The genomic substrate for adaptive radiation in African cichlid fish

Evolutionary diversification among species attracts the attention of scientist during long time. Adaptive radiation underlies evolution and comprises the rapid adaptation of a single lineage to its changed environment which provides new resources and opens new environmental niches. Among all biological groups which have undergone evolutionary adaptive radiation the cichlids have been more studied by biologists. In this paper, authors investigated the molecular mechanisms and genomic substrates triggering rapid evolutionary diversification in African cichlid fish through comparative analysis of genomes of five different African cichlid lineages, together with an examination of the genetic changes responsible for divergence in six closely related species from Lake Victoria. They found some differences in all investigated East African lineages compared to ancestral, including increasing gene duplication, an excess of non-coding elements, accelerated evolution of coding sequence and divergence in the expression levels connected with transposons insertions. They also discovered novel microRNAs that alter gene expression in cichlids and genome-wide diversifying selection in coding and regulatory elements. Thus, authors have concluded that multiple molecular mechanisms together with relaxed purifying selection can promote evolutionary diversification in African cichlid fish.
Principle results and discussion
Authors selected and sequenced the genome of five lineages of African cichlids: four members of the East African lineage, including Neolamprologus brichardi/pulcher from Lake Tanganyika characterized by older radiation, Metriaclima zebra from Lake Malawi, Pundamilia nyererei from Lake Victoria and Astatotilapia burtoni from Lake Tanganyika, as well as an ancestral lineage with low diversity Nile tilapia (Oreochromis niloticus). All these lineages diverged through geographical isolation and, then, three of them underwent evolutionary adaptive radiations. Figure 1 illustrates that cichlid phenotypic diversity is caused by natural selection and includes ecological specialization, variation in behaviour, body shape and coloration.
Authors found the high rate of nonsynonymous nucleotide substitutions in genes involved in morphological and developmental process in the East African lineages compared to ancestral that can indicate accelerated evolution. However, relaxed constraint and positive selection can also be associated with accelerated evolution. They also demonstrated that developmental genes implicated in the Bone Morphogenetic Proteins (BMP) pathway, including ligand (bmp4), receptor (bmpr1b) and antagonist (nog2), showed increased rates of protein evolution in haplochromine cichlids. Among 22 genes known to be involved in morphogenesis, body pigmentation and vision authors identified three that are supposed to undergo accelerated evolution, driven by new light condition in novel environment, and could be important for diversification of cichlids. These genes include endothelin receptor type B1 (ednrb1), green-sensitive opsin (kfh-g) and Rhodopsin (rho).
By using three different methods (read-depth analysis, gene and species tree reconciliation analysis and array comparative genomic hybridization analysis) Brawand et al. showed that the East African cichlids have a large number of gene duplicates that is illustrated on Figure 2. However, authors did not precise which method they applied to make this figure. Moreover, all three methods have evident constraints in detection of gene duplicates. This fact and expected low level of overlap between results cast doubt on the rational application of these methods together for study. According obtained results, cichlid specific gene duplicates were not related to particular categories of genes. Additionally, authors postulated that differences in the levels of duplicate genes expression may support evolutionary divergence of species. Duplicate gene pairs were categorized according their expression pattern among different tissues. Many of duplicates had increased specific expression in the testis that correlates with strong sexual selection observed in African cichlids.
Next part of the paper is devoted to analysis whether transposable elements (TE) alter gene expression. In each of investigated cichlid genome authors detected three waves of transposons insertion. Analysis of the distribution of TE insertions revealed that genes with TE insertions close to the 5’UTRs showed increased expression in all tissues in contrast with genes without transposon insertions. On the other hand, TE insertion near the 3’UTRs was associated with increased gene expression in all tissues except brain and skeletal muscles. Moreover, authors observed different orientation bias of transposable elements inserted within or near non-duplicated genes and TE occurring in introns of all investigated cichlid species. Based on these data, they discussed the long period of relaxed purifying selection during which transposable elements insertion happened.
The same idea was supported by further analysis of potential regulatory sequences. In all East African cichlids, authors found highly conserved noncoding elements (hCNEs) and accelerated CNEs (aCNEs) distributed in introns, intergenic regions or UTRs of protein coding genes and showed high rate of nucleotide substitutions, insertions and/or deletions. Interestingly, aCNEs functioned as enhancers and altered the expression of their target genes in contrast to hCNEs. Furthermore, identified novel microRNAs were also able to change target gene expression that is illustrated on Figure 3.
Finally, authors investigated patterns of genome-wide genetic variation of six closely related species from the most recent evolutionary radiation in Lake Victoria. They found that recent rapid speciation was related to genomically prevalent divergence. Moreover, they observed the minimal fixation of alternative alleles from divergent loci between species. Further analysis revealed that in morphologically divergent species there were no exonic SNPs whereas in introns an increasing proportion of SNPs was correlated with increasing Fst that is depicted on Figure 4. Thus, coding and regulatory polymorphism underlies the adaptive radiation of African cichlids and takes old alleles from standing variation.
Present study contributes to further understanding adaptive radiation in African cichlids. Complex approach used by authors reveals multiple genomic and evolutionary mechanisms underlying diversity of East African cichlids population including increased gene duplication, accelerated evolution of coding and regulatory elements, regulation of gene expression by novel microRNAs and transposons insertion, retention of ancient polymorphism. However, sometimes we saw an excess of data, especially in supplementary information, which can confuse the reader. In any case, this paper provides the great resource to deepen our understanding of factors affecting adaptive radiation.

Brawand, D., Wagner, C., Li, Y., Malinsky, M., Keller, I., Fan, S., Simakov, O., Ng, A., Lim, Z., Bezault, E., Turner-Maier, J., Johnson, J., Alcazar, R., Noh, H., Russell, P., Aken, B., Alföldi, J., Amemiya, C., Azzouzi, N., Baroiller, J., Barloy-Hubler, F., Berlin, A., Bloomquist, R., Carleton, K., Conte, M., D’Cotta, H., Eshel, O., Gaffney, L., Galibert, F., Gante, H., Gnerre, S., Greuter, L., Guyon, R., Haddad, N., Haerty, W., Harris, R., Hofmann, H., Hourlier, T., Hulata, G., Jaffe, D., Lara, M., Lee, A., MacCallum, I., Mwaiko, S., Nikaido, M., Nishihara, H., Ozouf-Costaz, C., Penman, D., Przybylski, D., Rakotomanga, M., Renn, S., Ribeiro, F., Ron, M., Salzburger, W., Sanchez-Pulido, L., Santos, M., Searle, S., Sharpe, T., Swofford, R., Tan, F., Williams, L., Young, S., Yin, S., Okada, N., Kocher, T., Miska, E., Lander, E., Venkatesh, B., Fernald, R., Meyer, A., Ponting, C., Streelman, J., Lindblad-Toh, K., Seehausen, O., & Di Palma, F. (2014). The genomic substrate for adaptive radiation in African cichlid fish Nature, 513 (7518), 375-381 DOI: 10.1038/nature13726

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