Journal of Molecular Evolution

, Volume 73, Issue 5–6, pp 355–368 | Cite as

Molecular Characterization of Two Endothelin Pathways in East African Cichlid Fishes

Article

Abstract

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.

Keywords

Endothelin receptor Pigmentation Pharyngeal jaw Neural crest Key innovation Molecular evolution 

Notes

Acknowledgments

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.

Supplementary material

239_2012_9483_MOESM1_ESM.doc (52 kb)
Supplementary material 1 (DOC 52 kb)
239_2012_9483_MOESM2_ESM.doc (54 kb)
Supplementary material 2 (DOC 53 kb)
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Supplementary material 3 (DOC 39 kb)
239_2012_9483_MOESM4_ESM.pdf (655 kb)
Supplementary Fig. 1 Expression patterns of studied loci. For each PCR 20 ng of template cDNA was used and 5 μl PCR product was loaded on a 1,5% agarose gel. a The PCR products of the amplificated GAPDH (~800 bp), EdnrAa (~300 bp), Edn1 (~600 bp), EdnrB1a (~700 bp) and Edn3b (~500 bp) loci for the following tissues; brain (Br), liver (Li), gonads (Go), muscle (Mu), pharyngeal jaw (Pj), maxilla (Mx), mandible (Mn), skin (Sk), anal fin (Af), caudal fin (Cf), eye (Ey), whole juveniles as positive control (Pc) and H2O as negative control (Nc). b The PCR products for the non-egg spot tissue (Ne) and egg spot tissue (E) (PDF 656 kb)
239_2012_9483_MOESM5_ESM.pdf (429 kb)
Supplementary Fig. 2 Consensus phylogenies of the ML analyses of the endothelin family members with their teleost homologs. a Phylogenetic relationships of cichlid endothelin proteins (223 AA) and their teleost orthologs using the JTT+I+G model. The cichlid Edn1 sequences (collapsed and depicted as triangle) cluster together with other teleost Edn1. Similarly, the cichlid Edn3b sequences cluster together with the teleost Edn3b sequences. b Phylogenetic relationships of cichlid endothelin receptor proteins (463 AA) and their teleost orthologs using the Blosum62+G model. Cichlid EdnrAa sequences cluster together with the teleost EdnrAa sequences, while cichlid EdnrB1a cluster together with teleost EdnrB1a sequences (PDF 428 kb)
239_2012_9483_MOESM6_ESM.pdf (897 kb)
Supplementary Fig. 3 Bayesian phylogenetic hypotheses of the wds data set of all studied loci. Five major cichlid lineages are retrieved in most analyses and indicated by the following color scheme: asparagus green=Lamprologini, blue=Perissodini, orange=Limnochromini, green=Ectodini, maroon=Tropheini and Haplochromini. The trees were rooted with T. polylepis (Tylochromini) and O. tanganicae (Tilapiini). Branch lengths for T. polylepis were shortened (50%) in all phylogenies. ML bootstrap values and BAY posterior probabilities above 50% are indicated respectively above and under the branch. a Phylogeny based on the concatenated data set (i.e., the four Endothelin family members plus one additional non-Endothelin, autosomal coding gene; total length: 9451 bp) using the GTR+I+G model. Tribes belonging to the C-lineage (Cyprichromini, Cyphotilapiini, Perissodini, Limnochromini, Ectodini, Tropheini and Haplochromini) are highlighted in grey. Phylogenetic relationships between clades are largely in agreement with available species trees (Salzburger et al. 2002; 2005; 2007). b Phylogeny based on Edn1 (2449 bp) using the HKY+G model showing a seven-tribe polytomy for the derived clades. C. leptosoma is clustering within the lamprologines. c Phylogeny based on Edn3b (512 bp) using the HKY+G model. The tree is mostly unresolved, with two Lamprologini species at the base of a major polytomy. Several tribes are identified (i.e., Perissodini, Ectodini and Tropheini and Haplochromini). d Phylogeny based on EdnrAa (963 bp) using the HKY+G model showing a six-tribe polytomy for the derived clades, while the five major tribes are recovered. e Phylogeny based on EdnrB1a (2091 bp) using the GTR+G model. A basal position was found for the ectodines, the lamprologines and perissodines were found at a more derived position. Note that the Tropheini are the Tanganyikan representatives of the Haplochromini (Salzburger et al. 2005) (PDF 897 kb)

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© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Zoological InstituteUniversity of BaselBaselSwitzerland

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