Parallel molecular mechanisms underlie convergent evolution of the exaggerated snout phenotype in East African cichlids

Abstract

Studying instances of convergent evolution of novel phenotypes can shed light on the evolutionary constraints that shape morphological diversity. Cichlid fishes from the East African Great Lakes are a prime model to investigate convergent adaptations. However, most studies on cichlid craniofacial morphologies have primarily considered bony structures, while soft tissue adaptations have been less intensely scrutinised. A rare example of an exaggerated soft tissue phenotype is the formation of a snout flap. This tissue flap develops from the upper lip and has evolved in only one cichlid genus from Lake Malawi and one genus from Lake Tanganyika. To investigate the molecular basis of snout flap convergence, we used mRNA sequencing to compare two species with snout flap (Labeotropheus trewavasae and Ophthalmotilapia nasuta) to their close relatives without snout flaps (Tropheops tropheops and Ophthalmotilapia ventralis) from Lake Tanganyika and Malawi. Our analysis revealed a greater complexity of differential gene expression patterns underlying the snout flap in the younger adaptive radiation of Lake Malawi than in the older Lake Tanganyika radiation. We identified 201 genes that were repeatedly differentially expressed between species with and without the snout flap in both lakes, suggesting that the pathway that gives rise to snout flaps is evolutionarily constrained, even though the flaps play very different functions in each species. The convergently expressed genes are involved in proline and hydroxyproline metabolism, which have been linked to human skin and facial deformities. Additionally, we also found enrichment for transcription factor binding sites upstream of differentially expressed genes such as members of the FOX transcription factor family, especially foxf1 and foxa2, which also showed an increased expression in the flapped snout and are linked to nose morphogenesis in mammals, as well as ap4 (tfap4), a transcription factor showing reduced expression in the flapped snout with an unknown role in the development of craniofacial soft tissues. As genes involved in cichlids snout flap development are associated with many human mid-line facial dysmorphologies, our findings imply a conservation of genes involved in mid-line patterning across vastly distant evolutionary lineages of vertebrates.

A Kiss of Deep Homology: Partial Convergence in the Genomic Basis of Hypertrophied Lips in Cichlid Fish and Human Cleft Lip

“…4 ; Henning et al 2017 ; Colombo et al 2013 ; Lecaudey et al 2021 ). Recent transcriptomic studies in East African cichlids also point to there being many genes that underlie similar craniofacial adaptations ( Lecaudey et al 2021 ; Duenser et al 2022 ). Furthermore, a QTL analysis of hypertrophied lip species in Lake Victoria cichlids that are closely related to those found in Lake Malawi also recovered a highly polygenic basis for this trait ( supplementary table S6, Supplementary Material online; Henning et al 2017 ).…”