Eur. J. Entomol. 99 (2): 225-239, 2002 | DOI: 10.14411/eje.2002.032
Latitudinal and local geographic mosaics in host plant preferences as shaped by thermal units and voltinism in Papilio spp. (Lepidoptera)
- Department of Entomology, Michigan State University, 47 Natural Science Building, East Lansing, MI 48824-1115, USA; e-mail: scriber@msu.edu
Laboratory and field tests support the "voltinism-suitability hypothesis" of host selection at various latitudes as well as in local "cold pockets": The best hosts for rapid development will be selected by herbivorous insects under severe thermal constraints for completion of the generation before winter. Papilio canadensis and P. glaucus females do select the best hosts for rapid larval growth in Alaska and in southern Michigan, but not in northern Michigan and southern Ohio. In addition to latitudinal patterns, local host preferences of P. canadensis are described in relation to "phenological twisting" of leaf suitability for larval growth in cold pockets with "thermally constrained" growing season lengths. White ash leaves (Fraxinus americana) have the highest nutritional quality (relative to cherry, aspen, birch, and other local trees) throughout June and July for P. canadensis populations inside the cold pocket, but not outside. In all areas outside the cold pockets, even with bud-break occurring much later than other tree species, ash leaves rapidly decline in quality after mid-June and become one of the worse tree host species for larvae. This temperature-driven phenology difference creates a geographic mosaic in host plant suitability for herbivores. However, we also report here that the cold pocket of northern Michigan has basically disappeared since 1998. Implications of these changes are discussed in relation to voltinism and host plant selection.
Various physiological and ecological adaptations to thermal unit constraints are evident with both species of naturally hybridizing butterflies (P. canadensis to the North and P. glaucus to the South). The rapid regional climate warming since 1998 in the Great Lakes region has allowed us to document some critical aspects of gene flow via analysis of independent "species-diagnostic" trait clines (including morphological, biochemical, and physiological characters). Narrower black bands on hind-wings, larger fore-wings, larval detoxification abilities for tulip tree leaves, behavioral preference of tulip tree leaves, and species-diagnostic allozymes such as PDG (x-linked) and HK (autosomal) provide evidence of these genodynamics. Laboratory hybridization studies (providing known reference groups) and field observations along the hybrid zone show that gene flow between P. glaucus and P. canadensis has recently been extensive across the historical hybrid zone.
Keywords: Butterflies, climate warming, degree days, diapause, "false-second" generation, introgression, oviposition preferences, Papilio glaucus, P. canadensis, North America, reproductive isolation, sex-linkage
Received: November 9, 2001; Revised: May 13, 2002; Accepted: May 20, 2002; Published: June 30, 2002 Show citation
References
- Arnold M.L. 1997: Natural Hybridization and Evolution. Oxford Univ. Press, UK, 215 pp
Go to original source... - Ayres M.P., Bossart J. & Scriber J.M. 1991: Variation in the nutritional physiology of tree-feeding swallowtail caterpillars. In: Baranchikov Y.N., Mattson W.J., Hain F.P. & Payne T.L. (eds) Forest Insect Guilds: Patterns of Interactions with Host Trees. Conference proceedings (August 12-20, 1989) Abakan, Siberia, U.S.S.R. USDA Forest Service, Gen. Tech. Report, NE-153, pp. 85-102
- Ayres M.P. & Scriber J.M. 1994: Local adaptations to regional climates in Papilio canadensis (Lepidoptera: Papilionidae). Ecological Monographs 64: 465-482
Go to original source... - Barton N.H. & Hewitt G.M. 1985: Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 16: 497-503
Go to original source... - Beck S.D. 1980: Insect Photoperiodism. 2nd ed. Academic Press, NY, 387 pp
Go to original source... - Berlocher S.H. & Feder J.L. 2002: Sympatric speciation in phytophagous insects: moving beyond controversy? Annu. Rev. Entomol. 47: 773-815
Go to original source... - Bossart J.L. & Scriber J.M. 1999: Preference variation in the polyphagous tiger swallowtail butterfly (Lepidoptera: Papilionidae). Environ. Entomol. 28: 628-637
Go to original source... - Bradshaw W.E. & Holzapfel C.M. 2001: Phenotypic evolution and the genetic architecture underlying photoperiodic time measurement. J. Insect Physiol. 47: 809-820
Go to original source... - Brakefield P.M. & Reitsma N. 1991: Phenotypic plasticity, seasonal climate and the population biology of Bicyclus butterflies. Ecol. Entomol. 10: 291-303
Go to original source... - Cronin J.T., Abrahamson W.G. & Craig T.P. 2001: Temporal variation in herbivore host-plant preference and performance: constraints on host-plant adaptation. Oikos 93: 312-320
Go to original source... - Danilevskii A.S. 1961: Photoperiodism and Seasonal Development in Insects. English translation 1965. Oliver & Boyd, London, 283 pp
- Deering M.D. & Scriber J.M. 2002: Field bioassays show heterospecific mating preference assymetry between hybridizing North American Papilio butterfly species (Lepidoptera: Papilionidae). J. Ethology (in press), published "on line", March, 2002
- Deering M.D., Haslitt T. & Scriber J.M. 2002: Factors affecting diapause termination in Papilio troilus pupae (Lepidoptera: Papilionidae) Holarctic Lepidoptera 8: 43-47
- Denlinger D.L. 2002: Regulation of diapause. Annu. Rev. Entomol. 47: 93-122
Go to original source... - Eberhardt W.G. 1996: Female Control: Sexual Selection by Cryptic Female Choice. Princeton Univ., NJ, 501 pp
Go to original source... - Feder J.L. 1998: The apple maggot fly, Rhagoletis pomonella: flies in the face of conventional wisdom about speciation? In: Howard D.J. & Berlocher S.H. (eds) Endless Forms: Species and Speciation. Oxford Univ. Press, London, pp 130-140
- Fox L.R. & Morrow P.A. 1981: Specialization: species property or local phenomenon? Science 214: 887-893
Go to original source... - Futuyma D.J. 1976: Food plant specialization and environmental predictability in Lepidoptera. Am. Natur. 10: 285-292
Go to original source... - Giroux P. 1998: Testing the "cold pocket" hypothesis: Oviposition preference in the Canadian tiger swallowtail, Papilio canadensis. M.S. Thesis. Michigan State University, East Lansing, MI, 86 pp
- Gomi T. 1997: Geographic variation in critical photoperiod for diapause induction and its temperature dependence in Hyphantria cunea Drury (Lepidoptera: Arctiidae). Oecologia 111: 160-165
Go to original source... - Grossmueller D.W. & Lederhouse R.C. 1985: Oviposition site selection; An aid to rapid growth and development in the tiger swallowtail, Papilio glaucus. Oecologia 66: 68-73
Go to original source... - Hagen R.H. 1990: Population structure and host use in hybridizing subspecies of Papilio glaucus: Linkage analysis and significance in hybrid zone. Evolution 44: 1914-1930
Go to original source... - Hagen R.H. & Lederhouse R.C. 1985: Polymodal emergence of the tiger swallowtail, Papilio glaucus (Lepidoptera: Papilionidae): Source of a false second generation in central New York State. Ecol. Entomol. 10: 19-28
Go to original source... - Hagen R.H. & Scriber J.M. 1989: Sex-linked diapause, color, and allozyme loci in Papilio glaucus: Linkage analysis and significance in a hybrid zone. Heredity 80: 179-185
Go to original source... - Hagen R.C. & Scriber J.M. 1991: Systematics of the Papilio glaucus and P. troilus groups (Lepidoptera: Papilionidae): inferences from allozymes. Ann. Entomol. Soc. Am. 84: 380-395
Go to original source... - Hagen R. & Scriber J.M. 1995: Sex chromosomes and speciation in the Papilio glaucus group. In: Scriber J.M., Tsubaki Y. & Lederhouse R.C. (eds) The Swallowtail Butterflies: their Ecology and Evolutionary Biology. Scientific Publishers, Inc. Gainesville, FL, pp. 211-221
- Hagen R.H., Lederhouse R.C., Bossart J. & Scriber J.M. 1991: Papilio canadensis and P. glaucus (Papilionidae) are distinct species. J. Lepid. Soc. 45: 245-258
- Hughes L. 2000: Biological consequences of global warming: is the signal already apparent? Trends Ecol. Evol. 15: 56-61
Go to original source... - Jaenike J. 1978: On optimal oviposition behavior in phytophagous insects. Theor. Popul. Biol. 14: 350-356
Go to original source... - Jiigins C.S. & Mallet J. 2000: Bimodal hybrid zones and speciation. Trends Ecol. Evol. 15: 250-255
Go to original source... - Kukal O., Ayres M. P. & Scriber J.M. 1991: Cold tolerance of pupae in relation to the distribution of tiger swallowtails. Can. J. Zool. 69: 3028-3037
Go to original source... - Leather S.R. 1994: Life history traits of insect herbivores in relation to host quality. In: Bernays E.A. (ed.) Insect-Plant Interactions. Vol. V. CRC Press, Boca Raton, FL, pp 175-207
- Lechowicz M.J. 1984: Why do temperate deciduous forest trees leaf out at different times? Adaptation and ecology of forest communities. Am. Natur. 124: 821-842
Go to original source... - Lederhouse R.C. & Scriber J.M. 1987: The ecological significance of a post-mating decline in egg viability in the tiger swallowtail, Papilio glaucus L. (Papilionidae). J. Lepid. Soc. 41: 83-93
- Lederhouse R.L., Ayres M.P. & Scriber J.M. 1989: Evaluation of spermatophore counts in studying mating systems of Lepidoptera. J. Lepid. Soc. 43: 93-101
- Lederhouse R.C., Ayres M.P. & Scriber J.M. 1990: Adult nutrition affects male virility in Papilio glaucus. Funct. Ecol. 4: 743-751
Go to original source... - Lederhouse R.C., Finke M. & Scriber J.M. 1982: The contributions of larval growth and pupal duration to protandry in the black swallowtail butterfly, Papilio polyxenes. Oecologia 53: 296-300
Go to original source... - Luebke H.J., Scriber J.M. & Yandell B.S. 1988: Use of multivariate discriminant analysis of male wing morphometrics to delineate the Wisconsin hybrid zone for Papilio glaucus glaucus and P.g. canadensis. Am. Midl. Natur. 119: 366-379
Go to original source... - Mattson W.J. & Scriber J.M. 1987: Nutritional ecology of insect folivores of woody plants: water, nitrogen, fiber, and mineral considerations. In: Slansky F. Jr. & Rodriguez J.G. (eds) Nutritional Ecology of Insects, Mites, and Spiders. John Wiley, NY. pp. 105-146
- Mayhew P.J. 1997: Adaptive patterns of host-plant selection by phytophagous insects. Oikos 79: 419-428
Go to original source... - Merriam C.H. 1894: Laws of temperature control of the geographic distribution of terrestrial animals and plants. Nat. Geogr. Mag. 6: 229-238
- Mopper S. 1996: Adaptive genetic structure in phytophagous insect populations. Trends Ecol. Evol. 11: 235-238
Go to original source... - Mousseau T.A., Sinervo B. & Endler J. 2000: Adaptive Genetic Variation in the Wild. Oxford Univ. Press, UK. Nylin S. 1988: Host-plant specialization and seasonality in a polyphagous butterfly, Polygonia c-album (Nymphalidae). Oikos 53: 381-386
Go to original source... - Nylin S. 1992: Seasonal plasticity in life history traits: growth and development in Polygonia c-album (Lepidoptera: Nymphalidae). Biol. J. Linn. Soc. 47: 301-323
Go to original source... - Nylin S. & Gotthard K. 1998: Plasticity in life-history traits. Annu. Rev. Entomol. 43: 63-83
Go to original source... - Nylin S., Janz N. & Wedell N. 1996: Oviposition plant preferences and offspring performance in the comma butterfly: correlations and conflicts. Entomol. Exp. Appl. 80: 141-144
Go to original source... - Nylin S., Wiklund C. & Wickman P-O. 1993: Absence of trade-offs between sexual size dimorphism and early male emergence in a butterfly. Ecology 74: 1414-1427
Go to original source... - Oliver C.G. 1983: Disturbance eclosion sequence in hybrid Lepidoptera. Can. Entomol. 115: 1445-1452
Go to original source... - Pimm S.L. 2001: Entrepreneurial insects. Nature 411: 531- 532
Go to original source... - Pullin A.S. 1986: Effect of photoperiod and temperature on the life-cycle of different populations of the peacock butterfly Inachis. Entomol. Exp. Appl. 41: 237-242
Go to original source... - Rand D.M. & Harrison R.G. 1989: Ecological genetics of a mosaic hybrid zone: mitochondrial, nuclear and reproductive differentiation of crickets by soil type. Evolution 43: 432-449
Go to original source... - Redman A. & Scriber J.M. 2000: Competition between gypsy moth, Lymantria dispar, and the northern tiger swallowtail, Papilio canadensis: interactions mediated by host plant chemistry, pathogens, and parasitoids. Oecologia 125: 218-228
Go to original source... - Reiseberg L.H., Whitton J. & Gardner K. 1999: Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152: 713-727
Go to original source... - Ritland D.B. & Scriber J.M. 1985: Larval developmental rates of three putative subspecies of tiger swallowtail butterflies, Papilio glaucus, and their hybrids in relation to temperature. Oecologia 65: 185-193
Go to original source... - Rockey S.J., Hainze J.H. & Scriber J.M. 1987a: Evidence of a sex-linked diapause response in Papilio glaucus subspecies and their hybrids. Physiol. Entomol. 12: 181-184
Go to original source... - Rockey S.J., Hainze J.H. & Scriber J.M. 1987b: A latitudinal and obligatory diapause response in three subspecies of the eastern tiger swallowtail Papilio glaucus (Lepidoptera: Papilionidae). Am. Midl. Nat. 118: 162-168
Go to original source... - Ronce O. & Kirkpatrick M. 2001: When sources become sinks: migrational meltdown in heterogenous habitats. Evolution 55: 1520-1531
Go to original source... - Scheirs J. 2002: Integrating optimal foraging and optimal oviposition theory in plant-insect research. Oikos 96: 187-191
Go to original source... - Scriber J.M. 1975: Comparative Nutritional Ecology of Herbivorous Insects: Generalized and Specialized Feeding Strategies in the Papilionidae and Saturniidae (Lepidoptera). Ph.D. dissertation, Cornell Univ. Ithaca, NY. 289 pp
- Scriber J.M. 1982: Foodplants and speciation in the Papilio glaucus group. In: Visser J.H. &. Minks A.K. (eds) Proc. 5th Int. Symp. on Insect Plant Relationships. PUDOC. Wageningen, Netherlands, pp. 307-314
- Scriber J.M. 1983: The evolution of feeding specialization physiological efficiency, and host races. In: Denno R.F. & McClure M.S. (eds) Variable Plants and Herbivores in Natural and Managed Systems. Academic Press, NY, pp. 373-412
Go to original source... - Scriber J.M. 1984: Insect/Plant Interactions - Host plant suitability. In: Bell W. & Carde R. (eds) The Chemical Ecology of Insects. Chapman & Hall, London, pp. 159-202
Go to original source... - Scriber J.M. 1990: Interaction of introgression from Papilio glaucus canadensis and diapause in producing "spring form" Eastern tiger swallowtail butterflies, P. glaucus. Great Lakes Entomol. 23: 127-138
Go to original source... - Scriber J.M. 1991: Differential suitability of 12 Great Lakes tree species for Papilio canadensis (Lepidoptera: Papilionidae) larval survival and growth. Great Lakes Entomol. 24: 239-252
Go to original source... - Scriber J.M. 1993: Absence of behavioral induction in oviposition preference of Papilio glaucus (Lepidoptera: Papilionidae). Great Lakes Entomol. 26: 81-95
Go to original source... - Scriber J.M. 1994: Climatic legacies and sex chromosomes: latitudinal patterns of voltinism, diapause size and host-plant selection in 2 species of swallowtail butterflies at their hybrid zone. In: Danks H.V. (ed.) Insect Life-Cycle Polymorphism: Theory, Evolution and Ecological Consequences for Seasonality and Diapause Control. Kluwer Academic Publ., Dordrecht, Netherlands, pp. 133-171
Go to original source... - Scriber J.M. 1996a: A new cold pocket hypothesis to explain local host preference shifts in Papilio canadensis. 9th Intern. Symp. Insects & Host Plants. Entomol. Exp. Appl. 80: 315-319
Go to original source... - Scriber J.M. 1996b: Tiger tales: natural history of native North American swallowtails. Am. Entomol. 42: 19-32
Go to original source... - Scriber J.M. 1998: Inheritance of diagnostic larval traits for interspecific hybrids and Papilio canadensis and P. glaucus (Lepidoptera: Papilionidae). Great Lakes Entomol. 31: 113-123
Go to original source... - Scriber J.M. 2002: Evolution of insect-plant relationships: Chemical constraints, coadaptation, and concordance of insect/plant traits. Entomol. Exp. Appl. (manuscript in press from invited speaker address) Scriber J.M. & Gage S. 1995: Pollution and global climate change: Plant ecotones, butterfly hybrid zones, and biodiversity. In: Scriber J.M., Tsubaki Y. & Lederhouse R.C. (eds) Swallowtail Butterflies: Their Ecology and Evolutionary Biology. Scientific Publishers, Inc., Gainesville, FL, pp. 319-344
Go to original source... - Scriber J.M. & Grabstein E.M. 1991: Foodplant processing adaptations in four Hyalophora species (Lepidoptera: Saturniidae): regional and taxonomic specialization. Great Lakes Entomol. 24: 109-120
Go to original source... - Scriber J.M. & Hainze J. 1987: Geographic variation in host utilization and the development of insect outbreaks. In: Barbosa P. & Schultz J.C. (eds) Insect Outbreaks: Ecological and Evolutionary Processes. Academic Press, NY, pp. 433-468
Go to original source... - Scriber J.M. & Lederhouse R.C. 1983: Temperature as a factor in the development and feeding ecology of tiger swallowtail caterpillars, Papilio glaucus. Oikos 40: 95-102
Go to original source... - Scriber J.M. & Lederhouse R.C. 1992: The thermal environment as a resource dictating geographic patterns of feeding specialization of insect herbivores. In: Hunter M.R., Ohgushi T. & Price P.W. (eds) Effects of Resource Distribution on Animal-Plant Interactions. Academic Press, NY, pp 429-466
Go to original source... - Scriber J.M., Deering M.D., Francke L., Wehling W. & Lederhouse R.C. 1998b: Notes on the butterfly population dynamics of 3 Papilio species in south central Florida (Highlands County) Holarctic Lepidoptera 5: 53-62
- Scriber J.M., Keefover K. & Nelson S. 2002b: Hot summer temperatures may stop movement of Papilio canadensis butterflies and genetic introgression south of the hybrid zone in the North American Great Lakes region. Ecography 25: 184-192
Go to original source... - Scriber J.M., Deering M.D. & Stump A. 1998a: Evidence of long range transport of a swallowtail butterfly (Papilio glaucus L.) on a storm front into northern Michigan. Great Lakes Entomol. 31: 151-160
Go to original source... - Scriber J.M., Deering M.D. & Stump A. 2002a: Hybrid zone ecology: geographical and genetic distance influences on behavioral, biochemical, and ecological trait clines of tiger swallowtail butterflies. In: Boggs C., Watt W. & Ehrlich P. (eds) Ecology and Evolution Taking Flight: Butterflies as Model Study Systems. University of Chicago Press, Chicago, IL. (in press)
- Scriber J.M., Giebink B.L. & Snider D. 1991: Reciprocal latitudinal clines in oviposition behavior of Papilio glaucus and P. canadensis across the Great Lakes hybrid zone: possible sex-linkage of oviposition preferences. Oecologia 87: 360-368
Go to original source... - Scriber J.M., Hagen R.H. & Lederhouse R.C. 1996: Genetics of mimicry in the tiger swallowtail butterflies, Papilio glaucus and P. canadensis. (Lepidoptera: Papilionidae). Evolution 50: 222-236
Go to original source... - Scriber J.M., Lindroth R.L. & Nitao J. 1989: Differential toxicity of a phenolic glycoside from quaking aspen leaves by Papilio glaucus butterfly subspecies, their hybrids, and backcrosses. Oecologia 81: 186-199
Go to original source... - Scriber J.M., Weir K., Parry D. & Deering J. 1999: Using hybrid and backcross larvae of Papilio canadensis and P. glaucus to detect induced chemical resistance in hybrid poplars experimentally defoliated by gypsy moths. Entomol. Exp. Appl. 91:233-236
Go to original source... - Shaw D.D., Marchant A.D., Arnold M.L., Contreras N. & Kohlmann B. 1990: The control of gene flow across a narrow hybrid zone: a selective role for chromosomal rearrangement? Can. J. Zool. 68: 1761-1769
Go to original source... - Singer M.C. & Thomas C.D. 1996: Evolutionary responses of a butterfly metapopulation to human- and climate-caused environmental variation. Am. Natur. 148: 9-39
Go to original source... - Slansky F. & Scriber J.M. 1985: Food consumption and utilization. Chapter 3. In: Kerkut G.A. & Gilbert L.I. (eds) Volume 4, Comprehensive Insect Physiology, Biochemistry, and Pharmacology. Pergamon Press, Oxford, pp. 87-163
Go to original source... - Stump A. 2000: Lack of Cryptic Reproductive Isolation between Papilio canadensis and Papilio glaucus and Population Genetics near their Hybrid Zone. MS Thesis. Dept. Entomology, Michigan State Univ., East Lansing, MI, 105 pp
- Tauber M.J., Tauber C.A. & Masaki S. 1986: Seasonal Adaptations of Insects. Oxford Univ. Press, NY, 411 pp
- Tesar D. & Scriber J.M. 2002: Growth season constraints in climatic cold pockets: Tolerance of subfreezing temperatures and compensatory growth by tiger swallowtail butterfly larvae. Holarctic Lepidoptera 7: 39-44. (in press)
- Thomas C.D. Bodsworth E.J., Wilson R.J., Simmons A.D., Davies Z.G., Musche M. & Conradt L. 2001: Ecological and evolutionary processes at expanding range margins. Nature 411: 577-581
Go to original source... - Thompson J.N. 1988: Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol. Exp. Appl. 47: 3-14
Go to original source... - Thompson T.N. 1996: Trade-offs in larval performance on normal and novel hosts. Entomol. Exp. Appl. 80: 133-139
Go to original source... - Tidwell P. 1995: Latitudinal Comparisons of Diapause Induction between Populations of Papilio glaucus and Papilio troilus (Lepidoptera: Papilionidae). MS Thesis, Michigan State Univ. East Lansing, MI, 80 pp
- Valella P. & Scriber J.M. 2002: Latitudinal variation in photoperiodic induction of pupal diapause in the spicebush swallowtail butterfly, Papilio troilus. Holarctic Lepidoptera 8: 37-41. (in press)
- Warren M.S., Hill J.K., Thomas J.A., Asher J., Fox R., Huntley B., Roy D.B., Telfer M.G., Jeffcoate S., Harding P., Jeffcoate G., Wills S.G., Greatorex-Davies J.N., Moss D. & Thomas C.D. 2001: Rapid responses of British butterflies to opposing forces of climate and habitat change. Nature 414: 65-69
Go to original source... - Wiklund C., Wickman P.-O. & Nylin S. 1992: A sex difference in the propensity to enter direct/diapause development: a result of selection for protandry. Evolution 46: 519-528
Go to original source... - Wood T.K., Olmstead K.L. & Guttman S.I. 1990: Insect phenology mediated by host-plant water relations. Evolution 44: 629-636
Go to original source... - Yamaga Y. & Ohgushi T. 1999: Preference-performance linkage in a herbivorous lady beetle; consequences of variability of natural enemies. Oecologia 119: 183-190
Go to original source... - Zalucki M.P., Clarke A.R. & Malcolm S.B. 2002: Ecology and behavior of first instar larval Lepidoptera. Annu. Rev. Entomol. 47: 361-393
Go to original source...
This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.




