Speciation through sensory drive in cichlid fish

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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).

References

  1. 1

    Schluter, D. & Price, T. Honesty, perception and population divergence in sexually selected traits. Proc. R. Soc. Lond. B 253, 117–122 (1993)

  2. 2

    Boughman, J. W. How sensory drive can promote speciation. Trends Ecol. Evol. 17, 571–577 (2002)

  3. 3

    Gray, S. M. & McKinnon, J. S. Linking color polymorphism maintenance and speciation. Trends Ecol. Evol. 22, 71–79 (2007)

  4. 4

    Chunco, A. J., McKinnon, J. S. & Servedio, M. R. Microhabitat variation and sexual selection can maintain male color polymorphisms. Evolution 61, 2504–2515 (2007)

  5. 5

    Kawata, M., Shoji, A., Kawamura, S. & Seehausen, O. A genetically explicit model of speciation by sensory drive within a continuous population in aquatic environments. BMC Evol. Biol. 7, 99 (2007)

  6. 6

    Boughman, J. W. Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411, 944–948 (2001)

  7. 7

    Levring, T. & Fish, G. R. The penetration of light in some tropical East African waters. Oikos 7, 98–109 (1956)

  8. 8

    Seehausen, O., van Alphen, J. J. M. & Witte, F. Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277, 1808–1811 (1997)

  9. 9

    Terai, Y. et al. Divergent selection on opsins drives incipient speciation in Lake Victoria cichlids. PLoS Biol. 4, 2244–2251 (2006)

  10. 10

    Shichida, Y. The Retinal Basis of Vision: Visual pigment: photochemistry and molecular evolution (ed. Toyoda, J.-I.) 23–35 (Elsevier Science, 1999)

  11. 11

    Yokoyama, S., Blow, N. S. & Radlwimmer, F. B. Molecular evolution of color vision of zebra finch. Gene 259, 17–24 (2000)

  12. 12

    Carleton, K. L. & Kocher, T. D. Cone opsin genes of African cichlid fishes: Tuning spectral sensitivity by differential gene expression. Mol. Biol. Evol. 18, 1540–1550 (2001)

  13. 13

    Terai, Y., Mayer, W. E., Klein, J., Tichy, H. & Okada, N. The effect of selection on a long wavelength-sensitive (LWS) opsin gene of Lake Victoria cichlid fishes. Proc. Natl Acad. Sci. USA 99, 15501–15506 (2002)

  14. 14

    Parry, J. W. L. et al. Mix and match color vision: Tuning spectral sensitivity by differential opsin gene expression in Lake Malawi cichlids. Curr. Biol. 15, 1734–1739 (2005)

  15. 15

    Carleton, K. et al. Visual sensitivities tuned by heterochronic shifts in opsin gene expression. BMC Biol. 6, 22 (2008)

  16. 16

    Carleton, K. L., Parry, J. W. L., Bowmaker, J. K., Hunt, D. M. & Seehausen, O. Colour vision and speciation in Lake Victoria cichlids of the genus Pundamilia . Mol. Ecol. 14, 4341–4353 (2005)

  17. 17

    Spady, T. C. et al. Adaptive molecular evolution in the opsin genes of rapidly speciating cichlid species. Mol. Biol. Evol. 22, 1412–1422 (2005)

  18. 18

    Genner, M. J. et al. Age of cichlids: New dates for ancient lake fish radiations. Mol. Biol. Evol. 24, 1269–1282 (2007)

  19. 19

    Maan, M. E. et al. Intraspecific sexual selection on a speciation trait, male coloration, in the Lake Victoria cichlid Pundamilia nyererei . Proc. R. Soc. Lond. B 271, 2445–2452 (2004)

  20. 20

    Endler, J. A. Some general comments on the evolution and design of animal communication systems. Phil. Trans. R. Soc. Lond. B 340, 215–225 (1993)

  21. 21

    Vandermeer, H. J., Anker, G. C. & Barel, C. D. N. Ecomorphology of retinal structures in zooplanktivorous haplochromine cichlids (Pisces) from Lake Victoria. Environ. Biol. Fishes 44, 115–132 (1995)

  22. 22

    Smit, S. A. & Anker, G. C. Photopic sensitivity to red and blue light related to retinal differences in two zooplanktivorous haplochromine species (Teleostei, Cichlidae). Neth. J. Zool. 47, 9–20 (1997)

  23. 23

    Maan, M. E., Hofker, K. D., van Alphen, J. J. M. & Seehausen, O. Sensory drive in cichlid speciation. Am. Nat. 167, 947–954 (2006)

  24. 24

    Endler, J. A. Gene flow and population differentiation. Science 179, 243–250 (1973)

  25. 25

    Schluter, D. & Nagel, L. M. Parallel speciation by natural selection. Am. Nat. 146, 292–301 (1995)

  26. 26

    Nosil, P., Egan, S. R. & Funk, D. J. Heterogeneous genomic differentiation between walking-stick ecotypes: “Isolation by adaptation” and multiple roles for divergent selection. Evolution 62, 316–336 (2008)

  27. 27

    Stinchcombe, J. T. & Hoektsra, H. E. Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100, 158–170 (2008)

  28. 28

    Doebeli, M. & Dieckmann, U. Speciation along environmental gradients. Nature 421, 259–264 (2003)

  29. 29

    Gavrilets, S. Fitness Landscapes and the Origin of Species (Princeton Univ. Press. (2004)

  30. 30

    Leimar, O., Doebeli, M. & Dieckmann, U. Evolution of phenotypic clusters through competition and local adaptation along an environmental gradient. Evolution 62, 807–822 (2008)

  31. 31

    Nosil, P., Vines, T. H. & Funk, D. J. Perspective: Reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59, 705–719 (2005)

  32. 32

    Seehausen, O. Lake Victoria Rock Cichlids. Taxonomy, Ecology and Distribution. (Verduijn Cichlids, 1996)

  33. 33

    Seehausen, O. & van Alphen, J. J. M. The effect of male coloration on female mate choice in closely related Lake Victoria cichlids (Haplochromis nyererei complex). Behav. Ecol. Sociobiol. 42, 1–8 (1998)

  34. 34

    Stelkens, R. B., Pierotti, M. E. R., Joyce, D. A., Smith, A. M., van der Sluijs, I. & Seehausen, O. Female mating preferences facilitate disruptive sexual selection on male nuptial colouration in hybrid cichlid fish. Phil. Trans. R. Soc. B 363 2861–2870 (2008)

  35. 35

    Okullo, W. et al. Parameterization of the inherent optical properties of Murchison Bay, Lake Victoria. Appl. Opt. 46, 8553–8561 (2007)

  36. 36

    Palczewski, K. et al. Crystal structure of rhodopsin: A G protein-coupled receptor. Science 289, 739–745 (2000)

  37. 37

    Asenjo, A. B., Rim, J. & Oprian, D. D. Molecular determinants of human red/green color discrimination. Neuron 12, 1131–1138 (1994)

  38. 38

    McDonald, J. H. Improved tests for heterogeneity across a region of DNA sequence in the ratio of polymorphism to divergence. Mol. Biol. Evol. 15, 377–384 (1998)

  39. 39

    Hudson, R. R., Kreitman, M. & Aguade, M. A test of neutral molecular evolution based on nucleotide data. Genetics 116, 153–159 (1987)

  40. 40

    Haesler, M. P. & Seehausen, O. Inheritance of female mating preference in a sympatric sibling species pair of Lake Victoria cichlids: implications for speciation. Proc. R. Soc. B 272, 237–245 (2005)

  41. 41

    van der Sluijs, I., van Alphen, J. J. M. & Seehausen, O. Preference polymorphism for coloration but no speciation in a population of Lake Victoria cichlids. Behav. Ecol. 19, 177–183 (2008)

  42. 42

    Nosil, P., Crespi, B. J. & Sandoval, C. P. Reproductive isolation driven by the combined effects of ecological adaptation and reinforcement. Proc. R. Soc. Lond. B 270, 1911–1918 (2008)

  43. 43

    Nosil, P. & Crespi, B. J. Does gene flow constrain adaptive divergence or vice versa? A test using ecomorphology and sexual isolation in Timema cristinae walking-sticks. Evolution 58, 102–112 (2004)

  44. 44

    Rasanen, K. & Hendry, A. Disentangling interactions between adaptive divergence and gene flow when ecology drives diversification. Ecol. Lett. 11, 624–636 (2008)

  45. 45

    Venables, W. N. & Ripley, B. D. Modern applied statistics with S. (Springer, 2002)

  46. 46

    Excoffier, L., Laval, G. & Schneider, S. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol. Bioinform. Online 1, 47–50 (2005)

  47. 47

    Rice, W. R. Analyzing tables of statistical tests. Evolution 43, 223–225 (1989)

  48. 48

    Belkhir K, Borsa P & Chikhi L Raufaste, N. & Bonhomme, F. Genetix Version 4.05 for Windows Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier (France) (1996–2004) http://www.genetix.univ-montp2.fr/genetix/genetix.htm

  49. 49

    Rozas, J., Sanchez-DelBarrio, J. C., Messeguer, X., Rozas, R. & Dna, S. P. DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497 (2003)

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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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This file contains Supplementary Material, Supplementary Methods, Supplementary Tables S1-S7, Supplementary Figures S1-S4 with Legends and Supplementary References (PDF 666 kb)

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