Adaptation to herbivory and detritivory drives the convergent evolution of large abdominal cavities in a diverse freshwater fish radiation (Otophysi: Characiformes)

Abstract

Convergent evolution is often interpreted as evidence of natural selection favoring an optimal phenotype during adaptation. Morphological convergence is frequently found among lineages that converge on diet, but most studies have focused on morphological traits that relate exclusively to food handling and processing. In vertebrates, there is a strong inverse relationship between intestine length and trophic level. However, little is known about whether adaptation to a low trophic level influences the evolution of abdominal cavities that can accommodate larger intestines. Here, I reconstruct the evolutionary history of trophic ecology and examine abdominal cavity shape across 157 species of the fish order Characiformes to determine whether adaptation to an herbivorous-detritivorous diet drives convergent evolution of large abdominal cavities. Herbivorous-detritivorous species evolved significantly larger abdominal cavities than other trophic groups and repeatedly converged on a similar abdominal cavity morphology. Other trophic groups evolved abdominal cavity morphologies either stochastically or by selective pressures from an untested ecological character. These findings demonstrate that the selective demands of a larger intestinal tract promote the repeated convergence of a large abdominal cavity within herbivorous-detritivorous characiform fishes, while allowing other lineages to evolve randomly or adapt in response to other selection pressures, contributing to the overall body shape diversity of the order.

Phylogeny, body morphology, and trophic level shape intestinal traits in coral reef fishes

“…We used body elongation to account for body shape as it is the major axis of body shape variation among reef fishes (Claverie & Wainwright, 2014 ). Moreover, body elongation is strongly related to abdominal cavity depth and the space available to accommodate the intestine and other organs (Burns, 2021 ).…”

“…Estimates are posterior medians (circles), 50% credible intervals (CIs; thick lines) and 95% CIs (thin lines) from Bayesian phylogenetic hierarchical linear models after controlling for the remaining fixed and random effects. Posterior densities are also displayed (shaded regions) for body shape, in addition to allometry, is important because larger fishes have long body plans (Friedman et al, 2019), which in turn have relatively small abdominal cavities (Burns, 2021) that may not accommodate large intestines. For instance, the two most distinctively elongated species in our dataset, Aulostomus chinensis and Fistularia commersonii, both of which are strict piscivores, had the lowest values across all intestinal traits.…”

True grit? Comparative anatomy and evolution of gizzards in fishes

“…Specifically, fishes with gizzards were generally characterized by near‐mean values along PC1 and positive values of PC2. This suggests that fishes with gizzards generally have longer hindguts and deeper bodies, as is characteristic of herbivorous or detritivorous fishes (Burns, 2021). Carpiodes cyprinus (Catostomidae) was representative of gut and body dimensions at the negative and positive extremes of PC1 and PC2, respectively, with a deep body and abdomen and a long hindgut.…”

Digestion and assimilation of benthic biofilm by the Sábalo, Prochilodus lineatus

“…have simple tube-like intestines without extensive development of mucosal folds (Bowen, 1983). Among the more than 2000 species in the order Characiformes of which P. lineatus is a member, those described as herbivores and detritivores have evolved larger abdominal cavities with longer intestines that hold larger volumes of food undergoing digestion and assimilation (Burns, 2021). Fish that were apparently at the end of a feeding period had empty stomachs but the posterior digestive tracts had a continuous series of segments containing food as the last material ingested in that feeding period was moving through the digestive tract.…”