The cichlid oral and pharyngeal jaws are evolutionarily and genetically coupled

Andrew J Conith,R Craig Albertson

doi:10.1038/s41467-021-25755-5

Andrew J Conith, R Craig Albertson

Open Access

https://doi.org/10.1038/s41467-021-25755-5

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Abstract

Evolutionary constraints may significantly bias phenotypic change, while “breaking” from such constraints can lead to expanded ecological opportunity. Ray-finned fishes have broken functional constraints by developing two jaws (oral-pharyngeal), decoupling prey capture (oral jaw) from processing (pharyngeal jaw). It is hypothesized that the oral and pharyngeal jaws represent independent evolutionary modules and this facilitated diversification in feeding architectures. Here we test this hypothesis in African cichlids. Contrary to our expectation, we find integration between jaws at multiple evolutionary levels. Next, we document integration at the genetic level, and identify a candidate gene, smad7, within a pleiotropic locus for oral and pharyngeal jaw shape that exhibits correlated expression between the two tissues. Collectively, our data show that African cichlid evolutionary success has occurred within the context of a coupled jaw system, an attribute that may be driving adaptive evolution in this iconic group by facilitating rapid shifts between foraging habitats, providing an advantage in a stochastic environment such as the East African Rift-Valley.

Highlights

Evolutionary constraints may significantly bias phenotypic change, while “breaking” from such constraints can lead to expanded ecological opportunity
We examined phenotypic associations between the lower oral and pharyngeal jaws (LOJ and lower pharyngeal jaw (LPJ), respectively) of 88 cichlid species from across Africa, primarily sampling from lakes in the East African Rift Valley: lakes Malawi, Tanganyika, and Victoria (Supplementary Data 1)
We found the lower oral jaw (LOJ) and LPJ were evolutionarily correlated (r-partial least squares (PLS) = 0.482, P = 0.002, effect size (Z) = 2.585), but some taxa, those with unique diets and/or modes of feeding, appeared to deviate from the best-fit line, indicating lower levels of integration between jaws (Fig. 2a)

Summary

Introduction

Evolutionary constraints may significantly bias phenotypic change, while “breaking” from such constraints can lead to expanded ecological opportunity. It is hypothesized that the oral and pharyngeal jaws represent independent evolutionary modules and this facilitated diversification in feeding architectures. We test this hypothesis in African cichlids. Constraints, when broken, can lead to rapid evolutionary change in a clade and may be responsible for the unevenness in rates of taxonomic and morphological evolution observed across metazoans, providing an opportunity to explore incipient stages of diversification[7,8]. Selection for shared functions or genetic pleiotropy can produce strong integration among traits, biasing phenotypic evolution to occur along a narrow line delimited by the covariation among traits––the line of least resistance[11,12]. Cichlids are characterized by rapid speciation within a diverse array of ecological niches throughout the subtropics

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