Phylogenomic Analyses Show Repeated Evolution of Hypertrophied Lips Among Lake Malawi Cichlid Fishes

Abstract

Cichlid fishes have repeatedly evolved an astounding diversity of trophic morphologies. For example, hypertrophied lips have evolved multiple times in both African and Neotropical cichlids and could have even evolved convergently within single species assemblages such as African Lake Malawi cichlids. However, the extremely high diversification rate in Lake Malawi cichlids and extensive potential for hybridization has cast doubt on whether even genome-level phylogenetic reconstructions could delineate if these types of adaptations have evolved once or multiple times. To examine the evolution of this iconic trait using protein-coding and noncoding single nucleotide polymorphisms (SNPs), we analyzed the genomes of 86 Lake Malawi cichlid species, including 33 de novo resequenced genomes. Surprisingly, genome-wide protein-coding SNPs exhibited enough phylogenetic informativeness to reconstruct interspecific and intraspecific relationships of hypertrophied lip cichlids, although noncoding SNPs provided better support. However, thinning of noncoding SNPs indicated most discrepancies come from the relatively smaller number of protein-coding sites and not from fundamental differences in their phylogenetic informativeness. Both coding and noncoding reconstructions showed that several "sand-dwelling" hypertrophied lip species, sampled intraspecifically, form a clade interspersed with a few other nonhypertrophied lip lineages. We also recovered Abactochromis labrosus within the rock-dwelling "mbuna" lineage, starkly contrasting with the affinities of other hypertrophied lip taxa found in the largely sand-dwelling "nonmbuna" component of this radiation. Comparative analyses coupled with tests for introgression indicate there is no widespread introgression between the hypertrophied lip lineages and taken together suggest this trophic phenotype has likely evolved at least twice independently within-lake Malawi.