Skip to main content
Log in

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

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Allison PD (1995) Survival analysis using the SAS system: a practical guide. SAS Institute, Inc., Cary

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 57:274–287

    Google Scholar 

  • 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 York

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Burnham KP, Anderson DA (1998) Model selection and inference. Springer Mathematics, New York

    Google Scholar 

  • Burnham KP, Anderson DA (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304. doi:10.1177/0049124104268644

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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

    Article  Google Scholar 

  • 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 153:1775–1787

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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) 41:283–290

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241. doi:10.1111/j.1461-0248.2004.00684.x

    Article  Google Scholar 

  • Kearsey MJ, Pooni HS (1996) The genetical analysis of quantitative traits. Chapman & Hall, London

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Inc, Sunderland

    Google Scholar 

  • Mackay TFC (2008) The genetic architecture of complex behaviors: lessons from Drosophila. Genetica. doi:10.1007/s10709-008-9310-6

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Mather K, Jinks JL (1982) Biometrical genetics, 3rd edn. Chapman & hall, London

    Google Scholar 

  • 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 58:1503–1510

    Google Scholar 

  • Meffert LM, Hicks SK, Regan JL (2002) Nonadditive genetic effects in animal behavior. Am Nat 160:S198–S213. doi:10.1086/342896

    Article  PubMed  Google Scholar 

  • Messina FJ (1989) Genetic basis of variable oviposition behavior in Callosobruchus maculatus (Coleoptera: Bruchidae). Ann Entomol Soc Am 82:792–796

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Messina FJ (1993) Heritability and ‘evolvability’ of fitness components in Callosobruchus maculatus. Heredity 71:623–629. doi:10.1038/hdy.1993.187

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Messina FJ (2004b) Predictable modification of body size and competitive ability following a host shift by a seed beetle. Evol Int J Org Evol 58:2788–2797

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Messina FJ, Slade AF (1997) Inheritance of host-plant choice in the seed beetle Callosobruchus maculatus (Coleoptera : Bruchidae). Ann Entomol Soc Am 90:848–855

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 317–330

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Nufio CR, Papaj DR (2001) Host marking behavior in phytophagous insects and parasitoids. Entomol Exp Appl 99:273–293. doi:10.1023/A:1019204817341

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 423–448

    Google Scholar 

  • 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 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zhang JZ, Kumar S (1997) Detection of convergent and parallel evolution at the amino acid sequence level. Mol Biol Evol 14:527–536

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Charles W. Fox.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fox, C.W., Wagner, J.D., Cline, S. et al. Genetic architecture underlying convergent evolution of egg-laying behavior in a seed-feeding beetle. Genetica 136, 179–187 (2009). https://doi.org/10.1007/s10709-008-9334-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-008-9334-y

Keywords