Revelation of the Genetic Basis for Convergent Innovative Anal Fin Pigmentation Patterns in Cichlid Fishes

Abstract

Determining whether convergent novelties share a common genetic basis is vital to understanding the extent to which evolution is predictable. The convergent evolution of innovative anal fin pigmentation patterns in cichlid fishes is an ideal model for studying this question. Here, we focused on two patterns: 1) egg-spots, circular pigmentation patterns with different numbers, sizes and positions; and 2) the blotch, irregular pattern with no variation among species. How these two novelties originate and evolve remains unclear. Based on a thorough comparative transcriptomic and genomic analysis, we observed a common genetic basis with high evolutionary rates and similar expression levels between egg-spots and the blotch. But the associations of common genes with transcription factors and signalling pathways in the core gene network, as well as the integration of advantageous genes were observed specifically for egg-spots. Focusing on the whole transcriptomic level instead of limited numbers of candidate genes can explain the opposite conclusion between our study and the one from Santos et al. (2016), which suggested that no common genetic basis is shared between the blotch and egg-spots. Here, we propose that the re-use of the common genetic basis indicates important conservative functions (e.g., toolkit genes) for the origin of these convergent novel phenotypes, whereas independently evolved associations of common genes with transcription factors and signalling pathways (intrinsic factor) can free the evolution of egg-spots, and together with the integration of advantageous genes (extrinsic factor) can provide a clue to link egg-spots as a key innovation to the adaptive radiation in cichlid fishes. This hypothesis will further illuminate the mechanism of the origin and evolution of novelties in a broad sense.