Evolution of the Hox Gene Cluster

Abstract

The Hox genes are a family of developmental control genes containing a homeobox motif, and tend to be organised in distinctive clustered arrays in animals. Organisation within the cluster can relate to how the genes function. Whilst much has been discovered about the Hox gene cluster in traditional model systems of developmental biology, increasing amounts of data from a wider variety of species are illuminating more about the nature of the Hox cluster deep in animal ancestry, as well as revealing the evolutionary flexibility and derivations along present‐day lineages. The consensus view of the Hox cluster is that it patterns the anterior–posterior axis of bilaterally symmetrical (bilaterian) animals and exhibits the phenomenon of colinearity. There is, however, much evolutionary change within this system. This diversity in the Hox system is linked to the evolution of animal diversity and informs our understanding of the pre‐bilaterian origins of the Hox genes themselves.

Key Concepts:

  • Spatial colinearity is the phenomenon whereby the order of the expression domains of the Hox genes along the anterior–posterior axis of the embryo corresponds with the order of the genes along the chromosome.

  • Temporal colinearity is a further form of colinearity in which the Hox genes in some taxa are activated progressively, with the earliest time at which a gene is activated matching its position within the Hox cluster.

  • Anterior–posterior patterning by the Hox genes is distinct from the initial determination of the anterior–posterior axis and instead involves the specification of different developmental fates within the anterior–posterior axis of an embryo. This is one of the major roles of the Hox genes within the bilaterians, but the Hox genes do have further roles in development subsequent to this anterior–posterior patterning function.

  • A range of Hox gene organisation has evolved across different lineages, forming organised, disorganised, split and atomised Hox clusters, such that the Hox genes of some species are not actually organised into a Hox gene cluster.

Keywords: homeobox; bilaterian; cnidarian; Hox gene; Hox cluster

Figure 1.

The diversity of Hox gene organisation in the animal kingdom and potential ancestral states. The phylogenetic relationships amongst the named species is shown, along with some indication of the major animal clades named along the branches of the tree. Note, the phylogenetic position of the Acoela is still the matter of some debate (see main text). Hox gene symbols are coloured to represent the four main types of Hox gene that are commonly recognised: Anterior (orange), Group 3 (green), Central (blue) and Posterior (red). The grey genes that have expanded within the Bombyx mori cluster are of an unclassified type. Horizontal lines connecting Hox genes represent known linkage and clustering, with parallel diagonal bars indicating large intergenic distances between genes on the same chromosome (i.e. linkage but not clustering). Genes that are known not to be linked are shown as off‐set, however, the distribution of the Oikopleura dioica and Nematostella vectensis genes is not known to the chromosomal level as this information is taken from the whole genome sequence assemblies in which the scaffolds tend to be assembled to a sub‐chromosomal level (Seo et al., ; Ryan et al., ). The Schistosoma mansoni data is taken from (Pierce et al., ), which does not include every S. mansoni Hox gene (Gu et al., ) but still indicates a dispersed cluster. Potential ancestral states of the Hox cluster are shown in magenta boxes (1, 2 and 3) along the basal parts of the tree. (1) The cnidarian–bilaterian ancestor may have had at least two or three genes. Cnidarians are generally recognised as having Anterior and Posterior genes, but may also have Central or Group 3 genes according to some authors (see main text), denoted by the bracketed gene. (2) The urbilaterian likely had four or five Hox genes, with an Anterior, two Central and a Posterior gene as well as a possible Group 3 (bracketed) according to (Jiménez‐Guri et al., ). (3) The Protostome–Deuterostome ancestor had at least seven Hox genes (de Rosa et al., ). The numbers of genes in these hypothesised ancestral clusters are necessarily minimum numbers.

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Further Reading

Deutsch JS (ed.) (2010) Hox genes: studies from the 20th to the 21st century. In: Advances in Experimental Medicine and Biology, vol. 689. New York, NY: Springer Science and Austin, TX: Landes Bioscience.

Papageorgiou S (ed.) (2007) Hox gene expression. New York, NY: Springer Science and Austin, TX: Landes Bioscience.

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Ferrier, David EK(Aug 2012) Evolution of the Hox Gene Cluster. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023989]