Biting disrupts integration to spur skull evolution in eels

Abstract

The demand that anatomical structures work together to perform biological functions is thought to impose strong limits on morphological evolution. Breakthroughs in diversification can occur, however, when functional integration among structures is relaxed. Although such transitions are expected to generate variation in morphological diversification across the tree of life, empirical tests of this hypothesis are rare. Here we show that transitions between suction-based and biting modes of prey capture, which require different degrees of coordination among skull components, are associated with shifts in the pattern of skull diversification in eels (Anguilliformes). Biting eels have experienced greater independence of the jaws, hyoid and operculum during evolution and exhibit more varied morphologies than closely related suction feeders, and this pattern reflects the weakened functional integration among skull components required for biting. Our results suggest that behavioural transitions can change the evolutionary potential of the vertebrate skeleton by altering functional relationships among structures.

Feeding kinematics and performance of basal otariid pinnipeds, Steller sea lions (Eumetopias jubatus), and northern fur seals (Callorhinus ursinus): implications for the evolution of mammalian feeding

“…However, the biting we observed in northern fur seals seemed stereotypical. In contrast, suction feeding, as observed in Steller sea lions, requires a series of morphological parts and behavioral events to be coordinated to function effectively (Collar et al, 2014). Such functional integration likely constrains skull evolution and suction feeding (Collar et al, 2014).…”

“…In contrast, suction feeding, as observed in Steller sea lions, requires a series of morphological parts and behavioral events to be coordinated to function effectively (Collar et al, 2014). Such functional integration likely constrains skull evolution and suction feeding (Collar et al, 2014). It has been suggested that the terrestrial arctoid ancestors of pinnipedimorphs ( pinnipeds and their extinct relatives) exhibited a biting feeding mode, and biting is considered the ancestral feeding mode among extant pinnipeds (Werth, 2000a;Adam and Berta, 2002;Berta et al, 2006).…”

Always chew your food: freshwater stingrays use mastication to process tough insect prey

“…In other fishes, decoupling of prey capture from prey processing is a function of having two sets of jaws, oral and pharyngeal, of which the latter performs the majority of processing [44]. In some fish lineages, decoupling of anatomical modules during feeding behaviour has led to radical changes in the morphology of formerly integrated cranial modules, correlated with increased diversification in these lineages [9]. Using the body as a method of prey restraint or to outright capture prey is prominent in other vertebrates outside fishes (e.g.…”

“…), prey capture and processing may be handled by two systems-prey capture is achieved with the disc (the morphological structure derived from encircling pectoral fins [8]), leaving the jaws and teeth for prey processing. In all these cases, different anatomical modules handle different functions, allowing for independent modular evolution [9] and increased evolutionary flexibility.…”

Replicated divergence in cichlid radiations mirrors a major vertebrate innovation

“…Other studies have examined divergence between biting and suction feeding fishes [17,40] but few have done so in a way that incorporates multiple recent transitions (but see [41]). A previous study of New World cichlids shows an association between enhanced jaw protrusion and foraging on evasive prey, though only some of the non-evasive prey specialists in that study were biting taxa [42].…”