Decoupled jaws promote trophic diversity in cichlid fishes

Abstract

Functional decoupling of oral and pharyngeal jaws is widely considered to have expanded the ecological repertoire of cichlid fishes. But, the degree to which the evolution of these jaw systems is decoupled and whether decoupling has impacted trophic diversification remains unknown. Focusing on the large Neotropical radiation of cichlids, we ask whether oral and pharyngeal jaw evolution is correlated and how their evolutionary rates respond to feeding ecology. In support of decoupling, we find relaxed evolutionary integration between the two jaw systems, resulting in novel trait combinations that potentially facilitate feeding mode diversification. These outcomes are made possible by escaping the mechanical trade-off between force transmission and mobility, which characterizes a single jaw system that functions in isolation. In spite of the structural independence of the two jaw systems, results using a Bayesian, state-dependent, relaxed-clock model of multivariate Brownian motion indicate strongly aligned evolutionary responses to feeding ecology. So, although decoupling of prey capture and processing functions released constraints on jaw evolution and promoted trophic diversity in cichlids, the natural diversity of consumed prey has also induced a moderate degree of evolutionary integration between the jaw systems, reminiscent of the original mechanical trade-off between force and mobility. K E Y W O R D S :Adaptive radiation, integration, key innovation, macroevolution, MuSSCRat, RevBayes. 9 5 0

The evolutionary ecology of fatty‐acid variation: Implications for consumer adaptation and diversification

“…In Environment B, however, only an increase in fatty acid X but not fatty acid Y is favoured consumers often encounter new food resources and undergo shifts in their trophic niche, culminating in the evolution of associated behavioural, morphological and physiological traits (Des Roches et al, 2016;Herrel et al, 2008;Leaver & Reimchen, 2012;Renaud et al, 2018). For instance, changes in jaw morphology (Burress et al, 2020), gut length (Davis et al, 2013) or even microbiome community composition (Rennison et al, 2019) can evolve rapidly, allowing consumers to profit from novel resources and persist in habitats that were previously suboptimal. Individuals from rangeedge and range-core populations also frequently differ in patterns of gene expression and metabolism (Rollins et al, 2015;Van Petegem et al, 2016).…”

Are Feeding Modes Concealing Morphofunctional Diversity? The Case of the New World Parrotfishes

“…However, there can be many different morphological ways to deliver the same function (Wainwright et al, 2005). Nevertheless, this is not the typical scenario, and it can be counter-intuitive given the expected match between ecology and morphology, as it has been found in other morpho-ecological studies, where high feeding morphological disparity is directly related to high diet diversity (Collar et al, 2005;Carlson and Wainwright, 2010;Price et al, 2010;Burress et al, 2020).…”

The cichlid oral and pharyngeal jaws are evolutionarily and genetically coupled

“…1c-d ). Functionally decoupling the jaw systems releases ray-finned fishes from mechanical constraints typically imposed by force-velocity trade-offs in single jaw systems 13 ; a single jaw cannot be optimized for both power and speed simultaneously, but a two jaw complex could optimize each jaw independently for one of power or speed 14 . Within the ray-finned fishes, some clades of percomorph fishes (i.e., Cichlidae, Labridae, Pomacentridae, and Embiotocidae), have independently evolved further specializations to their pharyngeal jaws that increased feeding efficiency, specializations that are theorized to be key to their success 15 .…”

“…Documenting the degree of integration between oral and pharyngeal jaws across genetic, molecular, and developmental levels is crucial to formulating a more comprehensive understanding of what constraints have shaped cichlid evolutionary dynamics and permitted such explosive adaptive radiations. While there is some evidence to suggest the jaw systems are evolutionarily decoupled based on certain functional metrics 22 , 24 , other work has demonstrated a degree of evolutionary and genetic integration between the oral and pharyngeal jaws 14 , 25 – 27 . There is also a need in the field to assess integration at multiple taxonomic levels, as patterns at higher, macroevolutionary levels (i.e., between genera) may or may not be related to those at lower, microevolutionary levels (i.e., within species) or developmental levels (i.e., within individuals), owing to distinct genetic and evolutionary phenomena influencing the manifestation of patterns at each level.…”

“…There is evidence to suggest that cichlids can experience some variation in the degree of integration between their oral and pharyngeal jaws, and that integration itself may be dependent on feeding ecology 14 . Specifically, despite the perceived ability of cichlids to free themselves from mechanical constraints, cichlids that hunt elusive prey typically pair slender, mobile oral jaws with gracile pharyngeal jaws, while cichlids that feed on algae or other tough foods typically pair robust, compact oral jaws with strong pharyngeal jaws.…”