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

Abstract

BackgroundA 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.ResultsWe 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.ConclusionsThe 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.

Vertebral column regionalisation in Chinook salmon, Oncorhynchus tshawytscha

“…Ward & Brainerd () hypothesised that the actinopterygian vertebral column contains two axial modules. Several studies on development and evolution of body shape and elongation of fish have collected evidence in favour of a separate evolution of the anterior and posterior axial modules (Ward & Brainerd, ; Ward & Mehta, , ; Maxwell & Wilson, ; Schilling & Long, ). For example, most actinopterygian fish evolve elongated bodies mainly by adding vertebral centra rather than by increasing the length of individual vertebrae.…”

Intraspecific variation in fossil vertebrate populations: Fossil killifishes (Actinopterygii: Cyprinodontiformes) from the Oligocene of Central Europe

“…Divergence in patterns of trait covariance have previously been reported over a range of time and spatial scales (population: Game and Caley, 2006;stratigraphic: Maxwell and Dececchi, 2013;phylogenetic: Goswami et al, 2014), and variability in the amount of morphological variation present has been shown in a general way between populations (Game and Caley, 2006). Our results suggest that not only can the variancecovariance matrix be restructured, and different amounts of absolute variation be present (Wilson, 2013), but the variability of specific traits also changes over evolutionary time. The ~10% absolute variation in vertebral numbers among individuals we found may have influenced locomotory performance in the populations studied (Brainerd and Patek, 1998;Spouge and Larkin, 1979), although the relationship between vertebral numbers and locomotory performance is complex.…”

“…The pre-ural caudal region of the vertebral column in fishes is hypothesized to be more variable than the precaudal region, as segmentation proceeds from anterior to posterior (Itazawa, 1963;Nagiec, 1977;Lindsey, 1988;Grande and Bemis, 1998;Barton and Wilson, 1999;Aguirre et al, 2014), and most actinopterygians add vertebrae to the caudal region preferentially (Ward and Mehta, 2014), suggesting increased variability in this region. However, this is not a universal rule: some actinopterygians do add vertebrae preferentially to the abdominal region Maxwell and Wilson, 2013), and this may result in increased variability in abdominal counts within species. Sexual dimorphism may also increase observed variation in abdominal vertebral counts preferentially relative to caudal counts due to selection for increased abdominal volume in females (Lindsey, 1975).…”

“…The traits we examine are relatively easy to obtain and are commonly reported in the literature. These include vertebral count (Winkler et al, 2012;Maxwell and Wilson, 2013;Aguirre et al, 2014) and median fin length (Webb, 1984), which pertain directly to fish body shape and thus ecomorphology.…”

Can spatial sorting associated with spawning migration explain evolution of body size and vertebral number inAnguillaeels?

“…Because VN affects locomotion and agility, it may also influence foraging performance (Arnold, ; Swain, ; a; Lindell et al., ; Tibblin, Berggren, Nordahl, Larsson, & Forsman, ). Previous studies based on among‐species comparisons indicate that the evolution of a larger and more elongated body shape has been accompanied by evolution of increasing VN in both snakes (Lindell, ) and fish (Lindsey, ; Maxwell & Wilson, ). Our aim was not to specifically test for such pleomerism.…”