The spandrels of Satan's perches: evidence for the co-optation of feeding traits in the convergent evolution of mouthbrooding in Neotropical cichlids

Abstract

The co-opting of existing traits for new functions (exaptation) offers an overall pattern in a noisy system: of the many paths evolution can take, exaptation suggests paths of least resistance, where the traits themselves precede their novel functions. Mouthbrooding, or oral brooding of offspring, may be one such function, having evolved independently 10-14 times within cichlids alone. Mechanically, mouthbrooding involves exaptation: a feeding and breathing structure is used in reproduction. While any fish with a mouth could mouthbrood, certain morphological traits—including some feeding adaptations—might increase mouthbrooding fitness. We hypothesized that mouthbrooding is more likely to evolve in lineages that have feeding adaptations that benefit mouthbrooding. We examined buccal morphologies in Neotropical cichlids, where mouthbrooding has evolved 5 times, 4 within winnowing (substrate sifting) clades. We found that mouthbrooders and winnowers overlapped substantially in their buccal morphologies. Accounting for phylogenetic and constructional constraints, species that exhibit one or both of these behaviors had larger buccal cavities, curved parasphenoids, and steeply angled vomers, while species that exhibit neither behavior had narrow buccal cavities and flat parasphenoids. These traits may be developmental consequences of the ventral orientation of the mouth for winnowing. We discuss the functional implications of these morphologies for both feeding and mouthbrooding. Our findings support our hypothesis that feeding can select for traits that can be exapted for mouthbrooding, but fully testing this hypothesis will require testing how these buccal morphologies impact both functions.