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Speciation through sensory drive in cichlid fish

Abstract

Theoretically, divergent selection on sensory systems can cause speciation through sensory drive. However, empirical evidence is rare and incomplete. Here we demonstrate sensory drive speciation within island populations of cichlid fish. We identify the ecological and molecular basis of divergent evolution in the cichlid visual system, demonstrate associated divergence in male colouration and female preferences, and show subsequent differentiation at neutral loci, indicating reproductive isolation. Evidence is replicated in several pairs of sympatric populations and species. Variation in the slope of the environmental gradients explains variation in the progress towards speciation: speciation occurs on all but the steepest gradients. This is the most complete demonstration so far of speciation through sensory drive without geographical isolation. Our results also provide a mechanistic explanation for the collapse of cichlid fish species diversity during the anthropogenic eutrophication of Lake Victoria.

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Figure 1: Male phenotypes, light gradients and LWS opsin absorbance.
Figure 2: Ecological, phenotypic, genetic and behavioural differentiation between blue and red Pundamilia nuptial phenotypes at five islands.
Figure 3: Measures of differentiation between sympatric Pundamilia phenotypes plotted against water transparency (left) and light slope (right).

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Acknowledgements

We acknowledge the Tanzania Commission for Science & Technology for research permissions, the Tanzania Fisheries Research Institute, and its Muranza Centre director E. F. B. Katunzi, for hospitality and logistical support; M. Kayeba, M. Haluna, S. Mwaiko, M. Haesler and E. Burgerhout for help with data and fish collection; H. Araki, L. Excoffier, L. Harmon, B. Ibelings, I. Keller, T. Kocher, P. Nosil, M. Pierotti, D. Schluter, A. Sivasundar and O. Svensson for comments on the manuscript; and M. Kawata, J. J. M. van Alphen, K. Young, R. Stelkens and E. Bezault for discussion. This work was supported by Swiss National Science Foundation project 3100A0-106573 (to O.S.), and by the Ministry of Education, Culture, Sports, Science and Technology of Japan (to N.O.).

Author Contributions O.S. conceived and designed the study, collected, photographed and identified fish, measured light and shore slopes, supervised field work, conducted the hybridization experiments, supervised microsatellite analyses and mate choice experiments, and did the statistical data analyses and the writing. Y.T. designed experiments on opsins, did most of the laboratory work and data analysis on opsins, and contributed to writing. I.S.M. collected depth distribution data and did all microsatellite analyses. K.L.C. determined LWS sequences from experimental females and contributed to writing. H.D.J.M. collected depth distribution, light data and fish. R.M. determined LWS and SWS2A sequences with Y.T. I.v.d.S. collected fish and conducted mate choice experiments. M.V.S. helped with the microsatellite analysis. M.E.M. collected fish and measured light. H.T. performed analysis of selection pressure with Y.T. H.I. measured opsin pigment absorbance with Y.T. N.O. designed and supervised the laboratory work on opsins and contributed to the writing.

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Correspondence to Ole Seehausen or Norihiro Okada.

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Seehausen, O., Terai, Y., Magalhaes, I. et al. Speciation through sensory drive in cichlid fish. Nature 455, 620–626 (2008). https://doi.org/10.1038/nature07285

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