Hostname: page-component-848d4c4894-4rdrl Total loading time: 0 Render date: 2024-06-30T07:03:19.656Z Has data issue: false hasContentIssue false

SEX-LINKED GENES AND SPECIES DIFFERENCES IN LEPIDOPTERA

Published online by Cambridge University Press:  31 May 2012

Felix A.H. Sperling
Affiliation:
Department of Biology, University of Ottawa, Ottawa, Ontario, Canada K1N 6N5

Abstract

I review reports on the genetic basis for species differences in the Lepidoptera. In the six best-studied species complexes, more than half of all ecological, behavioral, or physiological differences among species are controlled by X-linked genes. Because Lepidoptera have about 30 pairs of chromosomes, this finding clearly indicates strong bias toward X-linkage of genes for species differences. The proportion of X-linked species differences ranges from complete X-linkage in Colias butterflies, to almost none in Yponomeuta moths. Four other complexes all have at least one X-linked gene that is crucial to species differences, including the Choristoneura fumiferana Clemens, Papilio glaucus L., and Papilio machaon L. species groups, and Ostrinia nubilalis Hübner pheromone strains. The mechanisms that account for this phenomenon are open to speculation. Nonetheless, an interesting implication of disproportionate X-linkage is that reproductive isolation may frequently arise by selection on linkage complexes, rather than as a random byproduct of evolution in geographically isolated populations. If confirmed, the bias toward X-linked species differences may also help efforts to find characters that distinguish host races and sibling species, as well as provide an avenue by which genes crucial to speciation can be more easily mapped and characterized at the molecular level.

Résumé

J’ai fait la synthèse des données sur l’origine génétique des différences spécifiques chez les Lépidoptères. Chez les six complexes d’espèces les plus étudiés, plus de la moitié de toutes les différences écologiques, comportementales et physiologiques entre les espèces sont attribuables à des gènes liés au chromosome X. Comme les Lépidoptères ont environ 30 paires de chromosomes, cette constatation indique clairement que les différences spécifiques sont fortement reliées au linkage à l’X des différents gènes. La proportion des différences spécifiques liées à l’X va de 100% chez les espèces de Colias, à près de 0% chez les papillons nocturnes du genre Yponomeuta. Quatre autres complexes ont tous au moins un gène lié à l’X qui est essentiel aux différences spécifiques, notamment les groupes d’espèces de Choristoneura fumiferana Clemens, de Papilio glaucus L. et de Papilio machaon L., et les lignées d’Ostrinia nubilalis Hübner différenciées par leurs phéromones. Les mécanismes responsables de ce phénomène sont mal connus. Cependant, l’un des corollaires intéressants de l’hypothèse d’un linkage à l’X disproportionné suppose que l’isolement génétique est souvent le résultat de la sélection de complexes de linkage plutôt que le produit aléatoire de l’évolution chez des populations isolées géographiquement. Si cette hypothèse est confirmée, l’attribution des différences spécifiques aux gènes liés à l’X peut également rendre plus facile la détermination de caractères qui distinguent les races hôtes et les espèces soeurs; elle peut également faciliter la cartographie des gènes essentiels à la spéciation et permettre de les caractériser au niveau moléculaire.

[Traduit par la Rédaction]

Type
Articles
Copyright
Copyright © Entomological Society of Canada 1994

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

Ae, S.A. 1979. The phylogeny of some Papilio species based on interspecific hybridization data. Systematic Entomology 4: 116.CrossRefGoogle Scholar
Arduino, P., and Bullini, L.. 1985. Reproductive isolation and genetic divergence between the small ermine moths Yponomeuta padellus and Y. malinellus (Lepidoptera: Yponomeutidae). Atti della Accademia Nazionale dei Lincei Memorie, Serie 8, Sezione 3 18: 3361.Google Scholar
Brower, L.P. 1959. Speciaton in butterflies of the Papilio glaucus group. II. Ecological relationships and interspecific sexual behavior. Evolution 13: 4063.CrossRefGoogle Scholar
Campbell, I.M. 1958. A Genetic Study of Factors determining Fecundity in the Genus Choristoneura Led. (Lepidoptera: Tortricidae). Ph.D. dissertation, University of Toronto, Ont., Canada. 176 pp.Google Scholar
Campbell, I.M. 1961. Polygyny in Choristoneura Led. (Lepidoptera: Tortricidae). The Canadian Entomologist 93: 11601162.CrossRefGoogle Scholar
Campbell, I.M. 1962. Reproductive capacity in the genus Choristoneura Led. (Lepidoptera: Tortricidae). I. Quantitative inheritance and genes as controllers of rates. Canadian Journal of Genetics and Cytology 4: 272288.CrossRefGoogle Scholar
Cardé, R.T., Roelofs, W.L., Harrison, R.G., Vawter, A.T., Brussard, P.F., Mutuura, A., and Munroe, E.. 1978. European corn borer: Pheromone polymorphism or sibling species? Science 199: 555556.CrossRefGoogle ScholarPubMed
Caspari, E.W., and Gottlieb, F.J.. 1975. The Mediterranean meal moth, Ephestia kuhniella. pp. 125–148 in King, R.C.. (Ed.), Handbook of Genetics, Volume 3, Invertebrates of Genetic Interest. Plenum, New York, NY. 874 pp.Google Scholar
Castrovillo, P.J. 1982. Interspecific and introspecific genetic comparisons of North American spruce budworms (Choristoneura ssp.). Ph.D. dissertation, University of Idaho, Moscow, ID, USA. 154 pp.Google Scholar
Charlesworth, B., Coyne, J.A., and Barton, N.H.. 1987. The relative rates of evolution of sex chromosomes and auto-somes. American Naturalist 130: 113146.CrossRefGoogle Scholar
Clarke, C.A., Gordon, I.J., Smith, C.R., and Vane-Wright, R.I.. 1991. Phylogenetic relationships of three African swallowtail butterflies, Papilio dardanus, P. phorcas and P. constantinus: New data from hybrids (Lepidoptera: Papilionidae). Systematic Entomology 16: 257273.CrossRefGoogle Scholar
Clarke, C.A., Mittwoch, U., and Traut, W.. 1977. Linkage and cytogenetic studies in the swallowtail butterflies Papilio polyxenes Fab. and Papilio machaon L. and their hybrids. Proceedings of the Royal Society of London, Series B 198: 385399.Google Scholar
Clarke, C.A., and Sheppard, P.M.. 1955. A preliminary report on the genetics of the machaon group of swallowtail butterflies. Evolution 9: 182201.CrossRefGoogle Scholar
Clarke, C.A., and Sheppard, P.M.. 1972. The genetics of the mimetic butterfly Papilio memnon L. Philosophical Transactions of the Royal Society of London, Series B 263: 431458.Google Scholar
Clarke, C.A., Sheppard, P.M., and Thornton, I.W.B.. 1968. The genetics of the mimetic butterfly Papilio memnon L. Philosophical Transactions of the Royal Society of London, Series B 254: 3789.Google Scholar
Colvin, J.C., and Gatehouse, A.G.. 1993. Migration and genetic regulation of the pre-reproductive period in the Cotton-bollworm moth, Heliothis armigera. Heredity 70: 407412.CrossRefGoogle Scholar
Coyne, J.A. 1992. Genetics and speciation. Nature 355: 511515.CrossRefGoogle ScholarPubMed
Coyne, J.A., Charlesworth, B., and Orr, H.A.. 1991. Haldane's rule revisited. Evolution 45: 17101714.CrossRefGoogle ScholarPubMed
Coyne, J.A., and Orr, H.A.. 1989. Two rules of speciation. pp. 180–207 in Ott, D., and Endler, J.A. (Eds.), Speciation and its Consequences. Sinauer Associates Inc., Sunderland, MA. 679 pp.Google Scholar
Diehl, S.R., and Bush, G.L.. 1984. An evolutionary and applied perspective of insect biotypes. Annual Review of Entomology 29: 471504.CrossRefGoogle Scholar
Geiger, H. 1988. Enzyme electrophoresis and interspecific hybridization in Pieridae (Lepidoptera) — the case for enzyme electrophoresis. Journal of Research on the Lepidoptera 26: 6472.CrossRefGoogle Scholar
Glover, T., Campbell, M., Robbins, P., and Roelofs, W.. 1990. Sex-linked control of sex-pheromone behavioral responses in European corn-borer moths (Ostrinia nubilalis) confirmed with TPI marker gene. Archives of Insect Biochemistry and Physiology 15: 6777.CrossRefGoogle Scholar
Glover, T.J., Knodel, J.J., Robbins, P.S., Eckenrode, C.J., and Roelofs, W.L.. 1991. Gene flow among three races of European corn borers (Lepidoptera: Pyralidae) in New York State. Environmental Entomology 20: 13561362.CrossRefGoogle Scholar
Glover, T.J., Robbins, P.S., Eckenrode, C.J., and Roelofs, W.L.. 1992. Genetic control of voltinism characteristics in European corn borer races assessed with a marker gene. Archives of Insect Biochemistry and Physiology 20: 107117.CrossRefGoogle Scholar
Grula, J.W., and Taylor, O.R.. 1978. Genetics of mate-selection behavior in two species of Colias butterflies. Genetics 88: 3435.Google Scholar
Grula, J.W., and Taylor, O.R.. 1980 a. Some characteristics of hybrids derived from the sulphur butterflies, Colias eurytheme and C. philodice: Phenotypic effects of the X-chromosome. Evolution 34: 673687.Google Scholar
Grula, J.W., and Taylor, O.R.. 1980 b. The effect of X-chromosome inheritance on mate-selection behavior in the sulphur butterflies, Colias eurytheme and C. philodice. Evolution 34: 688695.Google ScholarPubMed
Hagen, R.H., Lederhouse, R.C., Bossart, J.L., and Scriber, J.M.. 1991. Papilio canadensis and P. glaucus (Papilionidae) are distinct species. Journal of the Lepidopterists' Society 45: 245258.Google Scholar
Hagen, R.H., and Scriber, J.M.. 1989. Sex-linked diapause, color, and allozyme loci in Papilio glaucus: Linkage analyis and significance in a hybrid zone. Journal of Heredity 80: 179185.CrossRefGoogle Scholar
Hagen, R.H., and Scriber, J.M.. 1991. Systematics of the Papilio glaucus and P. troilus species groups (Lepidoptera: Papilionidae): Inferences from allozymes. Annals of the Entomological Society of America 84: 380395.CrossRefGoogle Scholar
Haldane, J.B.S. 1922. Sex ratio and unisexual sterility in hybrid animals. Journal of Genetics 12: 101109.CrossRefGoogle Scholar
Han, E., and Gatehouse, A.G.. 1991. Genetics of precalling period in the oriental armyworm, Mythimna separata (Walker) (Lepidoptera; Noctuidae), and implications for migration. Evolution 45: 15021510.CrossRefGoogle ScholarPubMed
Harrison, R.G., and Vawter, A.T.. 1977. Allozyme differentiation between pheromone strains of the European corn borer, Ostrinia nubilalis. Annals of the Entomological Society of America 70: 717720.CrossRefGoogle Scholar
Harrison, R.G., Wintermeyer, S.F., and Odell, T.M.. 1983. Patterns of genetic variation within and among Gypsy Moth, Lymantria dispar (Lepidoptera: Lymantriidae), populations. Annals of the Entomological Society of America 76: 652656.CrossRefGoogle Scholar
Harvey, G.T. 1967. On coniferophagous species of Choristoneura (Lepidoptera: Tortricidae) in North America. V. Second diapause as a species character. The Canadian Entomologist 99: 486503.CrossRefGoogle Scholar
Harvey, G.T. 1985. The taxonomy of the coniferophagous Choristoneura (Lepidoptera Tortricidae): A review. pp. 16–48 in Sanders, C.J., Stark, R.W., Mullins, E.J., and Murphy, J. (Eds.), Recent Advance in Spruce Budworms Research, Proceedings of the CANUSA Spruce Budworms Research Symposium, Bangor, Maine, 16–20 Sept. 1984. Canadian Forestry Service, Ottawa, Ont.527 pp.Google Scholar
Heckel, D.G. 1993. Comparative genetic linkage mapping in insects. Annual Review of Entomology 38: 381408.CrossRefGoogle Scholar
Hendrikse, A. 1979. Activity patterns and sex pheromone specificity as isolating mechanisms in eight species of Yponomeuta (Lepidoptera: Yponomeutidae). Entomologia Experimentalis et Applicata 25: 172180.CrossRefGoogle Scholar
Hendrikse, A. 1988. Hybridization and sex-pheromone responses among members of the Yponomeuta padellus-complex. Entomologia Experimentalis et Applicata 48: 213233.CrossRefGoogle Scholar
Hendrikse, A., and Vos-Bünnemeyer, E.. 1987. Role of host-plant stimuli in sexual behavior of small ermine moths (Yponomeuta). Ecological Entomology 12: 363371.CrossRefGoogle Scholar
Hill, J.K., and Gatehouse, A.G.. 1992. Genetic control of the pre-reproductive period in Autographa gamma (L.) (Silver Y moth) (Lepidoptera: Noctuidae). Heredity 69: 458464.CrossRefGoogle Scholar
Hudon, M., LeRoux, E.J., and Harcourt, D.G.. 1989. Seventy years of European corn borer (Ostrinia nubilalis) research in North America. Agricultural Zoology Reviews 3: 5396.Google Scholar
Johnson, M.S., and Turner, J.R.G.. 1979. Absence of dosage compensation for a sex-linked enzyme in butterflies (Heliconius). Heredity 43: 7177.CrossRefGoogle Scholar
Kingsolver, J.G., and Wiernasz, D.C.. 1991. Development, function, and the quantitative genetics of wing melanin pattern in Pieris butterflies. Evolution 45: 14801492.Google ScholarPubMed
Klun, J.A., and cooperators. 1975. Insect sex pheromones: Intraspecific pheromonal variability of Ostrinia nubilalis in North America and Europe. Environmental Entomology 4: 891894.CrossRefGoogle Scholar
Klun, J.A., and Maini, S.. 1979. Genetic basis of an insect chemical communication system: The European corn borer. Environmental Entomology 8: 423426.CrossRefGoogle Scholar
Kochansky, J., Cardé, R.T., Liebherr, J., and Roelofs, W.L.. 1975. Sex pheromone of the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae), in New York. Journal of Chemical Ecology 1: 225231.CrossRefGoogle Scholar
Lee, D.A., and Spence, J.R.. 1987. Reproductive patterns of European corn borer (Ostrinia nubilalis) in Alberta. Canadian Journal of Zoology 65: 17331740.CrossRefGoogle Scholar
Liebherr, J., and Roelofs, W.. 1975. Laboratory hybridization and mating period studies using two pheromone strains of Ostrinia nubilalis. Annals of the Entomological Society America 68: 305309.CrossRefGoogle Scholar
Löfstedt, C. 1990. Population variation and genetic control of pheromone communication systems in moths. Entomologia Experimentalis et Applicata 54: 199218.CrossRefGoogle Scholar
Lorkovic, Z. 1986. Enzyme electrophoresis and interspecific hybridization in Pieridae (Lepidoptera). Journal of Research on the Lepidoptera 24: 334358.CrossRefGoogle Scholar
May, B., Leonard, D.E., and Vadas, R.L.. 1977. Electrophoretic variation and sex-linkage in spruce budworm. Journal of Heredity 68: 355359.CrossRefGoogle Scholar
McLeod, D.G.R. 1978. Genetics of diapause induction and termination in the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae), in southwestern Ontario. The Canadian Entomologist 110: 13511353.CrossRefGoogle Scholar
Menken, S.B.J. 1980. Inheritance of allozymes in Yponomeuta. II. Interspecific crosses within the padellus-complex and reproductive isolation. Proceedings of the Koninklijke Nederlandse Academie van Wetenschappen, Series C 83: 425431.Google Scholar
Menken, S.B.J. 1982. Biochemical genetics and systematics of small ermine moths. Zeitshrift für Zoologisches Systematik und Evoltionsforschung 20: 131143.CrossRefGoogle Scholar
Menken, S.B.J., Herrebout, W.M., and Wiebes, J.T.. 1992. Small ermine moths (Yponomeuta): Their host relations and evolution. Annual Review of Entomology 37: 4166.CrossRefGoogle Scholar
Menken, S.B.J., and Ulenberg, S.A.. 1987. Biochemical characters in agricultural entomology. Agricultural Zoology Reviews 2: 305360.Google Scholar
Mitter, C., Poole, R.W., and Matthews, M.. 1993. Biosystematics of the Heliothinae (Lepidoptera: Noctuidae). Annual Review of Entomology 38: 207225.CrossRefGoogle Scholar
Nilsson, N.-O., Löfstedt, C., and Dävring, L.. 1988. Unusual sex pheromone inheritance in six species of small ermine moths (Yponomeuta, Yponomeutidae, Lepidoptera). Hereditas 108: 259265.CrossRefGoogle Scholar
Orr, H.A. 1993. Haldane's rule has multiple genetic causes. Nature 361: 532533.CrossRefGoogle ScholarPubMed
Pashley, D.P., Hammond, A.M., and Hardy, T.N.. 1992. Reproductive isolating mechanisms in fall armyworm host strains (Lepidoptera: Noctuidae). Annals of the Entomological Society of America 85: 400405.CrossRefGoogle Scholar
Platt, A.P. 1983. Evolution of North American admiral butterflies. Bulletin of the Entomological Society of America 29: 1022.CrossRefGoogle Scholar
Robinson, R. 1971. Lepidoptera Genetics. Pergamon Press, Oxford, UK. 687 pp.Google Scholar
Rockey, S.J., Hainze, J.H., and Scriber, J.M.. 1987. Evidence of sex-linked diapause response in Papilio glaucus subspecies and their hybrids. Physiological Entomology 12: 181184.CrossRefGoogle Scholar
Roelofs, W.L., Du, J.-W., Tang, X.-H., Robbins, P.S., and Eckenrode, C.J.. 1985. Three European corn borer populations in New York based on sex pheromones and voltinism. Journal of Chemical Ecology 11: 829836.CrossRefGoogle ScholarPubMed
Roelofs, W., Glover, T., Tang, X.-H., Sreng, I., Robbins, P., Eckenrode, C., Löfstedt, C., Hansson, B.S., and Bengtsson, B.O.. 1987. Sex pheromone production and perception in European corn borer moths is determined by both autosomal and sex-linked genes. Proceedings of the National Academy of Sciences, USA 84: 75857589.CrossRefGoogle ScholarPubMed
Sanders, C.J., Daterman, G.E., and Ennis, T.J.. 1977. Sex pheromone responses of Choristoneura spp. and their hybrids (Lepidoptera: Tortricidae). The Canadian Entomologist 109: 12031220.CrossRefGoogle Scholar
Scott, J.A. 1986. The Butterflies of North America. Stanford University Press, Stanford, CA. 583 pp.CrossRefGoogle Scholar
Scriber, J.M. 1986. Allelochemicals and alimentary ecology: Heterosis in a hybrid zone? pp. 43–71 in Brattsten, L.B., and Ahmad, S. (Eds.), Molecular Aspects of Insect–Plant Associations. Plenum Press, New York, NY. 346 pp.Google Scholar
Scriber, J.M. 1992. Latitudinal clines in oviposition preferences: Ecological and genetic influences. pp. 212–214 in Menken, S.B.J., Visser, J.H., and Harrewijn, P. (Eds.), Proceedings of the 8th International Symposium on Insect–Plant Relationships. Kluwer Academic, Dordrecht. 424 pp.Google Scholar
Sheppard, P.M., Turner, J.R.G., Brown, K.S., Benson, W.W., and Singer, M.C.. 1985. Genetics and the evolution of Muellerian mimicry in Heliconius butterflies. Philosophical Transactions of the Royal Society of London, Series B 308: 433610.Google Scholar
Showers, W.B. 1981. Geographic variation of the diapause response in the European corn borer. pp. 97–111 in Denno, R.F., and Dingle, H. (Eds.), Insect Life History Patterns: Habitat and Geographic Variation. Springer-Verlag, New York, NY. 225 pp.Google Scholar
Silberglied, R.E., and Taylor, O.R.. 1973. Ultraviolet differences between the sulphur butterflies, Colias eurytheme and C. philodice, and a possible isolating mechanism. Nature 241: 406408.CrossRefGoogle Scholar
Silberglied, R.E., and Taylor, O.R.. 1978. Ultraviolet reflection and its behavioral role in the courtship of the sulphur butterflies Colias eurytheme and C. philodice (Lepidoptera, Pieridae). Behavioral Ecology and Sociobiology 3: 203243.CrossRefGoogle Scholar
Smith, S.G. 1953. Reproductive isolation and the integrity of two sympatric species of Choristoneura (Lepidoptera: Tortricidae). The Canadian Entomologist 85: 141151.CrossRefGoogle Scholar
Smith, S.G. 1954. A partial breakdown of temporal and ecological isolation between Choristoneura species (Lepidoptera: Tortricidae). Evolution 8: 206224.CrossRefGoogle Scholar
Sorenson, C.E., Kennedy, G.G., Van Duyn, W., Bradley, J.R. Jr., and Walgenbach, J.F.. 1992. Geographical variation in pheromone response of the European corn borer, Ostrinia nubilalis, in North Carolina. Entomologia Experimentalis et Applicata 64: 177185.CrossRefGoogle Scholar
Sperling, F.A.H. 1987. Evolution of the Papilio machaon species group in western Canada. Qaestiones Entomologica 23: 198315.Google Scholar
Sperling, F.A.H. 1990. Natural hybrids of Papilio (Insecta: Lepidoptera): Poor taxonomy or interesting evolutionary problem? Canadian Journal of Zoology 68: 17901799.CrossRefGoogle Scholar
Sperling, F.A.H. 1993 a. Mitochondrial DNA phylogeny of the Papilio machaon species group (Lepidoptera: Papilionidae). pp. 233–242 in Ball, G.E., and Danks, H.V. (Eds.), Systematics and Evolution: Diversity, Distribution, Adaptation, and Application. Memoirs of the Entomological Society of Canada 165: 272 pp.Google Scholar
Sperling, F.A.H. 1993 b. Mitochondrial DNA variation and Haldane's rule in the Papilio glaucus and P. troilus species groups. Heredity 70: 227233.CrossRefGoogle Scholar
Stehr, G. 1955. Brown female — a sex-linked and sex-limited character. Journal of Heredity 46: 263266.CrossRefGoogle Scholar
Stehr, G. 1959. Hemolymph polymorphism in a moth and the nature of sex-controlled inheritance. Evolution 13: 537560.CrossRefGoogle Scholar
Stehr, G. 1964. The determination of sex and polymorphism in microevolution. The Canadian Entomologist 96: 418428.CrossRefGoogle Scholar
Tauber, C.A., and Tauber, M.J.. 1989. Sympatric speciation in insects: Perception and perspective. pp. 307–344 in Ott, D., and Endler, J.A. (Eds.), Speciation and its Consequences. Sinauer Associates Inc., Sunderland, MA. 679 pp.Google Scholar
Taylor, O.R. 1972. Random vs. non-random mating in the sulphur butterflies, Colias eurytheme and Colias philodice (Lepidoptera: Pieridae). Evolution 26: 344356.Google ScholarPubMed
Tazima, Y., Doira, H., and Akai, H.. 1975. The domesticated silkmoth, Bombyx mori. pp. 63–124 in King, R.C. (Ed.), Handbook of Genetics, Volume 3, Invertebrates of Genetic Interest. Plenum, New York, NY. 874 pp.Google Scholar
Thompson, J.N. 1988. Evolutionary genetics of oviposition preference in swallowtail butterflies. Evolution 42: 12231235.CrossRefGoogle ScholarPubMed
Thompson, J.N., Wehling, W., and Podolsky, R.. 1990. Evolutionary genetics of host use in swallowtail butterflies. Nature 344: 148150.CrossRefGoogle Scholar
van Drongelen, W., and van Loon, J.. 1980. Inheritance of gustatory sensitivity in F1 progeny of crossses between Yponomeuta cagnagellus and Y. malinellus (Lepidoptera). Entomologia Experientalis et Applicata 28: 199203.CrossRefGoogle Scholar
Wilson, K., and Gatehouse, A.G.. 1992. Migration and genetics of the pre-reproductive period in the African armyworm moth, Spodoptera exempta. Heredity 69: 255262.CrossRefGoogle Scholar
Wu, C.-I. 1992. A note on Haldane's rule: Hybrid inviability versus hybrid sterility. Evolution 46: 15841587.CrossRefGoogle ScholarPubMed