Molecular Characterization of Two Endothelin Pathways in East African Cichlid Fishes
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The adaptive radiations of cichlid fishes in East Africa have been associated with the acquisition of evolutionary novelties as well as the ecological opportunities existing in the East African Great lakes. Two remarkable evolutionary innovations are the pharyngeal jaw apparatus, found in all cichlid species, and the anal fin egg-spots of mouthbrooding cichlids. Based on their conserved functions during the development of both the jaw apparatus and pigmentation, the endothelin ligands and receptors form a putative link between these naturally and sexually selected traits. Here we study the evolutionary history of four members of two endothelin pathways (Edn1/EdnrAa and Edn3b/EdnrB1a) to elucidate their possible roles during the evolution and development of key innovations in East African cichlids species. The analyses performed on partial sequences (ca. 6,000 bp per taxon) show that all four endothelin family members evolved under purifying selection, although both ligands are characterized by an accelerated rate of protein evolution in comparison to the receptors. In accordance with earlier findings, we show that the mature protein sequence of Edn1 and Edn3 are highly conserved, also in cichlids, whereas the preproendothelin parts are variable indicating relaxed selective constraints. In the receptors, nonsynonymous substitutions were mainly found in the ligand-binding domains suggesting functional divergence. Gene expression assays with Real-Time PCR indeed reveal that the two studied endothelin pathways are expressed in the cichlid pharyngeal jaw and in the haplochromine egg-spot (among other pigment-cell containing tissues), suggesting their involvement during morphogenesis of naturally and sexually selected traits in cichlids.
KeywordsEndothelin receptor Pigmentation Pharyngeal jaw Neural crest Key innovation Molecular evolution
We would like to thank Brigitte Aeschbach and Nicolas Boileau for help and advice on the lab work, Michael Matschiner for advice on the phylogenetic analyses, Emilia Santos for providing the “egg-spots” and “non-egg-spots” RNA samples and Laura Baldo for providing the K a/K s values from the cichlid EST comparison. We are very grateful to Ingo Braasch and the anonymous reviewers for their valuable comments and suggestions on earlier version of this manuscript. This study was supported by the European Research Council (Starting Grant “INTERGENADAPT” to WS) and the Swiss National Science Foundation (Grant 3100A0_122458 to WS).
Conflict of interest
The authors declare that they have no conflict of interest.
- Barlow GW (2000) The cichlid fishes: nature’s grand experiment in evolution. Perseus publishing, CambridgeGoogle Scholar
- Bruford MW, Hanotte O, Brookfield JFY, Burke T (1998) Multilocus and single-locus DNA fingerprinting. In: Hoelzel AR (ed) Molecular genetic analysis of populations: a practical approach. Oxford University Press, Oxford, pp 287–336Google Scholar
- Coulter GW (1991) Lake Tanganyika and its life. British Museum (Natural History) and Oxford University Press, OxfordGoogle Scholar
- Fryer G, Iles TD (1972) The cichlid fishes of the Great Lakes of Africa: their biology and Evolution. Oliver & Boyd, EdinburghGoogle Scholar
- Hall BK (1999) The neural crest in development and evolution. Springer-Verlag, New YorkGoogle Scholar
- Hughes AL (1999) Adaptive evolution of genes and genomes. Oxford University Press, OxfordGoogle Scholar
- Keenleyside MHA (1991) Cichlid fishes: behaviour, ecology and evolution. Chapman & Hall, LondonGoogle Scholar
- Kocher TD (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nat Genet 5:288–298Google Scholar
- Kurihara Y, Kurihara H, Suzuki H, Kodama T, Maemura K, Nagai R, Oda H, Kuwaki T, Cao W-H, Kamada N, Jishage K, Ouchi Y, Azuma S, Toyoda Y, Ishikawa T, Kumada M, Yazaki Y (1994) Elevated blood-pressure and craniofacial abnormalities in mice deficient in endothelin-1. Nature 368:703–710PubMedCrossRefGoogle Scholar
- Liem KF (1973) Evolutionary strategies and morphological innovations: cichlid pharyngeal jaws. Syst Biol 22:425–441Google Scholar
- McGill GG, Horstmann M, Widlund HR, Du J, Motyckova G, Nishimura E, Lin Y-L, Ramaswamy S, Avery W, Ding H-F, Jordan S, Jackson I, Korsmeyer S, Golub T, Fisher D (2002) Bcl2 regulation by the melanocyte master regulator Mitf modulates lineage survival and melanoma cell viability. Cell 109:707–718PubMedCrossRefGoogle Scholar
- Ohno S (1970) Evolution by gene duplication. Springer Verlag, New YorkGoogle Scholar
- Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, OxfordGoogle Scholar
- Simpson GG (1953) The major features of evolution. Columbia University Press, New YorkGoogle Scholar
- Slack JMW (2001) Essential developmental biology. Blackwell Publishing, OxfordGoogle Scholar
- Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). VERSION 4. Sinauer Associates, SunderlandGoogle Scholar