Hox cluster duplications and the opportunity for evolutionary novelties

Abstract

Hox genes play a key role in animal body plan development. These genes tend to occur in tightly linked clusters in the genome. Vertebrates and invertebrates differ in their Hox cluster number, with vertebrates having multiple clusters and invertebrates usually having only one. Recent evidence shows that vertebrate Hox clusters are structurally more constrained than invertebrate Hox clusters; they exclude transposable elements, do not undergo tandem duplications, and conserve their intergenic distances and gene order. These constraints are only relaxed after a cluster duplication. In contrast, invertebrate Hox clusters are structurally more plastic; tandem duplications are common, the linkage of Hox genes can change quickly, or they can lose their structural integrity completely. We propose that the constraints on vertebrate Hox cluster structure lead to an association between the retention of duplicated Hox clusters and adaptive radiations. After a duplication the constraints on Hox cluster structure are temporarily lifted, which opens a window of evolvability for the Hox clusters. If this window of evolvability coincides with an adaptive radiation, chances are that a modified Hox cluster becomes recruited in an evolutionary novelty and then both copies of duplicated Hox clusters are retained.

The duplication of the Hox gene clusters in teleost fishes*1

“…A duplicated pro-opiomelanocortin gene in paddlefish and sturgeon seems to have arisen by a chondrostean-specific duplication [11], and hence is unrelated to the teleostean genome duplication. Unpublished data mentioned in [72] also suggest a duplication before the most recent common ancestor of euteleosts and after the most recent common ancestor of the sturgeons and teleosts. These lines of still circumstantial evidence place the duplication event either immediately before or immediately after the divergence of osteoglossomorphs (for which molecular data are unfortunately very scarce) and the modern teleosts.…”

Evolution after gene duplication: models, mechanisms, sequences, systems, and organisms

“…Although none of the results listed above, if considered alone, provide full support for a connection of WGD coupled with following radiation, when combined with a variety of evidence, support for this connection can be observed throughout the evolutionary history of life on earth (Holland et al, '94;Ruddle et al, '94;Sidow, '96;Stellwag, '99;Depew et al, 2002;Aburomia et al, 2003;Wagner et al, 2003).…”

Organization of Hox genes in ascidians: Present, past, and future

“…These four clusters have arisen likely by segmental duplication from a single ancestral cluster at the origin of the vertebrates (Bailey et al, 1997;Wagner et al, 2003). Further duplications have occurred in teleosts, which possess seven or even more Hox gene clusters with various member gene numbers (Malaga-Trillo and Meyer, 2001; Amores et al, 2004).…”