Extensive non-redundancy in a recently duplicated developmental gene family

Background: It has been proposed that recently duplicated genes are more likely to be redundant with one another compared to ancient paralogues. The evolutionary logic underpinning this idea is simple, as the assumption is that recently derived paralogous genes are more similar in sequence compared to members of ancient gene families. We set out to test this idea by using molecular phylogenetics and exploiting the genetic tractability of the model nematode, Caenorhabditis elegans, in studying the nematode-specific family of Hedgehog-related genes, the Warthogs. Hedgehog is one of a handful of signal transduction pathways that underpins the development of bilaterian animals. While having lost a bona fide Hedgehog gene, most nematodes have evolved an expanded repertoire of Hedgehog-related genes, ten of which reside within the Warthog family.

Results: We have characterised their evolutionary origin and their roles in C. elegans and found that these genes have adopted new functions in aspects of post-embryonic development, including left-right asymmetry and cell fate determination, akin to the functions of their vertebrate counterparts. Analysis of various double and triple mutants of the Warthog family reveals that more recently derived paralogues are not redundant with one another, while a pair of divergent Warthogs do display redundancy with respect to their function in cuticle biosynthesis.

Conclusions: We have shown that newer members of taxon-restricted gene families are not always functionally redundant despite their recent inception, whereas much older paralogues can be, which is considered paradoxical according to the current framework in gene evolution.