The genetic basis of the repeated evolution of an adaptive character: Hypertrophic lips of cichlid fishes
Ecology and Biodiversity of Animals and Ecosystems, Organismic Interactions
Final Report Abstract
Convergent evolution is a well-known phenomenon where unrelated species that live in similar environments evolved similar phenotypic characteristics. However, it is still unclear if phenotypic convergence is produced by the same or different mutations in the same or different genes. Cichlid fishes are famous for their diversity in morphology, coloration, and behaviour and are a well-known textbook model for the study of speciation and adaptive evolution. The occurrence of convergent evolution in several characteristics such as coloration and body shape has also been documented in cichlids inhabiting independent lakes (e.g. African great lakes). Hypertrophied lips are an ecologically important trait related to feeding behaviour in rocky substrates and have evolved repeatedly in parallel in cichlids both in Africa and Central America. This exciting case of repeated evolution is very likely due to similar selective pressures associated with foraging behaviour. Since in this case of convergent evolution hypertrophic lips in cichlids evolved repeatedly, not only among relatively closely species from Africa, but also in New World cichlids, we were able to compare the genetic mechanisms at several levels of evolutionary relationships. To investigate these issues, we carried out comparative genetic maps using Next Generation Sequencing (NGS) approaches in order to identify the regions in the genomes that were associated with hypertrophied lips. After the regions had been identified, and whenever was possible, we tested whether the same gene(s) in different populations and species are causing these similar phenotypic traits. In this project, we addressed one of the most important questions in evolutionary biology in the age of genomics: (1) are adaptations the result of mutations at many loci each with small effects or a few loci of large effect? (2) What is the source of adaptive genetic variation (standing genetic variation or new mutations)? (3) Are similar adaptations to similar environmental pressures - i.e. repeated evolution - caused by the same mutations in the same genes or caused by different mutations even in different genes? This project made important contributions to a better understanding of the convergent of hypertrophied lips in cichlids, as we could show that: 1) Hypertrophied lips has a clear genetic component but have a plastic component in certain species. 2) The repeated evolution of hypertrophied-lip morphology in conjunction with a narrow and pointed head shape in cichlids represents an evolutionary innovation that facilitates foraging in rocky crevices, thus allowing access to a novel niche. 3) The thick- and thin-lipped morphs differ in their eco-morphology, which might promote, under certain circumstances, ecological and evolutionary divergence in Midas cichlids. 4) The loci underlying hypertrophied lip variation in African cichlids (Lake Victoria) are numerous and have small additive effects; and the distribution of additive effects suggests that natural selection had a genomewide effect. 5) Hypertrophied lips have a simple genetic basis in Midas cichlids, where one small genomic region in Chromosome 8 explains more than 70% of the variance in lip morphology. 6) Genome scans suggest that the core haplotype is shared across thick-lipped fish in all four Nicaraguan crater lakes, suggesting a shared genetic basis. This project generated a high amount of molecular data of an unprecentated level of resolution, including a high-order assembly of the Midas cichlid genome, highresolution genetic map and cross data and a large number of population resequencing data. These are extremely useful resources to foster further investigations on this exciting biological system.
Publications
- 2014. Species-specific differences in adaptive phenotypic plasticity in an ecologically relevant trophic trait: hypertrophic lips in Midas cichlid fishes. Evolution 68, 2086-2091
G. Machado-Schiaffino, F. Henning & A. Meyer
(See online at https://doi.org/10.1111/evo.12367) - 2015. What big lips are good for: on the adaptive function of repeatedly evolved hypertrophied lips of cichlid fishes. Biological Journal of the Linnean Society 115, 448-455
L. Baumgarten, G. Machado-Schiaffino, F. Henning & A. Meyer
(See online at https://doi.org/10.1111/bij.12502) - 2016. Multispecies Outcomes of Sympatric Speciation after Admixture with the Source Population in Two Radiations of Nicaraguan Crater Lake Cichlids. PLOS Genetics, 12(6): e1006157
A.F. Kautt, G. Machado-Schiaffino & A. Meyer
(See online at https://doi.org/10.1371/journal.pgen.1006157) - 2017. Genetic dissection of adaptive form and function in rapidly-speciating cichlid fishes. Evolution, 71(5), 1297-1312
F. Henning, G. Machado-Schiaffino, L. Baumgarten & A. Meyer
(See online at https://doi.org/10.1111/evo.13206) - 2017. Incipient Speciation Driven by Hypertrophied Lips in Midas Cichlids Fish? Molecular Ecology, 26, 2348-2362
G. Machado-Schiaffino, A.F. Kautt, J. Torres-Dowdall, L. Baumgarten, F. Henning & A. Meyer
(See online at https://doi.org/10.1111/mec.14029) - 2018. Agouti-related peptide 2 drives convergent evolution of stripe patterns across cichlid fish radiations. Science 362, 457-460
C.F. Kratochwil, Y. Liang, J. Gerwin, J.M. Woltering, S. Urban, F. Henning, G. Machado-Schiaffino, C.D. Hulsey & A. Meyer
(See online at https://doi.org/10.1126/science.aao6809) - Contrasting signatures of genomic divergence during sympatric speciation. Nature
A.F. Kautt, C.F. Kratochwil, A. Nater, G. Machado-Schiaffino, M. Olave, F. Henning, J. Torres-Dowdall, A. Härer, C.D. Hulsey, P. Franchini, M. Pippel, E.W. Myers & A. Meyer
(See online at https://doi.org/10.1038/s41586-020-2845-0)
