Inference of the ancestral vertebrate phenotype through vestiges of the whole-genome duplications

Abstract

Inferring the phenotype of the last common ancestor of living vertebrates is a challenging problem because of several unresolvable factors. They include the lack of reliable out-groups of living vertebrates, poor information about less fossilizable organs and specialized traits of phylogenetically important species, such as lampreys and hagfishes (e.g. secondary loss of vertebrae in adult hagfishes). These factors undermine the reliability of ancestral reconstruction by traditional character mapping approaches based on maximum parsimony. In this article, we formulate an approach to hypothesizing ancestral vertebrate phenotypes using information from the phylogenetic and functional properties of genes duplicated by genome expansions in early vertebrate evolution. We named the conjecture as 'chronological reconstruction of ohnolog functions (CHROF)'. This CHROF conjecture raises the possibility that the last common ancestor of living vertebrates may have had more complex traits than currently thought.

Figure 1.

Mapping hypothetical phenotypes to vertebrate phylogeny (A–D) schematic representations of a hypothetical vertebrate ancestor before the acquisition of paired fins (A), and ones just before and after the WGDs (B and C), and extant jawed vertebrates (D). Black circle, a whole-genome duplication. Note that the first pair of fins appeared with Tbx4/5 expression (dark purple) before the WGDs. After the WGDs, the paired fins temporally expressed both Tbx4 and Tbx5 (red and blue stripes).

Figure 2.

The basic concept of the CHROF conjecture. (A and B) Subfunctionalization of enhancers after WGDs. Rectangles, arbitrary gene Xs. Small dark and gray boxes, enhancers that are redundant, but have slightly different activities. (A) Redundant enhancers that existed before WGDs are lost in a complementary style, resulting in ohnologs flanked by nonhomologous enhancers with similar activities. (B) An enhancer is duplicated by WGDs, and retained with slightly different functions. (C) Inference of the ancestral state by gene expression. The arrows indicate logical flows. Here, ohnologs, Tbx2 and Tbx3 [39] are shown as an example. The right-most figures show the expression patterns of Tbx2 and Tbx3 in living tetrapod limb buds. Tbx2 (red) and Tbx3 (blue) are expressed in the lateral parts of limb buds, but each expression covers a slightly different region. The middle figure shows hypothetical expression patterns just after the WGDs. The spatial expression patterns are exactly same. The left figure shows a hypothetical ancestral state just before the WGDs. The ancestor had a limb/fin bud with the expression of a single gene, Tbx2/3 (dark purple).