Asymmetric evolution of egg laying behavior following reciprocal host shifts by a seed-feeding beetle

Abstract

Colonization of new environments can lead to rapid changes in fitness-related traits. For herbivorous insects, switching to a new host plant can be comparable to invading a new habitat. Behavioral, physiological, and life-history traits commonly vary among insect populations associated with different plants, but how host shifts cause trait divergence is often unclear. We investigated whether experimental host shifts would modify a key insect trait, egg-laying behavior, in a seed beetle. Beetle populations associated long-term with either a small-seeded host (mung bean) or a large-seeded host (cowpea) were switched to each other’s host. After 36–55 generations, we assayed three aspects of oviposition behavior known to differ between the mung bean- and cowpea-adapted populations. Responses to the host shifts were asymmetrical. Females from lines transferred from mung bean to cowpea produced less uniform distributions of eggs among seeds, were more likely to add an egg to an occupied seed, and were more likely to “dump” eggs when seeds were absent. These lines thus converged toward the cowpea-adapted population. In contrast, the reciprocal host shift had no effect; oviposition behavior was unchanged in lines transferred from cowpea to mung bean. We suggest that these results reflect an asymmetry in the fitness consequences of each host shift, which in turn depended on differences in larval competitiveness in the original populations. Interactions among multiple fitness components are likely to make evolutionary responses less predictable in novel environments.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Ågren J, Schemske DW (2012) Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range. New Phytol 194(4):1112–1122. doi:10.1111/j.1469-8137.2012.04112.x

    Article  PubMed  Google Scholar 

  2. Anderson JT, Lee C-R, Rushworth CA, Colautti RI, Mitchell-Olds T (2013) Genetic trade-offs and conditional neutrality contribute to local adaptation. Mol Ecol 22(3):699–708. doi:10.1111/j.1365-294X.2012.05522.x

    Article  PubMed  Google Scholar 

  3. Anderson JT, Perera N, Chowdhury B, Mitchell-Olds T (2015) Microgeographic patterns of genetic divergence and adaptation across environmental gradients in Boechera stricta (Brassicaceae). Am Nat 186:S60–S73. doi:10.1086/682404

    Article  PubMed  PubMed Central  Google Scholar 

  4. Angert AL, Bradshaw HD Jr, Schemske DW (2008) Using experimental evolution to investigate geographic range limits in monkeyflowers. Evolution 62(10):2660–2675. doi:10.1111/j.1558-5646.2008.00471.x

    Article  PubMed  Google Scholar 

  5. Blanquart F, Kaltz O, Nuismer SL, Gandon S (2013) A practical guide to measuring local adaptation. Ecol Lett 16(9):1195–1205. doi:10.1111/ele.12150

    Article  PubMed  Google Scholar 

  6. Bohren BB, Hill WG, Robertson A (1966) Some observations on asymmetrical correlated responses to selection. Genet Res 7(1):44–57. doi:10.1017/S0016672300009460

    CAS  Article  PubMed  Google Scholar 

  7. Buckling A, Brockhurst MA, Travisano M, Rainey PB (2007) Experimental adaptation to high and low quality environments under different scales of temporal variation. J Evol Biol 20(1):296–300. doi:10.1111/j.1420-9101.2006.01195.x

    CAS  Article  PubMed  Google Scholar 

  8. Colegrave N (1994) Game theory models of competition in closed systems: asymmetries in fighting and competitive ability. Oikos 71(3):499–505. doi:10.2307/3545838

    Article  Google Scholar 

  9. Colegrave N (1997) Can a patchy population structure affect the evolution of competition strategies? Evolution. doi:10.2307/2411121

  10. Credland PF, Dick KM, Wright AW (1986) Relationships between larval density, adult size and egg production in the cowpea seed beetle, Callosobruchus maculatus. Ecol Entomol 11(1):41–50. doi:10.1111/j.1365-2311.1986.tb00278.x

    Article  Google Scholar 

  11. Czesak ME, Fox CW, Wolf JB (2006) Experimental evolution of phenotypic plasticity: how predictive are cross-environment genetic correlations? Am Nat 168(3):323–335. doi:10.1086/506919

    PubMed  Google Scholar 

  12. Dercole F, Ferrière R, Rinaldi S (2002) Ecological bistability and evolutionary reversals under asymmetrical competition. Evolution 56(6):1081–1090. doi:10.1554/0014-3820(2002)056[1081:EBAERU]2.0.CO;2

    Article  PubMed  Google Scholar 

  13. Forister ML, Dyer LA, Singer MS, Stireman JO, Lill JT (2012) Revisiting the evolution of ecological specialization, with emphasis on insect–plant interactions. Ecology 93(5):981–991. doi:10.1890/11-0650.1

    CAS  Article  PubMed  Google Scholar 

  14. Fox CW, Savalli UM (1998) Inheritance of environmental variation in body size: superparasitism of seeds affects progeny and grand progeny body size via a nongenetic maternal effect. Evolution 52(1):172–182. doi:10.2307/2410932

    Article  PubMed  Google Scholar 

  15. Fox CW, Stillwell RC, Amarillo-S AR, Czesak ME, Messina FJ (2004) Genetic architecture of population differences in oviposition behaviour of the seed beetle Callosobruchus maculatus. J Evol Biol 17(5):1141–1151. doi:10.1111/j.1420-9101.2004.00719.x

    CAS  Article  PubMed  Google Scholar 

  16. Fox CW, Bush ML, Messina FJ (2010) Biotypes of the seed beetle Callosobruchus maculatus have differing effects on the germination and growth of their legume hosts. Agric For Entomol 12(4):353–362. doi:10.1111/j.1461-9563.2010.00484.x

    Article  Google Scholar 

  17. Fry JD (2003) Detecting ecological trade-offs using selection experiments. Ecology 84(7):1672–1678. doi:10.1890/0012-9658(2003)084[1672:DETUSE]2.0.CO;2

    Article  Google Scholar 

  18. Futuyma DJ, Bennett AF (2009) The importance of experimental studies in evolutionary biology. In: Garland Jr T, Rose MR (eds) Experimental evolution: concepts, methods, and applications of selection experiments. University of California Press, Berkeley, pp 15–30. www.jstor.org/stable/10.1525/j.ctt1ppqbc

  19. Garland T, Rose MR (2009) Experimental evolution. University of California Press. www.jstor.org/stable/10.1525/j.ctt1ppqbc

  20. Gompert Z, Messina FJ (2016) Genomic evidence that resource-based trade-offs limit host-range expansion in a seed beetle. Evolution 70:1249–1264. doi:10.1111/evo.12933

    CAS  Article  PubMed  Google Scholar 

  21. Gunathilake KGT, Wansapala MAJ, Herath MWH (2016) Comparison of nutritional and functional properties of mung bean (Vigna radiata) and cowpea (Vigna unguiculata) protein isolates processed by isoelectric precipitation. Int J Innov Res Technol 3:139–148

    Google Scholar 

  22. Haga EB, Rossi MN (2016) The effect of seed traits on geographic variation in body size and sexual size dimorphism of the seed-feeding beetle Acanthoscelides macrophthalmus. Ecol Evol 6(19):6892–6905. doi:10.1002/ece3.2364

    Article  PubMed  PubMed Central  Google Scholar 

  23. Horng SB (1997) Larval competition and egg-laying decisions by the bean weevil, Callosobruchus maculatus. Anim Behav 53(1):1–12. doi:10.1006/anbe.1996.9999

    Article  Google Scholar 

  24. Hughes AR, Hanley TC, Byers JE, Grabowski JH, Malek JC, Piehler MF, Kimbro DL (2017) Genetic by environmental variation but no local adaptation in oysters (Crassostrea virginica). Ecol Evol 7:697–709. doi:10.1002/ece3.2614

    Article  PubMed  Google Scholar 

  25. Jasmin JN, Kassen R (2007) On the experimental evolution of specialization and diversity in heterogeneous environments. Ecol Lett 10(4):272–281. doi:10.1111/j.1461-0248.2007.01021.x

    Article  PubMed  Google Scholar 

  26. Joshi J, Schmid B, Caldeira MC, Dimitrakopoulos PG, Good J, Harris R, Hector A, Huss-Danell K, Jumpponen A, Minns A, Mulder CPH, Pereira JS, Prinz A, Scherer-Lorenzen M, Siamantziouras A-SD, Terry AC, Troumbis AY, Lawton JH (2001) Local adaptation enhances performance of common plant species. Ecol Lett 4:536–544. doi:10.1046/j.1461-0248.2001.00262.x

    Article  Google Scholar 

  27. Kassen R (2002) The experimental evolution of specialists, generalists, and the maintenance of diversity. J Evol Biol 15(2):173–190. doi:10.1046/j.1420-9101.2002.00377.x

    Article  Google Scholar 

  28. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7(12):1225–1241. doi:10.1111/j.1461-0248.2004.00684.x

    Article  Google Scholar 

  29. Kawecki TJ, Lenski RE, Ebert D, Hollis B, Olivieri I, Whitlock MC (2012) Experimental evolution. Trends Ecol Evol 27(10):547–560. doi:10.1016/j.tree.2012.06.001

    Article  PubMed  Google Scholar 

  30. Klappert K, Reinhold K (2005) Local adaptation and sexual selection: a reciprocal transfer experiment with the grasshopper Chorthippus biguttulus. Behav Ecol Sociobiol 58(1):36–43. doi:10.1007/s00265-004-0902-6

    Article  Google Scholar 

  31. Lee MC, Chou HH, Marx CJ (2009) Asymmetric, bimodal trade-offs during adaptation of methylobacterium to distinct growth substrates. Evolution 63(11):2816–2830. doi:10.1111/j.1558-5646.2009.00757.x

    CAS  Article  PubMed  Google Scholar 

  32. Mano H, Toquenaga Y (2008) Wall-making behavior as a proximate mechanism to generate variation in larval competition in Callosobruchus maculatus (Coleoptera: Bruchidae). Evol Ecol 22(2):177–191. doi:10.1007/s10682-007-9167-7

    Article  Google Scholar 

  33. Marinosci C, Magalhaes S, Macke E, Navajas M, Carbonell D, Devaux C, Olivieri I (2015) Effects of host plant on life-history traits in the polyphagous spider mite Tetranychus urticae. Ecol Evol 5(15):3151–3158. doi:10.1002/ece3.1554

    Article  PubMed  PubMed Central  Google Scholar 

  34. Martin G, Lenormand T (2015) The fitness effect of mutations across environments: Fisher’s geometrical model with multiple optima. Evolution 69(6):1433–1447. doi:10.1111/evo.12671

    Article  PubMed  Google Scholar 

  35. Messina FJ (1991) Life-history variation in a seed beetle: adult egg-laying vs. larval competitive ability. Oecologia 85(3):447–455. doi:10.1007/BF00320624

    Article  PubMed  Google Scholar 

  36. Messina FJ (1993) Heritability and ‘evolvability’ of fitness components in Callosobruchus maculatus. Heredity 71(6):623–629. doi:10.1038/hdy.1993.187

    Article  Google Scholar 

  37. Messina FJ (2004) Predictable modification of body size and competitive ability following a host shift by a seed beetle. Evolution 58(12):2788–2797. doi:10.1554/04-372

    Article  PubMed  Google Scholar 

  38. Messina FJ, Fox CW (2011) Egg-dumping behavior is not correlated with wider host acceptance in the seed beetle Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae). Ann Entomol Soc Am 104(4):850–856. doi:10.1603/AN11040

    Article  Google Scholar 

  39. Messina FJ, Gompert Z (2017) Evolution of host acceptance and its reversibility in a seed beetle. Ecol Entomol 42(1):42–50. doi:10.1111/een.12352

    Article  Google Scholar 

  40. Messina FJ, Karren ME (2003) Adaptation to a novel host modifies host discrimination by the seed beetle Callosobruchus maculatus. Anim Behav 65(3):501–507. doi:10.1006/anbe.2003.2107

    Article  Google Scholar 

  41. Messina FJ, Mitchell R (1989) Intraspecific variation in the egg-spacing behavior of the seed beetle Callosobruchus maculatus. J Insect Behav 2(6):727–742. doi:10.1007/BF01049397

    Article  Google Scholar 

  42. Messina FJ, Gardner SL, Morse GE (1991) Host discrimination by egg-laying seed beetles: causes of population differences. Anim Behav 41(5):773–779. doi:10.1016/S0003-3472(05)80343-4

    Article  Google Scholar 

  43. Messina FJ, Morrey JL, Mendenhall M (2007) Why do host-deprived seed beetles ‘dump’ their eggs? Physiol Entomol 32(3):259–267. doi:10.1111/j.1365-3032.2007.00579.x

    Article  Google Scholar 

  44. Mitchell R (1991) The traits of a biotype of Callosobruchus maculatus (F.) (Coleoptera: Bruchidae) from South India. J Stored Prod Res 27(4):221–224. doi:10.1016/0022-474X(91)90004-V

    Article  Google Scholar 

  45. Mopper S, Beck M, Simberloff D, Stiling P (1995) Local adaptation and agents of selection in a mobile insect. Evolution 49(5):810–815. doi:10.2307/2410404

    Article  PubMed  Google Scholar 

  46. Proffit M, Khallaf MA, Carrasco D, Larsson MC, Anderson P (2015) ‘Do you remember the first time?’ Host plant preference in a moth is modulated by experiences during larval feeding and adult mating. Ecol Lett 18(4):365–374. doi:10.1111/ele.12419

    Article  PubMed  Google Scholar 

  47. Remold S (2012) Understanding specialism when the jack of all trades can be the master of all. Proc R Soc Lond B Biol Sci 279:4861–4869. doi:10.1098/rspb.2012.1990

    Article  Google Scholar 

  48. Richardson JL, Urban MC, Bolnick DI, Skelly DK (2014) Microgeographic adaptation and the spatial scale of evolution. Trends Ecol Evol 29(3):165–176. doi:10.1016/j.tree.2014.01.002

    Article  PubMed  Google Scholar 

  49. Savković U, ĐorĐević M, Šešlija Jovanović D, Lazarević J, Tucić N, Stojković B (2016) Experimentally induced host-shift changes life-history strategy in a seed beetle. J Evol Biol 29:837–847. doi:10.1111/jeb.12831

    Article  PubMed  Google Scholar 

  50. Smith RH, Lessells CM (1985) Oviposition, ovicide and larval competition in granivorous insects. In: Sibly RM, Smith RH (eds) Behavioural ecology: ecological consequences of adaptative behaviour. Blackwell Science, London, pp 423–448

    Google Scholar 

  51. 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(2):309–321. doi:10.1007/s00442-007-0748-5

    Article  PubMed  Google Scholar 

  52. Toquenaga Y, Ichinose M, Hoshino T, Fujii K (1994) Contest and scramble competitions in an artificial world: genetic analysis with genetic algorithms. In: Langdon CG (ed) Artificial life III. Addison-Wesley, Reading, pp 177–199

    Google Scholar 

  53. Travisano M (1997) Long-term experimental evolution in Escherichia coli. VI. Environmental constraints on adaptation and divergence. Genetics 146(2):471–479

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Tuda M, Iwasa Y (1998) Evolution of contest competition and its effect on host–parasitoid dynamics. Evol Ecol 12(7):855–870. doi:10.1023/A:1006550817371

    Article  Google Scholar 

  55. Tuda M, Kagoshima K, Toquenaga Y, Arnqvist G (2014) Global genetic differentiation in a cosmopolitan pest of stored beans: effects of geography, host-plant usage and anthropogenic factors. PLoS ONE 9(9):e106268. doi:10.1371/journal.pone.0106268

    Article  PubMed  PubMed Central  Google Scholar 

  56. Via S, Bouck AC, Skillman S (2000) Reproductive isolation between divergent races of pea aphids on two hosts. II. Selection against migrants and hybrids in the parental environments. Evolution 54(5):1626–1637. doi:10.1554/0014-3820(2000)054[1626:RIBDRO]2.0.CO;2

    CAS  Article  PubMed  Google Scholar 

  57. Wenger JW, Piotrowski J, Nagarajan S, Chiotti K, Sherlock G, Rosenzweig F (2011) Hunger artists: yeast adapted to carbon limitation show trade-offs under carbon sufficiency. PLoS Genet 7(8):e1002202. doi:10.1371/journal.pgen.1002202

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  58. Worley AC, Barrett SC (2000) Evolution of floral display in Eichhornia paniculata (Pontederiaceae): direct and correlated responses to selection on flower size and number. Evolution 54(5):1533–1545. doi:10.1554/0014-3820(2000)054[1533:EOFDIE]2.0.CO;2

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Bill Wallin, Elliot Campbell, Fariba Kanga, Anna Muncy and Daniel Sullivan for help running experiments. Jacqueline Dillard, Melise Lecheta, Allyssa Kilanowski, Josiah Ritchey, and Boris Sauterey provided comments on an earlier version of this manuscript. Rachel Zitomer participated in this project as part of a 10-week NSF-funded Research Experience for Undergraduates summer program at the University of Kentucky (summer 2013; NSF DBI-1062890). This work was funded in part by the Kentucky Agricultural Experiment Station and the Utah Agricultural Experiment Station (paper no. 8985).

Author’s contribution

CWF managed the selection experiment, quantified egg dispersion at 36 generations, and analyzed the data. RZ quantified egg dispersion (two experiments) at 50 generations and commented on the manuscript. JBD quantified egg dumping and commented on the manuscript. CWF and FJM co-wrote the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Charles W. Fox.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Fox, C.W., Zitomer, R., Deas, J.B. et al. Asymmetric evolution of egg laying behavior following reciprocal host shifts by a seed-feeding beetle. Evol Ecol 31, 753–767 (2017). https://doi.org/10.1007/s10682-017-9910-7

Download citation

Keywords

  • Callosobruchus maculatus
  • Egg dispersion
  • Experimental evolution
  • Oviposition behavior
  • Seed size