Regionalization of the axial skeleton in the ‘ambush predator’ guild – are there developmental rules underlying body shape evolution in ray-finned fishes?

Abstract

Background A long, slender body plan characterized by an elongate antorbital region and posterior displacement of the unpaired fins has evolved multiple times within ray-finned fishes, and is associated with ambush predation. The axial skeleton of ray-finned fishes is divided into abdominal and caudal regions, considered to be evolutionary modules. In this study, we test whether the convergent evolution of the ambush predator body plan is associated with predictable, regional changes in the axial skeleton, specifically whether the abdominal region is preferentially lengthened relative to the caudal region through the addition of vertebrae. We test this hypothesis in seven clades showing convergent evolution of this body plan, examining abdominal and caudal vertebral counts in over 300 living and fossil species. In four of these clades, we also examined the relationship between the fineness ratio and vertebral regionalization using phylogenetic independent contrasts. Results We report that in five of the clades surveyed, Lepisosteidae, Esocidae, Belonidae, Sphyraenidae and Fistulariidae, vertebrae are added preferentially to the abdominal region. In Lepisosteidae, Esocidae, and Belonidae, increasing abdominal vertebral count was also significantly related to increasing fineness ratio, a measure of elongation. Two clades did not preferentially add abdominal vertebrae: Saurichthyidae and Aulostomidae. Both of these groups show the development of a novel caudal region anterior to the insertion of the anal fin, morphologically differentiated from more posterior caudal vertebrae. Conclusions The preferential addition of abdominal vertebrae in fishes with an elongate body shape is consistent with the existence of a conservative positioning module formed by the boundary between the abdominal and caudal vertebral regions and the anterior insertion of the anal fin. Dissociation of this module is possible, although less probable than changes in the independently evolving abdominal region. Dissociation of the axial skeleton-median fin module leads to increased regionalization within the caudal vertebral column, something that has evolved several times in bony fishes, and may be homologous with the sacral region of tetrapods. These results suggest that modularity of the axial skeleton may result in somewhat predictable evolutionary outcomes in bony fishes.