Hydrobiologia

, Volume 791, Issue 1, pp 145–154 | Cite as

Effects of interspecific gene flow on the phenotypic variance–covariance matrix in Lake Victoria Cichlids

  • Kay Lucek
  • Lucie Greuter
  • Oliver M. Selz
  • Ole Seehausen
Advances in Cichlid Research II

Abstract

Quantitative genetics theory predicts adaptive evolution to be constrained along evolutionary lines of least resistance. In theory, hybridization and subsequent interspecific gene flow may, however, rapidly change the evolutionary constraints of a population and eventually change its evolutionary potential, but empirical evidence is still scarce. Using closely related species pairs of Lake Victoria cichlids sampled from four different islands with different levels of interspecific gene flow, we tested for potential effects of introgressive hybridization on phenotypic evolution in wild populations. We found that these effects differed among our study species. Constraints measured as the eccentricity of phenotypic variance–covariance matrices declined significantly with increasing gene flow in the less abundant species for matrices that have a diverged line of least resistance. In contrast, we find no such decline for the more abundant species. Overall our results suggest that hybridization can change the underlying phenotypic variance–covariance matrix, potentially increasing the adaptive potential of such populations.

Keywords

Eccentricity Line of least resistance Hybridization Evolutionary constraints P matrix 

Supplementary material

10750_2016_2838_MOESM1_ESM.eps (330 kb)
Supplementary material 1 (EPS 330 kb)Figure S1 A comparison of trait-by-trait covariances for Pundamilia pundamilia (ellipses in black) and P. nyereri (ellipses in blue) from Makobe Island. Covariances are scaled, hence only the differences in shape are shown. Red asterisks mark instances where the angle of the underlying LLR differs significantly (p < 0.05) between species, whereas green asterisks depict cases where the intercept differs between species. Abbreviations are as follow: BD - body depth, HL - head length, LJL - lower jaw length, LJW - lower jaw width, SnL - snout length, POD - preorbital depth, ChD - cheek depth, EyL - eye length, EyD - eye depth, IOW - interorbital width, POW - preorbital width, SnW - snout width
10750_2016_2838_MOESM2_ESM.docx (38 kb)
Supplementary material 2 (DOCX 38 kb)

References

  1. Abbott, R., D. Albach, S. Ansell, J. W. Arntzen, S. J. E. Baird, N. Bierne, J. W. Boughman, A. Brelsford, C. A. Buerkle, R. Buggs, R. K. Butlin, U. Dieckmann, F. Eroukhmanoff, A. Grill, S. H. Cahan, J. S. Hermansen, G. Hewitt, A. G. Hudson, C. Jiggins, J. Jones, B. Keller, T. Marczewski, J. Mallet, P. Martinez-Rodriguez, M. Möst, S. Mullen, R. Nichols, A. W. Nolte, C. Parisod, K. Pfennig, A. M. Rice, M. G. Ritchie, B. Seifert, C. M. Smadja, R. Stelkens, J. M. Szymura, R. Vainola, J. B. W. Wolf & D. Zinner, 2013. Hybridization and speciation. Journal of evolutionary Biology 26: 229–246.CrossRefPubMedGoogle Scholar
  2. Arnold, S. J. & P. C. Phillips, 1999. Hierarchical comparison of genetic variance-covariance matrices. II. Coastal-inland divergence in the garter snake. Thamnophis elegans. Evolution 53: 1516–1527.Google Scholar
  3. Arnold, S. J., R. Bürger, P. A. Hohenlohe, B. C. Ajie & A. G. Jones, 2008. Understanding the evolution and stability of the G-matrix. Evolution 62: 2451–2461.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bailey, R. I., F. Eroukhmanoff & G.-P. Sætre, 2013. Hybridization and genome evolution II: mechanisms of species divergence and their effects on evolution in hybrids. Current Zoology 59: 675–685.CrossRefGoogle Scholar
  5. Barel, C. D. N., M. vanOijen, F. Witte & E. Wittemaas, 1977. An introduction to taxonomy and morphology of haplochromine cichlidae from Lake Victoria. Netherlands Journal of Zoology 27: 333–380.CrossRefGoogle Scholar
  6. Berner, D., 2009. Correction of a bootstrap approach to testing for evolution along lines of least resistance. Journal of Evolutionary Biology 22: 2563–2565.CrossRefPubMedGoogle Scholar
  7. Blows, M. W., S. L. Allen, J. M. Collet, S. F. Chenoweth & K. McGuigan, 2015. The phenome-wide distribution of genetic variance. American Naturalist 186: 15–30.CrossRefPubMedGoogle Scholar
  8. Calsbeek, B., S. Lavergne, M. Patel & J. Molofsky, 2011. Comparing the genetic architecture and potential response to selection of invasive and native populations of reed canary grass. Evolutionary Applications 4: 726–735.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chapuis, E., G. Martin & J. Goudet, 2008. Effects of selection and drift on G matrix evolution in a heterogeneous environment: a multivariate Qst-Fst Test with the freshwater snail Galba truncatula. Genetics 180: 2151–2161.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cheverud, J. M., 1988. A Comparison of genetic and phenotypic correlations. Evolution 42: 958–968.CrossRefGoogle Scholar
  11. Draghi, J. A. & M. C. Whitlock, 2012. Phenotypic plasticity facilitates mutational variance, genetic variance, and evolvability along the major axis of environmental variation. Evolution 66: 2891–2902.CrossRefPubMedGoogle Scholar
  12. Eroukhmanoff, F., 2009. Just how much is the G-matrix actually constraining adaptation? Evolutionary Biology 36: 323–326.CrossRefGoogle Scholar
  13. Eroukhmanoff, F. & E. I. Svensson, 2008. Phenotypic integration and conserved covariance structure in calopterygid damselflies. Journal of Evolutionary Biology 21: 514–526.CrossRefPubMedGoogle Scholar
  14. Eroukhmanoff, F. & E. I. Svensson, 2011. Evolution and stability of the G-matrix during the colonization of a novel environment. Journal of Evolutionary Biology 24: 1363–1373.CrossRefPubMedGoogle Scholar
  15. Falconer, D. S., 1989. Introduction to Quantitative Genetics. Wiley, New York.Google Scholar
  16. Fox, J. & S. Weisberg, 2011. An R Companion to Applied Regression. Sage Publications Inc., Thousand Oaks.Google Scholar
  17. Gilman, R. T. & J. E. Behm, 2011. Hybridization, species collapse, and species reemergence after disturbance to premating mechanisms of reproductive isolation. Evolution 65: 2592–2605.CrossRefPubMedGoogle Scholar
  18. Grant, P. R. & B. R. Grant, 1994. Phenotypic and genetic effects of hybridization in Darwin’s finches. Evolution 48: 297–316.CrossRefGoogle Scholar
  19. Greg, S., 2015. Lake Victoria Shapefiles. figshare. https://dx.doi.org/10.6084/m9.figshare.1494839.v1
  20. Guillaume, F. & M. C. Whitlock, 2007. Effects of migration on the genetic covariance matrix. Evolution 61: 2398–2409.CrossRefPubMedGoogle Scholar
  21. Hine, E., S. F. Chenoweth, H. D. Rundle & M. W. Blows, 2009. Characterizing the evolution of genetic variance using genetic covariance tensors. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 364: 1567–1578.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Jones, A. G., S. J. Arnold & R. Borger, 2003. Stability of the G-matrix in a population experiencing pleiotropic mutation, stabilizing selection, and genetic drift. Evolution 57: 1747–1760.CrossRefPubMedGoogle Scholar
  23. Kirkpatrick, M., 2009. Patterns of quantitative genetic variation in multiple dimensions. Genetica 136: 271–284.CrossRefPubMedGoogle Scholar
  24. Klingenberg, C. P., 2010. Evolution and development of shape: integrating quantitative approaches. Nature Reviews Genetics 11: 623–635.PubMedGoogle Scholar
  25. Lande, R., 1979. Quantitative genetic analysis of multivariate evolution, applied to brain:body size allometry. Evolution 33: 402–416.CrossRefGoogle Scholar
  26. Lande, R., 2009. Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. Journal of Evolutionary Biology 22: 1435–1446.CrossRefPubMedGoogle Scholar
  27. Lande, R. & S. J. Arnold, 1983. The measurement of selection on correlated characters. Evolution 37: 1210–1226.CrossRefGoogle Scholar
  28. Lucek, K., A. Sivasundar, B. K. Kristjánsson, S. Skulason & O. Seehausen, 2014a. Quick divergence but slow convergence during ecotype formation in lake and stream stickleback pairs of variable age. Journal of Evolutionary Biology 27: 1878–1892.CrossRefPubMedGoogle Scholar
  29. Lucek, K., M. Lemoine & O. Seehausen, 2014b. Contemporary ecotypic divergence during a recent range expansion was facilitated by adaptive introgression. Journal of Evolutionary Biology 27: 2233–2248.CrossRefPubMedGoogle Scholar
  30. Lucek, K., A. Sivasundar & O. Seehausen, 2014c. Disentangling the role of phenotypic plasticity and genetic divergence in contemporary ecotype formation during a biological invasion. Evolution 68: 2619–2632.CrossRefPubMedGoogle Scholar
  31. Magalhaes, I. S., S. Mwaiko, M. V. Schneider & O. Seehausen, 2009. Divergent selection and phenotypic plasticity during incipient speciation in Lake Victoria cichlid fish. Journal of Evolutionary Biology 22: 260–274.CrossRefPubMedGoogle Scholar
  32. Mallet, J., 2007. Hybrid speciation. Nature 446: 279–283.CrossRefPubMedGoogle Scholar
  33. Meier, J. I., V. C. Sousa, D. A. Marques, O. M. Selz, C. E. Wagner, L. Excoffier, & O. Seehausen, 2016. Demographic modeling of whole genome data reveals parallel origin of similar Pundamilia cichlid species after hybridization. submitted.Google Scholar
  34. Nolte, A. W., J. Freyhof, K. Stemshorn & D. Tautz, 2005. An invasive lineage of sculpins, Cottus sp (Pisces, Teleostei) in the Rhine with new habitat adaptations has originated from hybridization between old phylogeographic groups. Proceedings of the Royal Society of London Series B, Biological Sciences 272: 2379–2387.CrossRefGoogle Scholar
  35. Orr, H. A., 2005. The genetic theory of adaptation: a brief history. Nature Reviews Genetics 6: 119–127.CrossRefPubMedGoogle Scholar
  36. Parsons, K. J., Y. H. Son & R. C. Albertson, 2011. Hybridization promotes evolvability in african cichlids: connections between transgressive segregation and phenotypic integration. Evolutionary Biology 38: 306–315.CrossRefGoogle Scholar
  37. Reist, J. D., 1986. An empirical evaluation of coefficients used in residual and allometric adjustment of size covariation. Canadian Journal Of Zoology 64: 1363–1368.CrossRefGoogle Scholar
  38. Renaud, S., P. Alibert & J.-C. Auffray, 2012. Modularity as a source of new morphological variation in the mandible of hybrid mice. BMC Evolutionary Biology 12: 141.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Rieseberg, L. H., O. Raymond, D. M. Rosenthal, Z. Lai, K. Livingstone, T. Nakazato, J. L. Durphy, A. E. Schwarzbach, L. A. Donovan & C. Lexer, 2003. Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301: 1211–1216.CrossRefPubMedGoogle Scholar
  40. Roseman, C. C., 2016. Random genetic drift, natural selection, and noise in human cranial evolution. American Journal of Physical Anthropology. doi:10.1002/ajpa.22918.PubMedGoogle Scholar
  41. Rudman, S. M. & D. Schluter, 2016. Ecological impacts of reverse speciation in threespine stickleback. Current Biology 26: 490–495.CrossRefPubMedGoogle Scholar
  42. Schluter, D., 1996. Adaptive radiation along genetic lines of least resistance. Evolution 50: 1766–1774.CrossRefGoogle Scholar
  43. Schluter, D., 2000. The Ecology of Adaptive Radiation. Oxford University Press, Oxford.Google Scholar
  44. Seehausen, O., 2006. African cichlid fish: a model system in adaptive radiation research. Proceedings of the Royal Society of London Series B, Biological Sciences 273: 1987–1998.CrossRefGoogle Scholar
  45. Seehausen, O. & N. Bouton, 1997. Microdistribution and fluctuations in niche overlap in a rocky shore cichlid community in Lake Victoria. Ecology of Freshwater Fish 6: 161–173.CrossRefGoogle Scholar
  46. Seehausen, O., J. vanAlphen & F. Witte, 1997. Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277: 1808–1811.CrossRefGoogle Scholar
  47. Seehausen, O., E. Lippitsch, N. Bouton & H. Zwennes, 1998. Mbipi, the rock-dwelling cichlids of Lake Victoria: description of three new genera and fifteen new species (Teleostei). Ichthyological Exploration of Freshwaters 9: 129–228.Google Scholar
  48. Seehausen, O., Y. Terai, I. S. Magalhaes, K. L. Carleton, H. D. J. Mrosso, R. Miyagi, I. van der Sluijs, M. V. Schneider, M. E. Maan, H. Tachida, H. Imai & N. Okada, 2008. Speciation through sensory drive in cichlid fish. Nature 455: 620–626.CrossRefPubMedGoogle Scholar
  49. Seehausen, O., R. K. Butlin, I. Keller, C. E. Wagner, J. W. Boughman, P. A. Hohenlohe, C. L. Peichel, G.-P. Saetre, C. Bank, Å. Brännström, A. Brelsford, C. S. Clarkson, F. Eroukhmanoff, J. L. Feder, M. C. Fischer, A. D. Foote, P. Franchini, C. D. Jiggins, F. C. Jones, A. K. Lindholm, K. Lucek, M. E. Maan, D. A. Marques, S. H. Martin, B. Matthews, J. I. Meier, M. Möst, M. W. Nachman, E. Nonaka, D. J. Rennison, J. Schwarzer, E. T. Watson, A. M. Westram & A. Widmer, 2014. Genomics and the origin of species. Nature Reviews Genetics 15: 176–192.CrossRefPubMedGoogle Scholar
  50. Selz, O. M., K. Lucek, K. A. Young & O. Seehausen, 2014. Relaxed trait covariance in interspecific cichlid hybrids predicts morphological diversity in adaptive radiations. Journal of Evolutionary Biology 27: 11–24.CrossRefPubMedGoogle Scholar
  51. Stelkens, R. B., M. A. Brockhurst, G. D. D. Hurst & D. Greig, 2014. Hybridization facilitates evolutionary rescue. Evolutionary Applications 7: 1209–1217.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Stelkens, R. & O. Seehausen, 2009. Genetic distance between species predicts novel trait expression in their hybrids. Evolution 63: 884–897.CrossRefPubMedGoogle Scholar
  53. Steppan, S., P. C. Phillips & D. Houle, 2002. Comparative quantitative genetics: evolution of the G matrix. Trends in Ecology and Evolution 17: 320–327.CrossRefGoogle Scholar
  54. Taylor, E. B., J. W. Boughman, M. Groenenboom, M. Sniatynski, D. Schluter & J. L. Gow, 2006. Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Molecular Ecology 15: 343–355.CrossRefPubMedGoogle Scholar
  55. Vonlanthen, P., D. Bittner, A. G. Hudson, K. A. Young, R. Müller, B. Lundsgaard-Hansen, D. Roy, S. Di Piazza, C. R. Largiadèr & O. Seehausen, 2012. Eutrophication causes speciation reversal in whitefish adaptive radiations. Nature 482: 357–362.CrossRefPubMedGoogle Scholar
  56. Wood, C. W. & E. D. Brodie, 2015. Environmental effects on the structure of the G-matrix. Evolution 69: 2927–2940.CrossRefPubMedGoogle Scholar
  57. Wright, S., 1932. The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proceedings of the sixth international congress of genetics: 356–366.Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Kay Lucek
    • 1
    • 2
    • 3
  • Lucie Greuter
    • 1
    • 2
  • Oliver M. Selz
    • 1
    • 2
  • Ole Seehausen
    • 1
    • 2
  1. 1.Division of Aquatic Ecology and Evolution, Institute of Ecology and EvolutionUniversity of BernBernSwitzerland
  2. 2.Department of Fish Ecology and Evolution, EAWAG Swiss Federal Institute of Aquatic Science and TechnologyCenter of Ecology, Evolution and BiogeochemistryKastanienbaumSwitzerland
  3. 3.Department of Animal and Plant SciencesUniversity of SheffieldSheffieldUK

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