Did homeobox gene duplications contribute to the Cambrian explosion?

Peter W H Holland

The Cambrian explosion describes an apparently rapid increase in the diversity of bilaterian animals around 540-515 million years ago. Bilaterian animals explore the world in three-dimensions deploying forward-facing sense organs, a brain, and an anterior mouth; they possess muscle blocks enabling efficient crawling and burrowing in sediments, and they typically have an efficient 'through-gut' with separate mouth and anus to process bulk food and eject waste, even when burrowing in sediment. A variety of ecological, environmental, genetic, and developmental factors have been proposed as possible triggers and correlates of the Cambrian explosion, and it is likely that a combination of factors were involved. Here, I focus on a set of developmental genetic changes and propose these are part of the mix of permissive factors. I describe how ANTP-class homeobox genes, which encode transcription factors involved in body patterning, increased in number in the bilaterian stem lineage and earlier. These gene duplications generated a large array of ANTP class genes, including three distinct gene clusters called NK, Hox, and ParaHox. Comparative data supports the idea that NK genes were deployed primarily to pattern the bilaterian mesoderm, Hox genes coded position along the central nervous system, and ParaHox genes most likely originally specified the mouth, midgut, and anus of the newly evolved through-gut. It is proposed that diversification of ANTP class genes played a role in the Cambrian explosion by contributing to the patterning systems used to build animal bodies capable of high-energy directed locomotion, including active burrowing.