Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-22T18:33:30.788Z Has data issue: false hasContentIssue false

Differences in oviposition behaviour of two sympatric sibling species of the genus Ostrinia

Published online by Cambridge University Press:  07 February 2008

T. Malausa*
Affiliation:
Laboratoire Dynamique de la Biodiversité, Université P. Sabatier – Toulouse III, UMR CNRS 5172, 31 062 Toulouse Cedex 09, France Centre de Biologie et de Gestion des Populations (CBGP), UMR INRA-IRD-SupAgro-CIRAD, Institut National de la Recherche Agronomique, Campus International de Baillarguet, 34 988 Montferrier/Lez, France
B. Pélissié
Affiliation:
Laboratoire Dynamique de la Biodiversité, Université P. Sabatier – Toulouse III, UMR CNRS 5172, 31 062 Toulouse Cedex 09, France
V. Piveteau
Affiliation:
Laboratoire Dynamique de la Biodiversité, Université P. Sabatier – Toulouse III, UMR CNRS 5172, 31 062 Toulouse Cedex 09, France
C. Pélissier
Affiliation:
Laboratoire Dynamique de la Biodiversité, Université P. Sabatier – Toulouse III, UMR CNRS 5172, 31 062 Toulouse Cedex 09, France
D. Bourguet
Affiliation:
Centre de Biologie et de Gestion des Populations (CBGP), UMR INRA-IRD-SupAgro-CIRAD, Institut National de la Recherche Agronomique, Campus International de Baillarguet, 34 988 Montferrier/Lez, France
S. Ponsard
Affiliation:
Laboratoire Dynamique de la Biodiversité, Université P. Sabatier – Toulouse III, UMR CNRS 5172, 31 062 Toulouse Cedex 09, France
*
*Author for correspondence: Fax: +33 492 386 401 E-mail: [email protected]

Abstract

Changes in host preferences are thought to be a major source of genetic divergence between phytophagous insect taxa. In western Europe, two sympatric taxa, O. nubilalis (the European corn borer) and O. scapulalis, feed mainly on maize and hop or mugwort, respectively. These two species may have diverged without geographic isolation after a host shift of ancestral populations onto maize or another cultivated species (e.g. sorghum). A previous study using inbred laboratory strains revealed that the two species differ in their oviposition choices in maize-mugwort tests. We sampled four natural populations in France (two of each taxon) and tested their oviposition behaviour toward four of their main host plant species: maize, sorghum, mugwort and hop. O. nubilalis females showed a very high preference for laying their eggmasses on maize, whereas O. scapulalis females displayed a more balanced range of preferences. O. nubilalis females were attracted slightly to sorghum, suggesting that this plant is an accidental, rather than a regular and ancestral host plant of O. nubilalis. One important result arising from this study is the significant proportion of eggs laid by both Ostrinia species on hop. This may explain why some stands of hop are sometimes not only infested by O. scapulalis but also by O. nubilalis larvae, a situation preventing assortative mating based on microallopatry. Hence, further studies must be conducted to see whether the host preference in the genus Ostrinia might be linked to assortative mating by a mechanism that is not mediated by the host plant.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2008

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

Abramoff, M., Magelhaes, P. & Ram, S. (2004) Image Processing with ImageJ. Biophotonics International 11, 3642.Google Scholar
Agresti, A. & Coull, B.A. (1998) Approximate is better than ‘exact’ for interval estimation of binomial proportions. American Statistician 52, 119126.Google Scholar
Atkins, R.E., Guthrie, W.D., Ross, W.M. & Kindler, S.D. (1983) Investigations of host-plant resistance to the European corn borer in sorghum. Iowa State Journal of Research 57, 275292.Google Scholar
Berlocher, S. & Feder, J. (2002) Sympatric speciation in phytophagous insects: moving beyond controversy? Annual Review of Entomology 47, 773815.CrossRefGoogle ScholarPubMed
Bethenod, M.-T., Thomas, Y., Rousset, F., Frérot, B., Pélozuelo, L., Genestier, G. & Bourguet, D. (2005) Genetic isolation between two sympatric host plant races of the European corn borer, Ostrinia nubilalis Hübner. II. Assortative mating and host plant preferences for oviposition. Heredity 94, 264270.CrossRefGoogle ScholarPubMed
Binder, B., Robbins, J. & Wilson, R. (1995) Chemically mediated ovipositional behaviors of the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae). Journal of Chemical Ecology 21, 13151327.CrossRefGoogle Scholar
Bontemps, A., Bourguet, D., Pélozuelo, L., Bethenod, M.-T. & Ponsard, S. (2004) Managing the evolution of Bacillus thuringiensis resistance in natural populations of the European corn borer, Ostrinia nubilalis: host plant, host race and pherotype of adult males at aggregation sites. Proceedings of the Royal Society of London Series B 271, 21792185.CrossRefGoogle ScholarPubMed
Bourguet, D., Bethenod, M.-T., Trouvé, C. & Viard, F. (2000) Host-plant diversity of the European corn borer Ostrinia nubilalis: what value for sustainable transgenic insecticidal Bt maize? Proceedings of the Royal Society of London Series B 267, 11771184.CrossRefGoogle ScholarPubMed
Bovey, P. & Maksymov, J. (1959) Le problème des races biologiques chez la Tordeuse grise du Mélèze Zeiraphera griseana (Hb.). Vierteljahresschrift der Naturforschenden Gesellschaft in Zürich 104, 264274.Google Scholar
Bush, G. (1975) Modes of animal speciation. Annual Review of Ecology and Systematics 6, 339364.CrossRefGoogle Scholar
Bush, G. (1994) Sympatric speciation in animals: new wine in old bottles. Trends in Ecology & Evolution 9, 285288.Google Scholar
Cantelo, W. & Jacobson, M. (1979) Corn silks volatiles attract many pests species of moths. Journal of Environmental Science and Health 14, 695707.Google Scholar
Craig, T.P., Itami, J.K., Abrahamson, W.G. & Horner, J.D. (1993) Behavioral evidence for host-race formation in Eurosta solidaginis. Evolution 47, 16961710.Google ScholarPubMed
Craig, T.P., Horner, J.D. & Itami, J.K. (2001) Genetics, experience, and host-plant preference in Eurosta solidaginis: Implications for host shifts and speciation. Evolution 55, 773782.CrossRefGoogle ScholarPubMed
Dalecky, A., Ponsard, S., Bailey, R.I., Pelissier, C. & Bourguet, D. (2006) Resistance evolution to Bt crops: Predispersal mating of European corn borers. PLoS Biology 4, 10481057.Google Scholar
Derridj, S., Gregoire, V., Boutin, J. & Fiala, V. (1989) Plant growth stages in the interspecific oviposition preference of the European corn borer and relations with chemicals present on leaf surfaces. Entomologia Experimentalis et Applicata 53, 267276.CrossRefGoogle Scholar
Drès, M. & Mallet, J. (2002) Host races in plant-feeding insects and their importance in sympatric speciation. Philosophical Transactions of the Royal Society of London, Series B 357, 471492.CrossRefGoogle ScholarPubMed
Emelianov, I., Dres, M., Baltensweiler, W. & Mallet, J. (2001) Host-induced assortative mating in host races of the larch budmoth. Evolution 55, 20022010.Google Scholar
Emelianov, I., Simpson, F., Narang, P. & Mallet, J. (2003) Host choice promotes reproductive isolation between host races of the larch budmoth Zeiraphera diniana. Journal of Evolutionary Biology 16, 208218.CrossRefGoogle ScholarPubMed
Feder, J., Opp, S., Wlazlo, B., Reynolds, K., Go, W. & Spisak, S. (1994) Host fidelity is an effective premating barrier between sympatric races of the apple maggot fly. Proceedings of the National Academy of Sciences, USA 91, 79907994.CrossRefGoogle ScholarPubMed
Frolov, A. (1991) Analysis of trophic relations of the European corn borer and brush-leg borer (Lepidoptera, Pyraustidae) in the border of the maize field weeded with mugwort. Ekologiya 3, 6369.Google Scholar
Frolov, A.N., Dyatlova, K.D. & Andriyash, N.V. (1995) European corn borer on sorghum in the Krasnodar region. Kukuruza i Sorgo 2, 56.Google Scholar
Frolov, A.N., Bourguet, D. & Ponsard, S. (2007) Reconsidering the taxomony of several Ostrinia species in the light of reproductive isolation: a tale for Ernst Mayr. Biological Journal of the Linnean Society 91, 4972.CrossRefGoogle Scholar
Funk, D.J., Filchak, K.E. & Feder, J.L. (2002) Herbivorous insects: model systems for the comparative study of speciation ecology. Genetica 116, 251267.CrossRefGoogle ScholarPubMed
Guthrie, W.D., Dharmalingam, S., Jarvis, J.L., Kindler, D., Atkins, R.E., Tseng, C.T. & Zhou, D. (1985) Resistance of sorghum genotypes to leaf feeding by first-generation European corn borer larvae compared with maize genotypes. Journal of Agricultural Entomology 2, 175184.Google Scholar
Hunt, T.E., Higley, L.G., Witkowski, J.F., Young, L.J. & Hellmich, R.L. (2001) Dispersal of adult European corn borer (Lepidoptera: Crambidae) within and proximal to irrigated and non-irrigated corn. Journal of Economic Entomology 94, 13691377.CrossRefGoogle Scholar
Leniaud, L., Audiot, P., Bourguet, D., Frerot, B., Genestier, G., Lee, S.F., Malausa, T., Le Pallec, A.H., Souqual, M.C. & Ponsard, S. (2006) Genetic structure of European and Mediterranean maize borer populations on several wild and cultivated host plants. Entomologia Experimentalis et Applicata 120, 5162.Google Scholar
Lupoli, R., Marion-Poll, F., Pham-Delègue, M. & Masson, C. (1990) Influence of maize leaf volatiles on the oviposition preferences of Ostrinia nubilalis (Lepidoptera: Pyralidae). Comptes Rendus de l'Academie des Sciences, Paris 311, 225230.Google Scholar
Malausa, T., Bethenod, M.T., Bontemps, A., Bourguet, D., Cornuet, J.M. & Ponsard, S. (2005) Assortative mating in sympatric host races of the European corn borer. Science 308, 258260.Google Scholar
Malausa, T., Leniaud, L., Martin, J.F., Audiot, P., Bourguet, D., Ponsard, S., Lee, S.F., Harrison, R.G. & Dopman, E. (2007a) Molecular differentiation at several nuclear loci in French host races of the European corn borer (Ostrinia nubilalis). Genetics 176, 23432355.Google Scholar
Malausa, T., Dalecky, A., Ponsard, S., Audiot, P., Chaval, Y., Streiff, R. & Bourguet, D. (2007b) Genetic structure and gene flow in French populations of two Ostrinia taxa: Host races or sibling species? Molecular Ecology 16, 42104222.CrossRefGoogle ScholarPubMed
Manojlovic, B. (1984) The possibility of survival of the larvae of the European corn borer (Ostrinia nubilalis Hbn., Lep. Pyralidae) on various food-plants. Zastita Bilja 35, 261270.Google Scholar
Martel, C., Réjasse, A., Rousset, F., Bethenod, M.-T. & Bourguet, D. (2003) Host-plant-associated genetic differentiation in northern French populations of the European corn borer. Heredity 90, 141149.CrossRefGoogle ScholarPubMed
Mitter, C., Farrell, B. & Wirgman, B. (1988) The phylogenetic study of adaptive zones: has phytophagy promoted insect diversification? American Naturalist 132, 107128.CrossRefGoogle Scholar
Nagy, B. (1976) Host selection of the European corn borer (Ostrinia nubilalis Hübner) populations in Hungary. Symposium Biologica Hungarica 16, 191195.Google Scholar
Painter, R. & Weibel, D. (1951) European corn borer damage to grain sorghums. Journal of Economic Entomology 44, 796798.CrossRefGoogle Scholar
Pappers, S.M., Velde, G.V.D. & Ouborg, N.J. (2002) Host preference and larval performance suggest host race formation in Galerucella nymphaeae. Oecologia 130, 433440.Google Scholar
Patch, L. (1942) Height of corn as a factor in egg laying by the European corn borer moth in the one-generation area. Journal of Agricultural Research 64, 503515.Google Scholar
Pélozuelo, L., Malosse, C., Genestier, G., Guenego, H. & Frérot, B. (2004) Host-plant specialization in pheromone strains of the European corn borer Ostrinia nubilalis in France. Journal Chemical Ecology 30, 335352.CrossRefGoogle ScholarPubMed
Ponsard, S., Bethenod, M.-T., Bontemps, A., Pélozuelo, L., Souqual, M.-C. & Bourguet, D. (2004) Carbon stable isotopes: a tool for studying the mating, oviposition, and spatial distribution of races of European corn borer, Ostrinia nubilalis, among host plants in the field. Canadian Journal of Zoology 82, 11771185.Google Scholar
Prokopy, R.J., Diehl, S.R. & Cooley, S.S. (1988) Behavioral evidence for host races in Rhagoletis pomonella flies. Oecologia 76, 138147.Google Scholar
Qureshi, J.A., Buschman, L.L., Throne, J.E. & Ramaswamy, S.B. (2005) Adult dispersal of Ostrinia nubilalis Hübner (Lepidoptera: Crambidae) and its implications for resistance management in Bt-maize. Journal of Applied Entomology 129, 281292.Google Scholar
Rundle, H. & Nosil, P. (2005) Ecological speciation. Ecology Letters 8, 336352.CrossRefGoogle Scholar
SAS (1989) JMP user's guide. SAS Institute, Cary, NC, USA.Google Scholar
Savinelli, C., Bacheler, J. & Bradley, J.R. (1988) Ovipositional preferences of the European corn borer (Lepidoptera: Pyralidae) for field corn and cotton under field cage conditions in North Carolina. Environmental Entomology 17, 688690.Google Scholar
Schluter, D. (2001) Ecology and the origin of species. Trends in Ecology & Evolution 16, 372380.CrossRefGoogle ScholarPubMed
Schurr, K. & Holdaway, F. (1970) Olfactory responses of female Ostrinia nubilalis (Lepidoptera: Pyraustinae). Entomologia Experimentalis et Applicata 13, 455461.Google Scholar
Sezer, M. & Butlin, R.K. (1998) The genetic basis of oviposition preference differences between sympatric host races of the brown planthopper (Nilaparvata lugens). Proceedings of the Royal Society of London Series B 265, 23992405.Google Scholar
Showers, W., Reed, G., Robinson, J. & Derozari, M. (1976) Flight and sexual activity of the European corn borer. Environmental Entomology 5, 10991104.Google Scholar
Showers, W., Hellmich, R.L., Derrick-Robinson, M.E. & Hendrix, W. (2001) Aggregation and dispersion behaviour of marked and released European corn borer (Lepidoptera: Crambidae) adults. Environmental Entomology 30, 700710.Google Scholar
Spangler, S. & Calvin, D. (2000) Influence of sweet corn growth stages on European corn borer (Lepidoptera: Crambidae) oviposition. Environmental Entomology 29, 12261235.CrossRefGoogle Scholar
Thomas, Y., Bethenod, M.-T., Pélozuelo, L., Frérot, B. & Bourguet, D. (2003) Genetics isolation between two sympatric host-plant races of the European corn borer, Ostrinia nubilalis Hübner. I. Sex pheromone, moth emergence timing, and parasitism. Evolution 57, 261273.Google Scholar
Via, S. (2001) Sympatric speciation in animals: the ugly duckling grows up. Trends in Ecology & Evolution 16, 381390.CrossRefGoogle ScholarPubMed
Via, S. & Hawthorne, D.J. (2002) The genetic architecture of ecological specialization: correlated gene effects on host use and habitat choice in pea aphids. American Naturalist 159, S76S88.CrossRefGoogle ScholarPubMed
Vilkova, N. & Frolov, A. (1978) Relations of maize and hemp populations of the European corn borer with their food plants in the North Caucasus. Bulletin Vsesoyuznogo Instituta Zashchiti Rastenii 43, 3741.Google Scholar
Ward, L.K., Hackshaw, A. & Clarke, R.T. (2003) Do food-plant preferences of modern families of phytophagous insects and mites reflect past evolution with plants? Biological Journal of the Linnean Society 78, 5183.Google Scholar