, Volume 136, Issue 1, pp 179–187 | Cite as

Genetic architecture underlying convergent evolution of egg-laying behavior in a seed-feeding beetle

  • Charles W. Fox
  • James D. Wagner
  • Sara Cline
  • Frances Ann Thomas
  • Frank J. Messina


Independent populations subjected to similar environments often exhibit convergent evolution. An unresolved question is the frequency with which such convergence reflects parallel genetic mechanisms. We examined the convergent evolution of egg-laying behavior in the seed-feeding beetle Callosobruchus maculatus. Females avoid ovipositing on seeds bearing conspecific eggs, but the degree of host discrimination varies among geographic populations. In a previous experiment, replicate lines switched from a small host to a large one evolved reduced discrimination after 40 generations. We used line crosses to determine the genetic architecture underlying this rapid response. The most parsimonious genetic models included dominance and/or epistasis for all crosses. The genetic architecture underlying reduced discrimination in two lines was not significantly different from the architecture underlying differences between geographic populations, but the architecture underlying the divergence of a third line differed from all others. We conclude that convergence of this complex trait may in some cases involve parallel genetic mechanisms.


Callosobruchus Dominance Epistasis Host shift Hybrid Line cross Oviposition preference 



This research was supported by grants from Kentucky EPSCoR (to CWF and JDW), the University of Kentucky Agricultural Experiment Station (to CWF), and the Utah Agricultural Experiment Station (to FJM; paper no. 8010).


  1. Allison PD (1995) Survival analysis using the SAS system: a practical guide. SAS Institute, Inc., CaryGoogle Scholar
  2. Arendt J, Reznick D (2008) Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends Ecol Evol 23:26–32. doi: 10.1016/j.tree.2007.09.011 PubMedCrossRefGoogle Scholar
  3. Basford KE, De Lacy IH (1979) The use of matrix specifications in defining gene action in genotypic value models and generation mean analysis. Theor Appl Genet 55:225–229. doi: 10.1007/BF00268116 CrossRefGoogle Scholar
  4. Bieri J, Kawecki TJ (2003) Genetic architecture of differences between populations of cowpea weevil (Callosobruchus maculatus) evolved in the same environment. Evol Int J Org Evol 57:274–287Google Scholar
  5. Bradshaw WE, Holzapfel CM (2000) The evolution of genetic architecture and the divergence of natural populations. In: Wolf JB, Brodie EDI, Wade MJ (eds) Epistasis and the evolutionary process. Oxford University Press, New YorkGoogle Scholar
  6. Bult A, Lynch CB (1996) Multiple selection responses in house mice bidirectionally selected for thermoregulatory nest-building behavior: crosses of replicate lines. Behav Genet 26:439–446. doi: 10.1007/BF02359488 PubMedCrossRefGoogle Scholar
  7. Burnham KP, Anderson DA (1998) Model selection and inference. Springer Mathematics, New YorkGoogle Scholar
  8. Burnham KP, Anderson DA (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304. doi: 10.1177/0049124104268644 CrossRefGoogle Scholar
  9. Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G, Dickson M, Grimwood J, Schmutz J, Myers RM, Schluter D, Kingsley DM (2005) Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307:1928–1933. doi: 10.1126/science.1107239 PubMedCrossRefGoogle Scholar
  10. Cooper TF, Rozen DE, Lenski RE (2003) Parallel changes in qene expression after 20, 000 generations of evolution in Escherichia coli. Proc Natl Acad Sci USA 100:1072–1077. doi: 10.1073/pnas.0334340100 PubMedCrossRefGoogle Scholar
  11. Craig TP, Horner JD, Itami JK (2001) Genetics, experience, and host-plant preference in Eurosta solidaginis: implications for host shifts and speciation. Evol Int J Org Evol 55:773–782. doi: 10.1554/0014-3820(2001)055[0773:GEAHPP]2.0.CO;2 Google Scholar
  12. Credland PF (1987) Effects of host change on the fecundity and development of an unusual strain of Callosobruchus maculatus (F) (Coleoptera: Bruchidae). J Stored Prod Res 23:91–98. doi: 10.1016/0022-474X(87)90022-1 CrossRefGoogle Scholar
  13. Credland PF, Wright AW (1990) Oviposition deterrents of Callosobruchus maculatus (Coleoptera: Bruchidae). Physiol Entomol 15:285–298. doi: 10.1111/j.1365-3032.1990.tb00517.x CrossRefGoogle Scholar
  14. Forister ML, Ehmer AG, Futuyma DJ (2007) The genetic architecture of a niche: variation and covariation in host use traits in the Colorado potato beetle. J Evol Biol 20:985–996. doi: 10.1111/j.1420-9101.2007.01310.x PubMedCrossRefGoogle Scholar
  15. Fox CW, Czesak ME, Wallin WG (2004a) Complex genetic architecture of population differences in adult lifespan of a beetle: nonadditive inheritance, gender differences, body size and a large maternal effect. J Evol Biol 17:1007–1017. doi: 10.1111/j.1420-9101.2004.00752.x PubMedCrossRefGoogle Scholar
  16. Fox CW, Stillwell RC, Amarillo AR, Czesak ME, Messina FJ (2004b) Genetic architecture of population differences in oviposition behaviour of the seed beetle Callosobruchus maculatus. J Evol Biol 17:1141–1151. doi: 10.1111/j.1420-9101.2004.00719.x PubMedCrossRefGoogle Scholar
  17. Fricke C, Arnqvist G (2007) Rapid adaptation to a novel host in a seed beetle (Callosobruchus maculatus): the role of sexual selection. Evol Int J Org Evol 61:440–454. doi: 10.1111/j.1558-5646.2007.00038.x Google Scholar
  18. Fry JD (2003) Detecting ecological trade-offs using selection experiments. Ecology 84:1672–1678. doi: 10.1890/0012-9658(2003)084[1672:DETUSE]2.0.CO;2 CrossRefGoogle Scholar
  19. Gilchrist AS, Partridge L (1999) A comparison of the genetic basis of wing size divergence in three parallel body size clines of Drosophila melanogaster. Genetics 153:1775–1787PubMedGoogle Scholar
  20. Harshman LG, Hoffmann AA (2000) Laboratory selection experiments using Drosophila: what do they really tell us? Trends Ecol Evol 15:32–36. doi: 10.1016/S0169-5347(99)01756-5 PubMedCrossRefGoogle Scholar
  21. Hoekstra HE, Nachman MW (2003) Different genes underlie adaptive melanism in different populations of rock pocket mice. Mol Ecol 12:1185–1194. doi: 10.1046/j.1365-294X.2003.01788.x PubMedCrossRefGoogle Scholar
  22. Hoekstra HE, Hirschmann RJ, Bundey RA, Insel PA, Crossland JP (2006) A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313:101–104. doi: 10.1126/science.1126121 PubMedCrossRefGoogle Scholar
  23. Horng SB, Lin HC, Wu WJ, Godfray HCJ (1999) Behavioral processes and egg-laying decisions of the bean weevil, Callosobruchus maculatus. Res Popul Ecol (Kyoto) 41:283–290Google Scholar
  24. Kawecki TJ (1995) Expression of genetic and environmental variation for life-history characters on the usual and novel hosts in Callosobruchus maculatus (Coleoptera: Bruchidae). Heredity 75:70–76. doi: 10.1038/hdy.1995.105 CrossRefGoogle Scholar
  25. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241. doi: 10.1111/j.1461-0248.2004.00684.x CrossRefGoogle Scholar
  26. Kearsey MJ, Pooni HS (1996) The genetical analysis of quantitative traits. Chapman & Hall, LondonGoogle Scholar
  27. Keese MC (1996) Feeding responses of hybrids and the inheritance of host-use traits in leaf feeding beetles (Coleoptera: Chrysomelidae). Heredity 76:36–42. doi: 10.1038/hdy.1996.5 CrossRefGoogle Scholar
  28. Losos JB, Jackman TR, Larson A, de Queiroz K, Rodriguez-Schettino L (1998) Contingency and determinism in replicated adaptive radiations of island lizards. Science 279:2115–2118. doi: 10.1126/science.279.5359.2115 PubMedCrossRefGoogle Scholar
  29. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Inc, SunderlandGoogle Scholar
  30. Mackay TFC (2008) The genetic architecture of complex behaviors: lessons from Drosophila. Genetica. doi: 10.1007/s10709-008-9310-6
  31. Mackay TFC, Anholt RRH (2007) Ain’t misbehavin? Genotype-environment interactions and the genetics of behavior. Trends Genet 23:311–314. doi: 10.1016/j.tig.2007.03.013 PubMedCrossRefGoogle Scholar
  32. Mather K, Jinks JL (1982) Biometrical genetics, 3rd edn. Chapman & hall, LondonGoogle Scholar
  33. Matos M, Simoes P, Duarte A, Rego C, Avelar T, Rose MR (2004) Convergence to a novel environment: comparative method versus experimental evolution. Evol Int J Org Evol 58:1503–1510Google Scholar
  34. Meffert LM, Hicks SK, Regan JL (2002) Nonadditive genetic effects in animal behavior. Am Nat 160:S198–S213. doi: 10.1086/342896 PubMedCrossRefGoogle Scholar
  35. Messina FJ (1989) Genetic basis of variable oviposition behavior in Callosobruchus maculatus (Coleoptera: Bruchidae). Ann Entomol Soc Am 82:792–796Google Scholar
  36. Messina FJ (1991) Life history variation in a seed beetle: adult egg-laying vs larval competitive ability. Oecologia 85:447–455. doi: 10.1007/BF00320624 CrossRefGoogle Scholar
  37. Messina FJ (1993) Heritability and ‘evolvability’ of fitness components in Callosobruchus maculatus. Heredity 71:623–629. doi: 10.1038/hdy.1993.187 CrossRefGoogle Scholar
  38. Messina FJ (2004a) How labile are the egg-laying preferences of seed beetles? Ecol Entomol 29:318–326. doi: 10.1111/j.1365-2311.2004.0599.x CrossRefGoogle Scholar
  39. Messina FJ (2004b) Predictable modification of body size and competitive ability following a host shift by a seed beetle. Evol Int J Org Evol 58:2788–2797Google Scholar
  40. Messina FJ, Karren ME (2003) Adaptation to a novel host modifies host discrimination by the seed beetle Callosobruchus maculatus. Anim Behav 65:501–507. doi: 10.1006/anbe.2003.2107 CrossRefGoogle Scholar
  41. Messina FJ, Mitchell R (1989) Intraspecific variation in the egg-spacing behavior of the seed beetle Callosobruchus maculatus. J Insect Behav 2:727–742. doi: 10.1007/BF01049397 CrossRefGoogle Scholar
  42. Messina FJ, Renwick JAA (1985) Ability of ovipositing seed beetles to discriminate between seeds with differing egg loads. Ecol Entomol 10:225–230. doi: 10.1111/j.1365-2311.1985.tb00552.x CrossRefGoogle Scholar
  43. Messina FJ, Slade AF (1997) Inheritance of host-plant choice in the seed beetle Callosobruchus maculatus (Coleoptera : Bruchidae). Ann Entomol Soc Am 90:848–855Google Scholar
  44. Messina FJ, Gardner SL, Morse GE (1991) Host discrimination by egg-laying seed beetles: causes of population differences. Anim Behav 41:773–779. doi: 10.1016/S0003-3472(05)80343-4 CrossRefGoogle Scholar
  45. Mitchell R (1990) Behavioral ecology of Callosobruchus maculatus. In: Fujii K, Gatehouse AMR, Johnson CD, Mitchell R, Yoshida T (eds) Bruchids and legumes: economics, ecology, and coevolution. Kluwer, The Netherlands, pp 317–330Google Scholar
  46. Mitchell R (1991) The traits of a biotype of Callosobruchus maculatus (F) (Coleoptera: Bruchidae) from south India. J Stored Prod Res 27:221–224. doi: 10.1016/0022-474X(91)90004-V CrossRefGoogle Scholar
  47. Nufio CR, Papaj DR (2001) Host marking behavior in phytophagous insects and parasitoids. Entomol Exp Appl 99:273–293. doi: 10.1023/A:1019204817341 CrossRefGoogle Scholar
  48. Odeen A, Hastad O (2003) Complex distribution of avian color vision systems revealed by sequencing the SWS1 opsin from total DNA. Mol Biol Evol 20:855–861. doi: 10.1093/molbev/msg108 PubMedCrossRefGoogle Scholar
  49. Parr MJ, Tran BMD, Simmonds MSJ, Credland PF (1996) Oviposition behaviour of the cowpea seed beetle, Callosobruchus maculatus. Physiol Entomol 21:107–117. doi: 10.1111/j.1365-3032.1996.tb00842.x CrossRefGoogle Scholar
  50. Price T, Schluter D (1991) On the low heritability of life history traits. Evol Int J Org Evol 45:853–861. doi: 10.2307/2409693 Google Scholar
  51. Protas ME, Hersey C, Kochanek D, Zhou Y, Wilkens H, Jeffery WR, Zon LI, Borowsky R, Tabin CJ (2006) Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism. Nat Genet 38:107–111. doi: 10.1038/ng1700 PubMedCrossRefGoogle Scholar
  52. Rego C, Santos M, Matos M (2007) Quantitative genetics of speciation: additive and non-additive genetic differentiation between Drosophila madeirensis and Drosophila subobscura. Genetica 131:167–174. doi: 10.1007/s10709-006-9128-z PubMedCrossRefGoogle Scholar
  53. Smith RH, Lessells CM (1985) Oviposition, ovicide and larval competition in granivorous insects. In: Sibly R, Smith RH (eds) Behavioural ecology. Blackwell Scientific, Oxford, pp 423–448Google Scholar
  54. Stern DL, Orgogozo V (2008) The loci of evolution: how predictable is genetic evolution? Evol Int J Org Evol 62:2155–2177. doi: 10.1111/j.1558-5646.2008.00450.x Google Scholar
  55. Stillwell RC, Wallin WG, Hitchcock LJ, Fox CW (2007) Phenotypic plasticity in a complex world: interactive effects of food and temperature on fitness components of a seed beetle. Oecologia 153:309–321. doi: 10.1007/s00442-007-0748-5 PubMedCrossRefGoogle Scholar
  56. Teotónio H, Matos M, Rose MR (2004) Quantitative genetics of functional characters in Drosophila melanogaster populations subjected to laboratory selection. J Genet 83:265–277. doi: 10.1007/BF02717896 PubMedCrossRefGoogle Scholar
  57. Travisano M, Mongold JA, Bennett AF, Lenski RE (1995) Experimental tests of the roles of adaptation, chance and history in evolution. Science 267:87–90. doi: 10.1126/science.7809610 PubMedCrossRefGoogle Scholar
  58. Tucić N, Šešlija D (2007) Genetic architecture of differences in oviposition preference between ancestral and derived populations of the seed beetle Acanthoscelides obtectus. Heredity 98:268–273. doi: 10.1038/sj.hdy.6800930 PubMedCrossRefGoogle Scholar
  59. Tuda M, Iwasa Y (1998) Evolution of contest competition and its effect on host-parasitoid dynamics. Evol Ecol 12:855–870. doi: 10.1023/A:1006550817371 CrossRefGoogle Scholar
  60. Tuda M, Ronn J, Buranapanichpan S, Wasano N, Arnqvist G (2006) Evolutionary diversification of the bean beetle genus Callosobruchus (Coleoptera : Bruchidae): traits associated with stored-product pest status. Mol Ecol 15:3541–3551. doi: 10.1111/j.1365-294X.2006.03030.x PubMedCrossRefGoogle Scholar
  61. Wasserman SS, Futuyma DJ (1981) Evolution of host plant utilization in laboratory populations of the southern cowpea weevil, Callosobruchus maculatus Fabricius (Coleoptera: Bruchidae). Evol Int J Org Evol 35:605–617. doi: 10.2307/2408234 Google Scholar
  62. Wichman HA, Badgett MR, Scott LA, Boulianne CM, Bull JJ (1999) Different trajectories of parallel evolution during viral adaptation. Science 285:422–424. doi: 10.1126/science.285.5426.422 PubMedCrossRefGoogle Scholar
  63. Wood TE, Burke JM, Rieseberg LH (2005) Parallel genotypic adaptation: when evolution repeats itself. Genetica 123:157–170. doi: 10.1007/s10709-003-2738-9 PubMedCrossRefGoogle Scholar
  64. Yokoyama S, Radlwimmer FB, Blow NS (2000) Ultraviolet pigments in birds evolved from violet pigments by a single amino acid change. Proc Natl Acad Sci USA 97:7366–7371. doi: 10.1073/pnas.97.13.7366 PubMedCrossRefGoogle Scholar
  65. Zhang JZ, Kumar S (1997) Detection of convergent and parallel evolution at the amino acid sequence level. Mol Biol Evol 14:527–536PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Charles W. Fox
    • 1
  • James D. Wagner
    • 1
    • 2
  • Sara Cline
    • 1
    • 2
  • Frances Ann Thomas
    • 1
    • 2
  • Frank J. Messina
    • 3
  1. 1.Department of Entomology, S-225 Agricultural Science Center NorthUniversity of KentuckyLexingtonUSA
  2. 2.Biology ProgramTransylvania UniversityLexingtonUSA
  3. 3.Department of BiologyUtah State UniversityLoganUSA

Personalised recommendations