Expression ofHoxa‐11andHoxa‐13in the pectoral fin of a basal ray‐finned fish,Polyodon spathula: implications for the origin of tetrapod limbs

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Abstract
SummaryPaleontological and anatomical evidence suggests that the autopodium (hand or foot) is a novel feature that distinguishes limbs from fins, while the upper and lower limb (stylopod and zeugopod) are homologous to parts of the sarcopterygian paired fins. In tetrapod limb developmentHoxa‐11plays a key role in differentiating the lower limb andHoxa‐13plays a key role in differentiating the autopodium. It is thus important to determine the ancestral functions of these genes in order to understand the developmental genetic changes that led to the origin of the tetrapod autopodium. In particular it is important to understand which features of gene expression are derived in tetrapods and which are ancestral in bony fishes. To address these questions we cloned and sequenced theHoxa‐11andHoxa‐13genes from the North American paddlefish,Polyodon spathula, a basal ray‐finned fish that has a pectoral fin morphology resembling that of primitive bony fishes ancestral to the tetrapod lineage. Sequence analysis of these genes shows that they are not orthologous to the duplicated zebrafish and fugu genes. This implies that the paddlefish has not duplicated its HoxA cluster, unlike zebrafish and fugu. The expression ofHoxa‐11andHoxa‐13in the pectoral fins shows two main phases: an early phase in whichHoxa‐11is expressed proximally andHoxa‐13is expressed distally, and a later phase in whichHoxa‐11andHoxa‐13broadly overlap in the distal mesenchyme of the fin bud but are absent in the proximal fin bud. Hence the distal polarity ofHoxa‐13expression seen in tetrapods is likely to be an ancestral feature of paired appendage development. The main difference in HoxA gene expression between fin and limb development is that in tetrapods (with the exception of newts)Hoxa‐11expression is suppressed byHoxa‐13in the distal limb bud mesenchyme. There is, however, a short period of limb bud development whereHoxa‐11andHoxa‐13overlap similarly to the late expression seen in zebrafish and paddlefish. We conclude that the early expression pattern in tetrapods is similar to that seen in late fin development and that the local exclusion byHoxa‐13ofHoxa‐11from the distal limb bud is a derived feature of limb developmental regulation.