution of WntA and the evolution of the mouth in chordates.Electronic supplementary materialThe online version of this article (10.1186/s13059-018-1468-3) contains supplementary material, which is available to authorized users.

The dopamine receptor D5gene shows signs of independent erosion in Toothed and Baleen whales

“…The rise of large-scale genomic sequencing projects has emphasized the role of gene loss as a potent driver of evolutionary change: underlying phenotypic adaptations or neutral regressions in response to specific environmental cues and niches [23–28]. Interestingly, gene loss mechanisms seem pervasive in lineages that endured drastic environmental adaptations in the course of evolution, such as Cetacea, entailing niche-specific physiological and morphological adaptations [25,29–33].…”

Evolution of vertebrate spinal cord patterning

“…Lamprey; data only on noncanonical Wnt5 which is expressed across the DV spinal cord . Amphioxus; Wnt1 in the tailbud, Wnt3 in the tail fin and distributed along spinal cord . Notch in the ventricular zone in vertebrates and in the tailbud in amphioxus.…”

“…45 Amphioxus; Wnt1 in the tailbud, Wnt3 in the tail fin and distributed along spinal cord. 46 Notch in the ventricular zone in vertebrates and in the tailbud in amphioxus. References: Gnathostomes; Mouse, 47 ; Chick, 48 ; Zebrafish, ventricular zone notch and delta 49,50 ; Lamprey 11,45 ; Amphioxus.…”

“…Hox14 is also responsive to RA even though it is only expressed in the posterior notochord, gut, and cerebral vesicle at larval stage. 133,134 Several Wnt genes show tailbud expression, 46,135 though only limited manipulation of Wnt signaling has been conducted in amphioxus to date 136 and we do not know whether Wnt regulates Hox. FGF inhibition alone does not seem to have an effect on Hox1 expression but when coupled with an RA antagonist there is no Hox1 expression in the neural plate.…”

A wnt2 ortholog in the sea urchin Paracentrotus lividus

“…WNT ligands constitute a highly conserved family of secreted glycoproteins, which can be subdivided into 13 distinct subfamilies. Importantly, the overall number of wnt genes per subfamily varies significantly between different metazoan phyla and even sometimes between different species of a given phylum (Janssen et al, ; Kusserow et al, ; Somorjai et al, ). This suggests thus that the wnt gene complements of extant animals resulted from complex superimpositions of gene duplication and gene loss events that took place during evolution.…”