Evolution of axial patterning in elongate fishes

Abstract

Within the ray-finned fishes, eel-like (extremely elongate) body forms have evolved multiple times from deeper-bodied forms. Previous studies have shown that elongation of the vertebral column may be associated with an increase in the number of vertebrae, an increase in the length of the vertebral centra, or a combination of both. Because the vertebral column of fishes has at least two anatomically distinct regions (i.e. abdominal and caudal), an increase in the number and relative length of the vertebrae could be region-specific or occur globally across the length of the vertebral column. In the present study, we recorded vertebral counts and measurements of vertebral aspect ratio (vertebral length/width) from museum specimens for 54 species representing seven groups of actinopterygian fishes. We also collected, from published literature, vertebral counts for 813 species from 14 orders of actinopterygian and elasmobranch fishes. We found that the number of vertebrae can increase independently in the abdominal and caudal regions of the vertebral column, but changes in aspect ratio occur similarly in both regions. These findings suggest that abdominal vertebral number, caudal vertebral number, and vertebral aspect ratio are controlled by separate developmental modules. Based on these findings, we suggest some candidate developmental mechanisms that may contribute to vertebral column patterning in fishes. Our study is an example of how comparative anatomical studies of adults can generate testable hypotheses of evolutionary changes in developmental mechanisms.

Tetrapod-like axial regionalization in an early ray-finned fish

“…Under this scenario of shared regional identity, a tetrapod distribution of Hox domains would be ancestral for gnathostomes and osteichthyans by the rules of parsimony [11]. In contrast, axial patterning in model teleosts (figure 2f ) would be derived: the axis of Danio has far fewer trunk vertebrae than Tarrasius and many other bony fishes (figure 2g) [1,18,25]. Indeed, experimental insertion of zebrafish Hoxd11 regulatory genes into mice reduces trunk vertebral counts by anteriorizing the sacrum [42].…”

Sex-specific responses to fecundity selection in the broad-nosed pipefish

“…Pleomerism, the positive correlation between maximum body length and vertebral number, has been found across different hierarchical levels in many fishes: within suborders, families, genera, and species (Lindsey 1975). Intraspecific variation in vertebral number is also correlated with sexual size dimorphism (SSD) in several fish species (Springer 1971;Lindsey 1975), and regionspecific body size changes have been shown to correspond to changes in regional vertebral counts across several lineages of actinopterygians (Ward and Brainerd 2007), supporting the tight link between vertebral and body size evolution in this group. As vertebral number is fixed early in ontogeny, the presence of pleomerism in a species illustrates how adult body size and proportions can be influenced by factors fixed during early development.…”

“…Modules-units of covarying morphological traits that are relatively independent of other such units (Klingenberg 2005)-are seen as important intrinsic factors influencing the direction and rate of evolution (Gould and Lewontin 1979;Gould 2002). Plethodontid salamanders (Wake 1966), snakes (Polly et al 2001) and teleost fishes (Asano 1977;Ward and Brainerd 2007) all show region-specific changes in vertebral numbers correlated with body elongation, indicating the existence of relatively independent modules along the vertebral column, corresponding to the pre-anal abdominal region, or trunk, and the post-anal caudal region, or tail.…”

Exceptional fossil preservation demonstrates a new mode of axial skeleton elongation in early ray-finned fishes

“…E longation of the body has evolved multiple times among vertebrates, as exemplified by snakes and numerous other groups of reptiles, as well as amphibians, mammals and fishes [1][2][3] . Changes in the axial skeleton drive that process in most cases, either through elongation or addition of vertebrae [1][2][3][4][5] ( Fig.…”

“…Changes in the axial skeleton drive that process in most cases, either through elongation or addition of vertebrae [1][2][3][4][5] ( Fig. 1).…”