Ontogenetic development of intestinal length and relationships to diet in an Australasian fish family (Terapontidae)

Abstract

BackgroundOne of the most widely accepted ecomorphological relationships in vertebrates is the negative correlation between intestinal length and proportion of animal prey in diet. While many fish groups exhibit this general pattern, other clades demonstrate minimal, and in some cases contrasting, associations between diet and intestinal length. Moreover, this relationship and its evolutionary derivation have received little attention from a phylogenetic perspective. This study documents the phylogenetic development of intestinal length variability, and resultant correlation with dietary habits, within a molecular phylogeny of 28 species of terapontid fishes. The Terapontidae (grunters), an ancestrally euryhaline-marine group, is the most trophically diverse of Australia’s freshwater fish families, with widespread shifts away from animal-prey-dominated diets occurring since their invasion of fresh waters.ResultsDescription of ontogenetic development of intestinal complexity of terapontid fishes, in combination with ancestral character state reconstruction, demonstrated that complex intestinal looping (convolution) has evolved independently on multiple occasions within the family. This modification of ontogenetic development drives much of the associated interspecific variability in intestinal length evident in terapontids. Phylogenetically informed comparative analyses (phylogenetic independent contrasts) showed that the interspecific differences in intestinal length resulting from these ontogenetic developmental mechanisms explained ~65% of the variability in the proportion of animal material in terapontid diets.ConclusionsThe ontogenetic development of intestinal complexity appears to represent an important functional innovation underlying the extensive trophic differentiation seen in Australia’s freshwater terapontids, specifically facilitating the pronounced shifts away from carnivorous (including invertebrates and vertebrates) diets evident across the family. The capacity to modify intestinal morphology and physiology may also be an important facilitator of trophic diversification during other phyletic radiations.

Widespread ecomorphological convergence in multiple fish families spanning the marine–freshwater interface

“…Subtle niche variations in otherwise broad ecological roles probably also increase the area of phenotypic morphospace occupied within broadly similar trophic designations. Differences in specific dietary targets and foraging behaviours of several closely related, nominally 'herbivorous' clades included in this study (Kyphosidae-Girellidae and Scortum, Syncomistes, Pingalla) are associated with notable differences in aspects of tooth shape and length and intestinal morphology [15,21,32]. That multiple adaptive peaks occur in functional morphology of such admittedly broadly classified dietary categories is not surprising.…”

“…Here, multiple families have evolved across diverse temperate-tropical regions and macrohabitats, including several marine-to-freshwater transitions. Collective lineages exhibit comparable ecological roles (figure 1a) [15,21], with trophic groups including benthic invertivores, herbivores and carnivores that are frequently associated with distinctive morphotypes relating to body shape, intestinal length and oral anatomy [14,21,22]. If convergence has played a significant role in shaping the macroevolutionary history of the Terapontoidei, we predict ecologically similar species with respect to diet (otherwise phylogenetically distant and often geographically isolated) will converge into the same areas of morphological and dietary space.…”

Trophic relationships in fish assemblages of Neotropical floodplain lakes: selectivity and feeding overlap mediated by food availability

“…In addition to detritus, these species ingested algae and other non-insect aquatic invertebrates. The selection of detritus by these species was expected, independent of its availability in the lakes, mainly because of the foraging behavior, morphology of their digestive tracts, physiological traits as well as by phylogeny (Bowen, 1983;Fugi et al, 1996;Lujan et al, 2011;Davis et al, 2013;Correa & Winemiller, 2014), are factors that limit the use of other items.…”

Evidence for a multi-peak adaptive landscape in the evolution of trophic morphology in terapontid fishes

“…The terapontids are one of the most speciose and trophically diverse of Australia's freshwater fish families, exhibiting feeding habits that span carnivorous, insectivorous, omnivorous, herbivorous, frugivorous and detritivorous trophic strategies (Davis et al ., ). Recent comparative studies have demonstrated that a single freshwater invasion by marine terapontid ancestors prompted significantly higher rates of lineage, morphological and trophic diversification (particularly adoption of non‐animal prey dominated diets) in freshwater clades compared to marine counterparts, as well as significant dietary‐ecomorphological correlations across the family (Davis et al ., , , ). With a diversity of feeding modes across freshwater and marine species, terapontids also offer scope for assessing potential phenotypic convergence across the marine‐freshwater interface, the primary macrohabitat divergence for aquatic fauna.…”