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

Abstract

Higher teleost fishes, including zebrafish and fugu, have duplicated their Hox genes relative to the gene inventory of other gnathostome lineages. The most widely accepted theory contends that the duplicate Hox clusters orginated synchronously during a single genome duplication event in the early history of ray-finned fishes. In this contribution we collect and re-evaluate all publicly available sequence information. In particular, we show that the short Hox gene fragments from published PCR surveys of the killifish Fundulus heteroclitus, the medaka Oryzias latipes and the goldfish Carassius auratus can used to determine with little ambiguity not only their paralog group but also their membership in a particular cluster. Together with a survey of the genomic sequence data from the pufferfish Tetraodon nigroviridis we show that at least percomorpha, and possibly all eutelosts, share a system of seven orthologous Hox gene clusters, while at least the HoxC and HoxD clusters in ostariophysian (zebrafish) lineage might have arisen independently. There is little doubt about the orthology of the two teleost duplicates of the HoxA and HoxB clusters. A careful analysis of both the coding sequence of Hox genes and of conserved noncoding sequences provides additional support for the "duplication early" hypothesis that the Hox clusters in teleosts are derived by subsequent gene loss from an eight-cluster situation, although the data remain ambiguous in particular for the HoxC clusters. Assuming the "duplication early" hypothesis we use the new evidence on the Hox gene complements to determine the phylogenetic positions of gene-loss events in the wake of the cluster duplication. Surprisingly, we find that the resolution of redundancy seems to be a slow process that ist still-ongoing. A few suggestion on which additional sequence data would be most informative for resolving the history of the teleostean Hox genes are discussed.

PCR survey of hox genes in the goldfish Carassius auratus auratus

“…The identities of the PCR fragments were also investigated by reconstructing phylogenetic trees using different methods following the procedure outlined by Prohaska and Stadler (2004). Neighbor-joining (Saitou and Nei,'87), parsimony, and maximum likelihood analysis for each PG was performed using the Phylip package (Felsenstein,'89), using other teleost Hox homeobox fragments for comparison (D. rerio, Tetraodon nigroviridis, Takifugu rubripes, Oryzias latipes, and Fundulus heteroclitus).…”

“…In this regard, questions such as the characterization of evolutionary patterns after the FSGD including Hox gene retention/deletion, and evolution at the nucleotide level is of particular interest (Holland et al, '94;Malaga-Trillo and Meyer, 2001;Wagner et al, 2003;Prohaska and Stadler, 2004;Hoegg and Meyer, 2005;Crow et al, 2006;Kurosawa et al, 2006). Available DNA sequences from teleosts have shown a variety of gene retention and deletion patterns.…”

Whole-genome duplication in teleost fishes and its evolutionary consequences

“…After identifying many supernumerous Hox genes to the already known ones from tetrapods (Njolstad et al, 1988;Misof and Wagner, 1996;Aparicio et al, 1997), the 5 systematic evaluations of Hox genes revealed seven Hox clusters in zebrafish (Amores et al, 1998;Prince et al, 1998) as opposed to the four found in tetrapods. Although duplicated Hox genes have also been identified in other teleosts, it was initially not clear whether the increase in the number of Hox clusters is universal for teleosts (Prohaska and Stadler, 2004). Recently, duplicated Hox gene clusters were found in the two most basal extant groups of teleost fishes, the Elopomorpha (including eels and tarpons) (Guo et al, 2009;Henkel et al, 2012).…”

The Evolutionary Emergence of Vertebrates From Among Their Spineless Relatives

“…Some have argued for a direct causal linkage such that genome duplication drives a geologically instantaneous burst of evolution (Sidow 1996;Wagner et al 2003), while others have argued for a more permissive role wherein genome duplication is a necessary prerequisite of organismal evolution, but the effect on organismal evolution unfolds gradually over a protracted period of time (Prohaska and Stadler 2004). The principal evidence marshaled in support of the evolutionary burst hypothesis is the observation that living vertebrates and gnathostomes are distinguished from living invertebrate chordates and jawless vertebrates, respectively, by very large inventories of anatomical and developmental characters-surely only genome duplication can explain the emergence of so many characters in concert?…”