Gene duplication in an African cichlid adaptive radiation

Abstract

Background: Gene duplication is a source of evolutionary innovation and can contribute to the divergence of lineages; however, the relative importance of this process remains to be determined. The explosive divergence of the African cichlid adaptive radiations provides both a model for studying the general role of gene duplication in the divergence of lineages and also an exciting foray into the identification of genomic features that underlie the dramatic phenotypic and ecological diversification in this particular lineage. We present the first genome-wide study of gene duplication in African cichlid fishes, identifying gene duplicates in three species belonging to the Lake Malawi adaptive radiation (Metriaclima estherae, Protomelas similis, Rhamphochromis "chilingali") and one closely related species from a non-radiated riverine lineage (Astatotilapia tweddlei).

Results: Using Astatotilapia burtoni as reference, microarray comparative genomic hybridization analysis of 5689 genes reveals 134 duplicated genes among the four cichlid species tested. Between 51 and 55 genes were identified as duplicated in each of the three species from the Lake Malawi radiation, representing a 38%-49% increase in number of duplicated genes relative to the non-radiated lineage (37 genes). Duplicated genes include several that are involved in immune response, ATP metabolism and detoxification.

Conclusions: These results contribute to our understanding of the abundance and type of gene duplicates present in cichlid fish lineages. The duplicated genes identified in this study provide candidates for the analysis of functional relevance with regard to phenotype and divergence. Comparative sequence analysis of gene duplicates can address the role of positive selection and adaptive evolution by gene duplication, while further study across the phylogenetic range of cichlid radiations (and more generally in other adaptive radiations) will determine whether the patterns of gene duplication seen in this study consistently accompany rapid radiation.

Figure 1

Maximum likelihood phylogeny illustrating the positions of experimental (stars) and reference (circle) taxa. The maximum likelihood tree is based on 1785 bp mitochondrial ND2. Nodes not supported by 50% maximum likelihood SH values collapsed and Lake Victoria, Lake Makgadikgadi, and Lake Tanganyika radiations are represented by triangles. The tree is rooted with Oreochromis and the scale bar indicates the mean number of nucleotide substitutions per site (DRYAD doi:10.5061/dryad.7vs2c).

Figure 2

Genes identified as duplicated among test species (P < 0.1 FDR). A. twe: A. tweddlei; M. est: M. estherae; P. sim: P. similis; R. chi: R. “chilingali”. Shared: genes found duplicated in multiple species; Specific: genes found duplicated in only one species; lake: species belonging to the Lake Malawi radiation (M. estherae, P. similis, R. “chilingali”); river: the river species A. tweddlei.

Figure 3

qPCR validates gene copy number determined by aCGH. Abbreviations are genus and species initials. Primer loci are named for the Genbank number of the A. burtoni array feature sequence. **P <0.1 FDR, *P <0.2 FDR found by array analysis.