Migration and the Genetic Covariance between Habitat Preference and Performance

P. Nosil, B. J. Crespi, C. P. Sandoval and M. Kirkpatrick
The American Naturalist
Vol. 167, No. 3 (March 2006), pp. E66-E78
DOI: 10.1086/499383
Stable URL: http://www.jstor.org/stable/10.1086/499383
Page Count: 13
  • Download PDF
  • Cite this Item

You are not currently logged in.

Access your personal account or get JSTOR access through your library or other institution:


Log in to your personal account or through your institution.

Migration and the Genetic Covariance between Habitat Preference and Performance
We're having trouble loading this content. Download PDF instead.


Abstract: Studies of the genetic covariance between habitat preference and performance have reported conflicting outcomes ranging from no covariance to strong covariance. The causes of this variability remain unclear. Here we show that variation in the magnitude of genetic covariance can result from variability in migration regimes. Using data from walking stick insects and a mathematical model, we find that genetic covariance within populations between host plant preference and a trait affecting performance on different hosts (cryptic color pattern) varies in magnitude predictably among populations according to migration regimes. Specifically, genetic covariance within populations is high in heterogeneous habitats where migration between populations locally adapted to different host plants generates nonrandom associations (i.e., linkage disequilibrium) between alleles at color pattern and host preference loci. Conversely, genetic covariance is low in homogeneous habitats where a single host exists and migration between hosts does not occur. Our results show that habitat structure and patterns of migration can strongly affect the evolution and variability of genetic covariance within populations.

Notes and References

This item contains 62 references.

Literature Cited
  • ['Armbruster, W. S., and K. E. Schwaegerle. 1996. Causes of covariation in phenotypic traits among populations. Journal of Evolutionary Biology 9:261–276.']
  • ['Arnold, S. J. 1992. Constraints on phenotypic evolution. American Naturalist 140(suppl.):S85–S107.']
  • ['Barton, N. H. 1995. Linkage and the limits to natural selection. Genetics 140:821–841.']
  • ['Beerli, P., and J. Felsenstein. 2001. Maximum‐likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proceedings of the National Academy of Sciences of the USA 98:4563–4568.']
  • ['Begin, M., and D. Roff. 2004. From micro‐ to macroevolution through quantitative genetic variation: positive evidence from field crickets. Evolution 58:2287–2304.']
  • ['Bernays, E. A., and W. T. Wcislo. 1994. Sensory capabilities, information processing, and resource specialization. Quarterly Review of Biology 69:187–204.']
  • ['Blows, M. W., and M. Higgie. 2003. Genetic constraints on the evolution of mate recognition under natural selection. American Naturalist 161:240–253.']
  • ['Bond, A. B., and A. C. Kamil. 2002. Visual predators select for crypticity and polymorphism in virtual prey. Nature 415:609–613.']
  • ['Bossart, J. L. 2003. Covariance of performance and preference on normal and novel hosts in a locally monophagous and locally polyphagous butterfly population. Oecologia (Berlin) 135:477–486.']
  • ['Brodie, B. 1989. Genetic correlations between morphology and antipredator behavior in natural populations of the garter snake Thampnophis ordinoides. Nature 342:542–543.']
  • ['Cott, H. B. 1940. Adaptive coloration in animals. Oxford University Press, New York.']
  • ['Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer, Sunderland, MA.']
  • ['Crespi, B. J., and C. P. Sandoval. 2000. Phylogenetic evidence for the evolution of ecological specialization in Timema walking‐sticks. Journal of Evolutionary Biology 13:249–262.']
  • ['Diehl, S. R., and G. L. Bush. 1989. The role of habitat preference in adaptation and speciation. Pages 345–365 in D. Otte and J. Endler, eds. Speciation and its consequences. Sinauer, Sunderland, MA.']
  • ['Endler, J. A. 1984. Progressive background matching in moths, and a quantitative measure of crypsis. Biological Journal of the Linnean Society 22:187–231.']
  • ['Falconer, D. S., and T. F. C. MacKay. 1996. Introduction to quantitative genetics. 4th ed. Prentice Hall, Englewood Cliffs, NJ.']
  • ['Felsenstein, J. 1981. Skepticism towards Santa Rosalia, or why are there so few kinds of animals? Evolution 35:124–138.']
  • ['Fisher, R. A. 1918. The correlation between relatives on the supposition of Mendelian inheritance. Transactions of the Royal Society of Edinburg 52:399–433.']
  • ['Forister, M. L. 2004. Oviposition preference and larval performance within a diverging lineage of lycaenid butterflies. Ecological Entomology 29:264–272.']
  • ['Fox, C. W. 1993. A quantitative genetic analysis of oviposition preference and larval performance on two hosts in the bruchid beetle, Callosobruchus maculatus. Evolution 47:166–175.']
  • ['Fry, J. D. 1996. The evolution of host specialization: are trade‐offs overrated? American Naturalist 148(suppl.):S84–S107.']
  • ['Funk, D. J. 1998. Isolating a role for natural selection in speciation: host adaptation and sexual isolation in Neochlamisus bebbianae leaf beetles. Evolution 52:1744–1759.']
  • ['Funk, D. J., K. E. Filchak, and J. L. Feder. 2002. Herbivorous insects: model systems for the comparative study of speciation ecology. Genetica 116:251–267.']
  • ['Futuyma, D. J., and G. Moreno. 1988. The evolution of ecological specialization. Annual Review of Ecology and Systematics 19:207–233.']
  • ['Gillis, J. E. 1982. Substrate color‐matching cues in the cryptic grasshopper Circotettix rabula rabula (Rehn and Hebard). Animal Behaviour 30:113–116.']
  • ['Gould, S. J. 1977. Ontogeny and phylogeny. Harvard University Press, Cambridge, MA.']
  • ['Grant, B., and R. J. Howlett. 1988. Background selection by the peppered moth (Biston betularia Linn.): individual differences. Biological Journal of the Linnean Society 33:217–232.']
  • ['Hawthorne, D. J., and S. Via. 2001. Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature 412:904–907.']
  • ['Hodges, S. A., J. B. Whittall, M. Fulton, and J. Y. Yang. 2002. Genetics of floral traits influencing reproductive isolation between Aquilegia formosa and Aquilegia pubescens. American Naturalist 159(suppl.):S51–S60.']
  • ['Jaenike, J., and R. D. Holt. 1991. Genetic variation for habitat preference: evidence and explanations. American Naturalist 137(suppl.):S67–S90.']
  • ['Jernigan, R. W., D. C. Culver, and D. W. Fong. 1994. The dual role of selection and evolutionary history as reflected in genetic correlations. Evolution 48:587–596.']
  • ['Kawecki, T. J. 2004. Genetic theories of sympatric speciation. Pages 36–53 in U. Dieckmann, M. Doebeli, J. A. J. Metz, and D. Tautz, eds. Adaptive speciation. Cambridge University Press, Cambridge.']
  • ['Kettlewell, H. B. D. 1955. Recognition of appropriate backgrounds by the pale and black phases of Lepidoptera. Nature 175:943–944.']
  • ['———. 1973. The evolution of melanism. Clarendon, Oxford.']
  • ['Kimura, M. 1956. A model of genetic system which leads to closer linkage by natural selection. Evolution 10:278–287.']
  • ['Kirkpatrick, M., and V. Ravigné. 2002. Speciation by natural and sexual selection: models and experiments. American Naturalist 159(suppl.):S22–S35.']
  • ['Kirkpatrick, M., T. Johnson, and N. Barton. 2002. General models of multilocus evolution. Genetics 161:1727–1750.']
  • ['Lande, R. 1979. Quantitative genetic‐analysis of multivariate evolution, applied to brain‐body size allometry. Evolution 33:402–416.']
  • ['———. 1980. The genetic covariance between characters maintained by pleiotropic mutations. Genetics 94:203–221.']
  • ['Lynch, M., and B. Walsh. 1998. Genetics and analysis of quantitative traits. Sinauer, Sunderland, MA.']
  • ['Nei, N., and W.‐H. Li. 1973. Linkage disequilibrium in subdivided populations. Genetics 75:213–219.']
  • ['Nosil, P. 2004. Reproductive isolation caused by visual predation on migrants between divergent environments. Proceedings of the Royal Society of London B 271:1521–1528.']
  • ['Nosil, P., and B. J. Crespi. 2004. 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.']
  • ['Nosil, P., B. J. Crespi, and C. P. Sandoval. 2002. Host‐plant adaptation drives the parallel evolution of reproductive isolation. Nature 417:441–443.']
  • ['———. 2003. Reproductive isolation driven by the combined effects of ecological adaptation and reinforcement. Proceedings of the Royal Society of London B 270:1911–1918.']
  • ['———. 2005. The evolution of host preference in allopatric versus parapatric populations of Timema cristinae walking‐sticks. Journal of Evolutionary Biology (forthcoming).']
  • ['Otto, S. P. 2004. Two steps forward, one step back: the pleiotropic effects of favoured alleles. Proceedings of the Royal Society of London B 271:705–714.']
  • ['Phillips, P. C., and S. J. Arnold. 1999. Hierarchical comparison of genetic variance‐covariance matrices. I. Using the Flury hierarchy. Evolution 53:1506–1515.']
  • ['Poore, A. G. B., and P. D. Steinberg. 2001. Host‐plant adaptation in a marine amphipod: genetic potential not realized in field populations. Evolution 55:68–80.']
  • ['Roff, D. 2000. The evolution of the G matrix: selection or drift? Heredity 84:135–142.']
  • ['Sandoval, C. P. 1993. Geographic, ecological and behavioral factors affecting spatial variation in color or morph frequency in the walking‐stick Timema cristinae. PhD diss. University of California, Santa Barbara.']
  • ['———. 1994a. Differential visual predation on morphs of Timema cristinae (Phasmatodeae: Timemidae) and its consequences for host range. Biological Journal of the Linnean Society 52:341–356.']
  • ['———. 1994b. The effects of relative geographic scales of gene flow and selection on morph frequencies in the walking stick Timema cristinae. Evolution 48:1866–1879.']
  • ['Sandoval, C. P., and P. Nosil. 2005. Counteracting selective regimes and host preference evolution in ecotypes of two species of walking‐sticks. Evolution 59:2405–2413.']
  • ['Schluter, D. 1996. Adaptive radiation along genetic lines of least resistance. Evolution 50:1766–1774.']
  • ['Sinervo, B., and E. Svensson. 2002. Correlational selection and the evolution of genomic architecture. Heredity 89:329–338.']
  • ['Singer, M. C., D. Ng, and C. D. Thomas. 1988. Heritability of oviposition preference and its relationship to offspring preference within a single insect population. Evolution 42:977–985.']
  • ['Slatkin, M. 1987. Gene flow and the geographic structure of natural populations. Science 236:787–792.']
  • ['Steward, R. C. 1985. Evolution of resting behavior in polymorphic “industrial melanic” moth species. Biological Journal of the Linnean Society 24:285–293.']
  • ['Thompson, J. N. 1988. Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomologia Experimentalis et Applicata 47:3–14.']
  • ['Turelli, M. 1988. Phenotypic evolution, constant covariances, and the maintenance of additive variance. Evolution 42:1342–1347.']
  • ['Via, S. 1986. Genetic covariance between oviposition preference and larval performance in an insect herbivore. Evolution 40:778–785.']