The role of microRNAs in the diversification of Midas cichlids from Nicaragua
Bioinformatics and Theoretical Biology
Final Report Abstract
Since the ground-breaking work of Britten and Davidson (1969), gene regulation has increasingly been acknowledged as one of the major drivers of species differentiation. Yet, the hypothesis that changes in gene expression commonly underlie phenotypic divergence has only become testable with the development of approaches that permit quantitative estimates of gene expression. Now, gene regulation is widely considered one of the fastest and most effective mechanisms underlying adaptive evolution and is thought to be particularly relevant in the initial stages of speciation. Although nonsynonymous changes in widely expressed protein-coding sequences can produce major pleiotropic effects on the phenotype, gene regulatory mechanisms such as transcription factors, DNA methylation, and microRNAs (miRNAs) can produce a more fine-tuned outcome. By modifying the gene expression that facilitates adaptation and potentially reproductive isolation, gene regulation could lay the foundation for genetically based divergence even in the face of gene flow. An ideal model system to address these hypotheses is represented by cichlid fishes, a textbook example of explosive phenotypic diversification and sympatric speciation. The main goal of this project was to increase knowledge of the molecular basis that underlies the evolutionary success of cichlids. Specifically, the aim of the proposed research program was to explore the role of miRNA regulatory function (1) in the diversification of species, (2) in the molecular mechanism of adaptation and (3) in the parallel evolution of phenotypes in repeated adaptive radiations. This project made important contributions to a better understanding of the molecular mechanisms that have facilitated the rapid radiation of cichlid fishes, as we could show that: 1) The target sites of miRNAs showed a genomic signature of purifying selection by comparing with surrounding non-target regions of the 3’ UTRs, but relaxed purifying selection might fuel rapid species divergence. 2) Later in development more and larger gene coexpression modules were associated with the divergence between benthic (high-bodied) and limnetic (streamlined) fish compared with the earlier life stage. 3) 3’ UTRs in cichlids tend to be longer than those in non-cichlids, and this is associated, on average, with one more miRNA target per gene in cichlids. These cis-regulatory features might serve as important meta-regulators, regulators of other mechanisms governing post-transcriptional regulation. 4) Regulation by miRNAs might be an important and extremely fast-evolving mechanism that contributed to the rapid phenotypic evolution of cichlid fishes even in the presence of gene flow. A novel Midas cichlid miRNA might have a major role in shaping the cichlids' trophic apparatus. 5) High emergence rate of miRNAs (i.e. several novel miRNAs were gained in each cichlid lineage) might increase the gene regulatory possibilities of this fast-evolving group of fish, thus fueling their adaptation potential. 6) Variation of adaptive phenotypes (e.g. lip size and pharyngeal jaw morphology) has a polygenic basis and post-transcriptional regulation of novel genes might underlie such divergence. This project generated a high amount of molecular data of an unprecedented level of resolution. These extremely useful resources will foster further investigations on this exciting biological system.
Publications
- (2016) Genetic linkage of distinct adaptive traits in sympatrically speciating crater lake cichlid fish. Nature Communications 7, 12736
Fruciano C, Franchini P, Kovacova V, Elmer K, Henning F, Meyer A
(See online at https://doi.org/10.1038/ncomms12736) - (2016) The role of microRNAs in the repeated parallel diversification of lineages of Midas cichlid fish from Nicaragua. Genome biology and evolution 8, 1543-1555
Franchini P, Xiong P, Fruciano C, Meyer A
(See online at https://doi.org/10.1093/gbe/evw097) - (2018) Evolutionary divergence of 3’UTR in cichlid fishes. BMC Genomics 19, 433
Xiong P, Hulsey D, Meyer A, Franchini P
(See online at https://doi.org/10.1186/s12864-018-4821-8) - (2019) Divergent allometric trajectories in gene expression and coexpression produce species differences in sympatrically speciating Midas cichlid fish. Genome Biology and Evolution 11, 1644-1657
Fruciano C, Meyer A, Franchini P
(See online at https://doi.org/10.1093/gbe/evz108) - Conservation and novelty in the microRNA genomic landscape of hyperdiverse cichlid fishes. Scientific Reports. SREP-19-22445. 2019
Xiong P, Schneider RF, Hulsey CD, Meyer A, Franchini P
(See online at https://doi.org/10.1038/s41598-019-50124-0) - MicroRNA Gene Regulation in Extremely Young and Parallel Adaptive Radiations of Crater Lake Cichlid Fish. Molecular Biology and Evolution. Volume 36, Issue 11, November 2019, Pages 2498–2511
Franchini P, Xiong P, Fruciano C, Schneider FR, Woltering JM, Hulsey CD, Meyer A
(See online at https://doi.org/10.1093/molbev/msz168)
