Morphological and temporal variation in early embryogenesis contributes to species divergence in Malawi cichlid fishes

Abstract

The cichlid fishes comprise the largest extant vertebrate family and are the quintessential example of rapid "explosive" adaptive radiations and phenotypic diversification. Despite low genetic divergence, East African cichlids harbour a spectacular intra- and interspecific morphological diversity, including the hyper-variable, neural crest (NC)-derived traits such as colouration and craniofacial skeleton. Although the genetic and developmental basis of these phenotypes has been investigated, understanding of when, and specifically how early, in ontogeny species-specific differences emerge, remains limited. Since adult traits often originate during embryonic development, the processes of embryogenesis could serve as a potential source of species-specific variation. Consequently, we compared the features of embryogenesis between three Malawi cichlid species - Astatotilapia calliptera, Tropheops sp. 'mauve' and Rhamphochromis sp. 'chilingali' - representing a wide spectrum of variation in pigmentation and craniofacial morphologies. Our results showed fundamental differences in multiple aspects of embryogenesis that could underlie interspecific divergence in adult adaptive traits. Firstly, we identified variation in the somite number and signatures of temporal variation, or heterochrony, in the rates of somite formation. The heterochrony was also evident within and between species throughout ontogeny, up to the juvenile stages. Finally, the identified interspecific differences in the development of pigmentation and craniofacial cartilages, present at the earliest stages of their overt formation, provide compelling evidence that the species-specific trajectories begin divergence during early embryogenesis, potentially during somitogenesis and NC development. Altogether, our results expand our understanding of fundamental cichlid biology and provide new insights into the developmental origins of vertebrate morphological diversity.

East African cichlid fishes

“…1 A). Furthermore, there are concise developmental descriptions for a few of other species [ 12 – 15 ] and more targeted ontogenetic descriptions focused on early embryogenesis [ 16 ], coloration [ 17 – 19 ], fin development [ 20 ], skeleton development [ 21 , 22 ], and gene expression [ 23 ]. Development of cichlids is similar to other teleost species, although early development in cichlids is two to three times slower in comparison with zebrafish, as shown for the African non-haplochromine cichlid Oreochromis niloticus and the Neotropical Midas cichlid Amphilophus citrinellus [ 24 ].…”