Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-28T02:52:10.079Z Has data issue: false hasContentIssue false
  • English
  • Français

Mode of inheritance of increased host acceptance in a seed beetle

Published online by Cambridge University Press:  24 February 2012

F.J. Messina  and
N.M. Peña
F.J. Messina*
Affiliation:
Department of Biology, Utah State University, Logan, Utah 84322-5305, USA
N.M. Peña
Affiliation:
Department of Biology, Utah State University, Logan, Utah 84322-5305, USA
*
*Author for correspondence Fax: + 1 435 797 1575 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Colonization of a novel plant by herbivorous insects is frequently accompanied by genetic changes that progressively improve larval or adult performance on the new host. This study examined the genetic basis of adaptation to a marginal host (lentil) by the seed beetle Callosobruchus maculatus (F.). Quasi-natural selection in the laboratory rapidly increased the tendency to oviposit on lentil. The mode of inheritance of this increase in host acceptance was determined from crosses between three lentil-adapted lines and a line maintained on the ancestral host, mung bean. In each set of crosses, females from the lentil lines laid two to three times more eggs on lentil than did females from the mung-bean line. Hybrid females consistently displayed an intermediate level of host acceptance, which did not differ between reciprocal crosses. Alleles promoting greater oviposition on lentil thus were inherited additively, with no evidence of sex-linkage or cytoplasmic effects. In a time-course study, hybrid females initially resembled the parent from the mung-bean line, as few eggs were laid on lentil during the first 24 h. However, oviposition rates on lentil after 72 h were closer to the rate observed in the lentil-line parent. Inferences about additivity vs. dominance in genes affecting oviposition may, therefore, depend on experimental protocol. Comparison with earlier work suggests that inheritance patterns observed in crosses between recently derived selection lines (as in this study) may differ from those obtained in crosses between long-divergent geographic populations.

Keywords

Callosobruchusadaptationlentilline crossesovipositionselection experiment
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 102 , Issue 5 , October 2012 , pp. 497 - 503
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agosta, S.J. (2006) On ecological fitting, plant-insect associations, herbivore host shifts, and host plant selection. Oikos 114, 556–565.CrossRefGoogle Scholar
Agrawal, A.A. (2000) Host range evolution: adaptation of mites and trade-offs on alternate hosts. Ecology 81, 500–508.CrossRefGoogle Scholar
Berenbaum, M.R. & Feeny, P.P. (2008) Chemical mediation of host-plant specialization: the papilionid paradigm. pp. 3–19in Tilmon, K.J. (Ed.) Specialization, Speciation, and Radiation: The Evolutionary Biology of Herbivorous Insects. Berkeley, CA, USA, University of California Press.Google Scholar
Bieri, J. & Kawecki, T.J. (2003) Genetic architecture of differences between populations of cowpea weevil (Callosobruchus maculatus) evolved in the same environment. Evolution 57, 274–287.Google ScholarPubMed
Burke, M.K., Dunham, J.P., Shahrestani, P., Thornton, K.R., Rose, M.R. & Long, A.D. (2010) Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature 467, 587–592.CrossRefGoogle ScholarPubMed
Chi, Y.H., Salzman, R.A., Balfe, S., Ahn, J.E., Sun, W., Moon, J., Yun, D.J., Lee, S.Y., Higgins, T.J., Pittendrigh, B., Murdock, L.L. & Zhu-Salzman, K. (2009) Cowpea bruchid midgut transcriptome response to a soybean cystatin – costs and benefits of counter-defense. Insect Molecular Biology 18, 97–110.CrossRefGoogle Scholar
Chiu, Y. & Messina, F.J. (1994) Effect of experience on host preference in Callosobruchus maculatus (Coleoptera: Bruchidae): variability among populations. Journal of Insect Behavior 7, 503–515.CrossRefGoogle Scholar
Choi, H.-K., Mun, J.-H., Kim, D.-J., Zhu, H., Baek, J.-M., Mudge, J., Roe, B., Ellis, N., Doyle, J., Kiss, G.B., Young, N.D. & Cook, D.R. (2004) Estimating genome conservation between crop and model legume species. Proceedings of the National Academy of Sciences USA 101, 15289–15294.CrossRefGoogle ScholarPubMed
Coyne, J.A. & Orr, H.A. (2004) Speciation. Sunderland, MA, USA, Sinauer Press.Google Scholar
Craig, T.P. & Itami, J.K. (2011) Divergence of Eurosta solidaginis in response to host plant variation and natural enemies. Evolution 65, 802–817.CrossRefGoogle ScholarPubMed
Credland, P.F. (1987) Effects of host change on the fecundity and development of an unusual strain of Callosobruchus maculatus (F.) (Coleoptera: Bruchidae). Journal of Stored Products Research 23, 91–98.CrossRefGoogle Scholar
Credland, P.F. (1990) Biotype variation and host change in bruchids: causes and effects in the evolution of bruchid pests. pp. 271–287in Fujii, K., Gatehouse, A.M.R., Johnson, C.D., Mitchell, R. & Yoshida, Y. (Eds) Bruchids and Legumes: Economics, Ecology, and Coevolution. Dordrecht, The Netherlands, Kluwer Academic Publishers.CrossRefGoogle Scholar
Downey, M.H. & Nice, C.C. (2011) Experimental evidence of host race formation in Mitoura butterflies (Lepidoptera: Lycaenidae). Oikos 120, 1165–1174.CrossRefGoogle Scholar
Downie, D.A. (2010) Baubles, bangles, and biotypes: a critical review of the use and abuse of the biotype concept. Journal of Insect Science 10, 176.CrossRefGoogle ScholarPubMed
Drès, M. & Mallet, J. (2002) Host races in plant-feeding insects and their importance in sympatric speciation. Philosophical Transactions of the Royal Society London, Series B 357, 471–492.CrossRefGoogle ScholarPubMed
Dworkin, I. & Jones, C.D. (2009) Genetic changes accompanying the evolution of host specialization in Drosophila sechellia. Genetics 181, 721–736.CrossRefGoogle ScholarPubMed
Feder, J.L. & Forbes, A.A. (2008) Host fruit-odor discrimination and sympatric host-race formation. pp. 101–116in Tilmon, K.J. (Ed.) Specialization, Speciation, and Radiation: The Evolutionary Biology of Herbivorous Insects. Berkeley, CA, USA, University of California Press.Google Scholar
Fordyce, J.A. (2010) Host shifts and evolutionary radiations of butterflies. Proceedings of the Royal Society London, Series B 277, 3735–3743.Google ScholarPubMed
Forister, M.L., Ehmer, A. & Futuyma, D.J. (2007) The genetic architecture of a niche: variation and covariation in host use traits in the Colorado potato beetle. Journal of Evolutionary Biology 20, 985–996.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Fox, C.W., Stillwell, R.C., Amarillo-S, A.R., Czesak, M.E. & Messina, F.J. (2004) Genetic architecture of population differences in oviposition behaviour of the seed beetle Callosobruchus maculatus. Journal of Evolutionary Biology 17, 1141–1151.CrossRefGoogle ScholarPubMed
Fox, C.W., Wagner, J.D., Cline, S., Thomas, F.A. & Messina, F.J. (2009) Genetic architecture underlying convergent evolution of egg-laying behavior in a seed-feeding beetle. Genetica 136, 179–187.CrossRefGoogle Scholar
Fricke, C. & Arnqvist, G. (2007) Rapid adaptation to a novel host in a seed beetle (Callosobruchus maculatus): the role of sexual selection. Evolution 61, 440–454.CrossRefGoogle Scholar
Fry, J.D. (2003) Detecting ecological trade-offs using selection experiments. Ecology 84, 1672–1678.CrossRefGoogle Scholar
Futuyma, D.J. (2008) Sympatric speciation: norm or exception? pp. 136–148in Tilmon, K.J. (Ed.) Specialization, Speciation, and Radiation: The Evolutionary Biology of Herbivorous Insects. Berkeley, CA, USA, University of California Press.Google Scholar
Garcia-Robledo, C. & Horvitz, C.C. (2011) Experimental demography and the vital rates of generalist and specialist insect herbivores on native and novel host plants. Journal of Animal Ecology 80, 976–989.CrossRefGoogle ScholarPubMed
Garland, T. Jr & Rose, M.R. (2009) Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments. Berkeley, CA, USA, University of California Press.CrossRefGoogle Scholar
Graves, S.D. & Shapiro, A.M. (2003) Exotics as host plants of the California butterfly fauna. Biological Conservation 110, 413–433.CrossRefGoogle Scholar
Henniges-Janssen, K., Schöfk, G., Reineke, A., Heckel, D.G. & Groot, A.T. (2010) Oviposition of diamondback moth in the presence and absence of a novel host plant. Bulletin of Entomological Research 101, 99–105.CrossRefGoogle ScholarPubMed
Janz, N. (1998) Sex-linked inheritance of host-plant specialization in a polyphagous butterfly. Proceedings of the Royal Society London, Series B 265, 1675–1678.CrossRefGoogle Scholar
Janz, N., Nylin, S. & Wahlberg, N. (2006) Diversity begets diversity: host expansions and the diversification of plant-feeding insects. BMC Evolutionary Biology 6, 4.CrossRefGoogle ScholarPubMed
Keese, M.C. (1996) Feeding responses of hybrids and the inheritance of host-use traits in leaf feeding beetles (Coleoptera: Chrysomelidae). Heredity 76, 36–42.CrossRefGoogle Scholar
Lushai, G., Markovitch, O. & Loxdale, H.D. (2002) Host-based genotype variation in insects revisited. Bulletin of Entomological Research 92, 159–164.CrossRefGoogle ScholarPubMed
Magalhães, S., Fayard, J., Janssen, A., Carbonell, D. & Olivieri, I. (2007) Adaptation in a spider mite population after long-term evolution on a single host plant. Journal of Evolutionary Biology 20, 2016–2027.CrossRefGoogle Scholar
Martel, V. & Boivin, G. (2011) Do choice tests really test choice? Journal of Insect Behavior 24, 329–336.CrossRefGoogle Scholar
Matsubayashi, K.W., Ohshima, I. & Nosil, P. (2010) Ecological speciation in phytophagous insects. Entomologia Experimentalis et Applicata 134, 1–27.CrossRefGoogle Scholar
Matzkin, L.M., Watts, T.D., Bitler, B.G., Machado, C.A. & Markow, T.A. (2006) Functional genomics of cactus host shifts in Drosophila mojavensis. Molecular Ecology 15, 4635–4643.CrossRefGoogle ScholarPubMed
Messina, F.J. (1991) Life history variation in a seed beetle: adult egg-laying vs. larval competitive ability. Oecologia 85, 447–455.CrossRefGoogle Scholar
Messina, F.J. (2004a) Predictable modification of body size and competitive ability following a host shift by a seed beetle. Evolution 58, 2788–2797.Google ScholarPubMed
Messina, F.J. (2004b) How labile are the egg-laying preferences of seed beetles? Ecological Entomology 29, 318–326.CrossRefGoogle Scholar
Messina, F.J. & Jones, J.C. (2009) Does rapid adaptation to a poor-quality host by Callosobruchus maculatus (F.) cause cross-adaptation to other legume hosts? Journal of Stored Products Research 45, 215–219.CrossRefGoogle Scholar
Messina, F.J. & Jones, J.C. (2011) Inheritance of traits mediating a major host shift by a seed beetle, Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae). Annals of the Entomological Society of America 104, 808–815.CrossRefGoogle Scholar
Messina, F.J. & Slade, A.F. (1997) Inheritance of host-plant choice in the seed beetle Callosobruchus maculatus (Coleoptera: Bruchidae). Annals of the Entomological Society of America 90, 848–855.CrossRefGoogle Scholar
Messina, F.J., Mendenhall, M. & Jones, J.C. (2009a) An experimentally induced host shift in a seed beetle. Entomologia Experimentalis et Applicata 132, 39–49.CrossRefGoogle Scholar
Messina, F.J., Jones, J.C., Mendenhall, M. & Muller, A. (2009b) Genetic modification of host acceptance by a seed beetle, Callosobruchus maculatus (Coleoptera: Bruchidae). Annals of the Entomological Society of America 102, 181–188.CrossRefGoogle Scholar
Michel, A.P., Sim, S., Powell, T.H.Q., Taylor, M.S., Nosil, P. & Feder, J.L. (2010) Widespread genomic divergence during sympatric speciation. Proceedings of the National Academy of Sciences USA 107, 9724–9729.CrossRefGoogle ScholarPubMed
Midamegbe, A., Vitalis, R., Malausa, T., Delava, E., Cros-Arteil, S. & Streiff, R. (2011) Scanning the European corn borer (Ostrinia spp.) genome for adaptive divergence between host-affiliated sibling species. Molecular Ecology 20, 1414–1430.CrossRefGoogle ScholarPubMed
Mitchell, R. (1991) The traits of a biotype of Callosobruchus maculatus (F.) (Coleoptera: Bruchidae) from South India. Journal of Stored Products Research 27, 221–224.CrossRefGoogle Scholar
Olivieri, I., Singer, M.C., Magalhães, S., Courtiol, A., Dubois, Y., Carbonell, D., Justy, F., Beldade, P., Parmesan, C. & Michalakis, Y. (2008) Genetic, ecological, behavioral and geographic differentiation of populations in a thistle weevil: implications for speciation and biocontrol. Evolutionary Applications 1, 112–128.CrossRefGoogle Scholar
Rova, E. & Björklund, M. (2011) Can preference for oviposition sites initiate reproductive isolation in Callosobruchus maculatus? PLoS One 6, e14628.CrossRefGoogle ScholarPubMed
Scriber, J.M. (2010) Integrating ancient patterns and current dynamics of insect-plant interactions: taxonomic and geographic variation in herbivore specialization. Insect Science 17, 471–507.CrossRefGoogle Scholar
Sheck, A.L. & Gould, F. (1995) Genetic analysis of differences in oviposition preferences in Heliothis virescens and H. subflexa (Lepidoptera: Noctuidae). Environmental Entomology 24, 341–347.CrossRefGoogle Scholar
Singer, M.C., Wee, B., Hawkins, S. & Butcher, M. (2008) Rapid natural and anthropogenic diet evolution: three examples from checkerspot butterflies, pp. 311–324in Tilmon, K.J. (Ed.) Specialization, Speciation, and Radiation: The Evolutionary Biology of Herbivorous Insects. Berkeley, CA, USA, University of California Press.Google Scholar
Stapley, J., Reger, J., Feulner, P.G.D., Smadja, C., Galindo, J., Ekblom, R., Bennison, C., Ball, A.D., Beckerman, A.P. & Slate, J. (2010) Adaptation genomics: the next generation. Trends in Ecology and Evolution 25, 705–712.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Van Asch, M., Julkunen-Tiito, R. & Visser, M.E. (2010) Maternal effects in an insect herbivore as a mechanism to adapt to host plant phenology. Functional Ecology 24, 1103–1109.CrossRefGoogle Scholar
Wasserman, S.S. (1986) Genetic variation in the adaptation to foodplants among populations of the southern cowpea weevil, Callosobruchus maculatus: evolution of oviposition preference. Entomologia Experimentalis et Applicata 42, 201–212.CrossRefGoogle Scholar
Wasserman, S.S. & Futuyma, D.J. (1981) Evolution of host plant utilization in laboratory populations of the southern cowpea weevil, Callosobruchus maculatus F. (Coleoptera: Bruchidae). Evolution 35, 605–617.CrossRefGoogle Scholar
Wilkinson, L., Blank, G. & Gruber, C. (1996) Desktop Data Analysis with SYSTAT. Upper Saddle River, NJ, USA, Prentice Hall Publishers.Google Scholar
Xue, H.-J., Magalhães, S., Li, W.-L. & Yang, X.-K. (2009) Reproductive barriers between two sympatric beetle species specialized on different host plants. Journal of Evolutionary Biology 22, 2258–2266.CrossRefGoogle ScholarPubMed