Skip to main content
SpringerLink
Log in

Allochronic isolation and incipient hybrid speciation in tiger swallowtail butterflies

  • Global change ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Hybridization leading to reproductively isolated, novel genotypes is poorly understood as a means of speciation and few empirical examples have been studied. In 1999, a previously non-existent delayed flight of what appeared to be the Canadian tiger swallowtail butterfly, Papilio canadensis, was observed in the Battenkill River Valley, USA. Allozyme frequencies and morphology suggest that this delayed flight was the product of hybridization between Papilio canadensis and its sibling species Papilio glaucus. The mitochondrial DNA (mtDNA) restriction fragment length polymorphisms presented here indicate that only P. canadensis-like mtDNA occurs in this population, suggesting that introgression likely occurred from hybrid males mating with P. canadensis females. Preliminary studies of this population indicated that delayed post-diapause pupal emergence in this hybrid genotype was the root cause behind the observed delayed flight, which suggests a potential empirical example of a mechanism leading to reproductive isolation. Here we provide further evidence of the role of adult pupal emergence as a reproductive barrier likely leading to reproductive isolation. In particular, we present results from pupal emergence studies using four different spring and two different winter temperature treatments. The results indicate a clear separation of adult emergences between the hybrid population and both parental species. However, our results indicate that exceptionally hot springs are likely to lead to greater potential for overlap between the local parental species, P. canadensis, and this delayed population with hybrid origins. Conversely, our results also show that warmer winters are likely to increase the temporal separation of the hybrid population and the parental species. Finally, we report recently collected evidence that this hybrid population remains morphologically distinct.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abbot P, Withgott JH (2004) Phylogenetic and molecular evidence for allochronic speciation in gall-forming aphids (Pemphigus). Evolution 58:539–553

    CAS  PubMed  Google Scholar 

  • Abrahamson WG, Blair CP (2008) Sequential radiation through host-race formation: herbivore diversity leads to diversity in natural enemies. In: Tilmon KJ (ed) Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects. University of California Press, Berkley, pp 188–202

    Google Scholar 

  • Alexander RD, Bigelow RS (1960) Allochronic speciation in field crickets and a new species, Acheta veletis. Evolution 14:334–346

    Article  Google Scholar 

  • Andolfatto P, Scriber JM, Charlesworth B (2003) No association between mitochondrial DNA haplotypes and a female-limited mimicry phenotype in Papilio glaucus. Evolution 57:305–316

    CAS  PubMed  Google Scholar 

  • Berlocher SH, Feder JL (2002) Sympatric speciation in phytophagous insects: moving beyond controversy? Annu Rev Entomol 47:773–815

    Article  CAS  PubMed  Google Scholar 

  • Blair CP, Abrahamson WG, Jackman JA, Tyrrell L (2005) Cryptic speciation and host race formation in a purportedly generalist tumbling flower beetle. Evolution 59:304–316

    PubMed  Google Scholar 

  • Bush GL (1994) Sympatric speciation in animals: new wine in old bottles. Trends Ecol Evol 9:285–288

    Article  Google Scholar 

  • Carling MD, Brumfield RT (2009) Haldane’s rule in an avian system: using cline theory and divergence population genetics to test for differential introgression of mitochondrial, autosomal, and sex-linked loci across the passerine bunting hybrid zone. Evolution 10:2600–2615

    Google Scholar 

  • Carroll SP, Boyd C (1992) Host race radiation in the soapberry bug: natural history with the history. Evolution 46:1052–1069

    Article  Google Scholar 

  • Caterino MS, Sperling FAH (1999) Papilio phylogeny based on mitochondrial cytochrome oxidase I and II genes. Mol Phylogenet Evol 11:122–137

    Article  CAS  PubMed  Google Scholar 

  • Cooley JR, Simon CS, Marshall DC, Slon K, Ehrhardt C (2001) Allochronic speciation, secondary contact, and reproductive character displacement in periodical cicadas (Hemiptera: Magicicada spp.): genetic, morphological, and behavioural evidence. Mol Ecol 10:661–671

    Article  CAS  PubMed  Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinauer, Sunderland

    Google Scholar 

  • Dopman EB, Perez L, Bogdanowicz SM, Harrison RG (2005) Consequences of reproductive barriers for genealogical discordance in the European corn borer. Proc Natl Acad Sci USA 102:14706–14711

    Article  CAS  PubMed  Google Scholar 

  • Dowling TE, Secor CL (1997) The role of hybridization and introgression in the diversification of animals. Annu Rev Ecol Syst 28:593–619

    Article  Google Scholar 

  • Eckenrode CJ, Robbins PS, Andaloro JT (1983) Variations in flight patterns of European corn borer (Lepidoptera: Pyralidae) in New York. Environ Entomol 12:393–396

    Google Scholar 

  • Emalianov I, Simpson F, Narang P, Mallet J (2003) Host choice promotes reproductive isolation between host races of the larch budmoth, Zeiraphera diniana. J Evol Biol 16:208–218

    Article  Google Scholar 

  • Feder JL, Roethele JB, Filchak K, Niedbalski J, Romero-Severson J (2003) Evidence for inversion polymorphism related to sympatric host race formation in the apple maggot fly, Rhagoletis pomonella. Genetics 163:939–954

    CAS  PubMed  Google Scholar 

  • Forbes AA, Powell THQ, Stelinski LL, Smith JJ, Feder JL (2009) Sequential speciation across trophic levels. Science 323:776–779

    Article  CAS  PubMed  Google Scholar 

  • Funk DJ, Nosil P (2008) Comparative analyses of ecological speciation. In: Tilmon KJ (ed) Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects. University of California Press, Berkeley, pp 117–135

    Google Scholar 

  • Futuyma DJ (2008) Ecology, speciation, and adaptive radiation: the long view. Evolution 62(9):2446–2449

    Article  Google Scholar 

  • Glover TJ, Robbins PS, Eckenrode CJ, Roelofs WL (1992) Genetic control of voltinism characteristics in European corn borer races assessed with a marker gene. Arch Insect Biochem 20:107–117

    Article  CAS  Google Scholar 

  • Gompert Z, Fordyce JA, Forister ML, Shapiro AM, Nice CC (2006) Homoploid hybrid speciation in an extreme habitat. Science 314:1923–1925

    Article  CAS  PubMed  Google Scholar 

  • Gompert Z, Forister ML, Fordyce JA, Nice CC (2008) Widespread mito-nuclear discordance with evidence for introgressive hybridization ands selective sweeps in Lycaedes. Mol Ecol 17:5231–5244

    Article  CAS  PubMed  Google Scholar 

  • Hagen RH, Lederhouse RC (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

    Article  Google Scholar 

  • Hagen RH, Scriber JM (1989) Sex linked diapause, color, and allozyme loci in Papilio glaucus: linkage analysis and significance in a hybrid zone. Heredity 80:179–185

    Google Scholar 

  • Hagen RH, Lederhouse RC, Bossart JL, Scriber JM (1991) Papilio canadensis and P. glaucus (Papilionidae) are distinct species. J Lep Soc 45:245–258

    Google Scholar 

  • Harrison RG, Bogdanowicz SM (1995) Mitochondrial DNA phylogeny of North American field crickets: perspectives on the evolution of life cycles, songs, and habitat associations. J Evol Biol 8:209–232

    Article  CAS  Google Scholar 

  • Lederhouse RC, Ayres MP, Scriber JM (1990) Adult nutrition affects male virility in Papilio glaucus L. Ecology 72:1428–1435

    Google Scholar 

  • Luebke HJ, Scriber JM, Yandell BS (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 Nat 119:366–379

    Article  Google Scholar 

  • Mavarez J, Salazar CA, Bermingham E, Salcedo C, Jiggins CD, Linares M (2006) Speciation by hybridization in Heliconius butterflies. Nature 441:868–871

    Article  CAS  PubMed  Google Scholar 

  • McMillan WO, Jiggins CD, Mallet J (1997) What initiates speciation in passion-vine butterflies? Proc Natl Acad Sci USA 94:8628–8633

    Article  CAS  PubMed  Google Scholar 

  • Mercader RJ, Scriber JM (2007) Diversification of host use in two polyphagous butterflies: differences in oviposition specificity or host rank hierarchy? Entomol Exp Appl 125:89–101

    Article  Google Scholar 

  • Mercader RJ, Scriber JM (2008) Asymmetrical thermal constraints on the parapatric species boundaries of two widespread generalist butterflies. Ecol Entomol 33:537–545

    Article  Google Scholar 

  • Mercader RJ, Aardema ML, Scriber JM (2009) Hybridization leads to host use divergence in a polyphagous butterfly sibling species pair. Oecologia 158:65–662

    Article  Google Scholar 

  • Morbey YE, Ydenberg RC (2001) Protandrous arrival timing to breeding areas: a review. Ecol Lett 4:663–673

    Article  Google Scholar 

  • Mullen SP, Dopman EB, Harrison RG (2008) Hybrid zone origins, species boundaries, and the evolution of wing-pattern diversity in a polytypic species complex of North American Admiral butterflies (Nymphalidae: Limenitis). Evolution 62:1401–1417

    Google Scholar 

  • Nosil P, Vines TH, Funk DJ (2005) Perspective: reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59:705–719

    PubMed  Google Scholar 

  • Nosil P, Funk DJ, Ortiz-Barrientos D (2009) Divergent selection and heterogeneous genomic divergence. Mol Ecol 18:375–402

    Article  PubMed  Google Scholar 

  • Ording GJ (2008) An analysis of climate induced hybrid speciation in tiger swallowtail butterflies (Papilio). PhD dissertation, Michigan State University

  • Pavulaan H, Wright DM (2002) Pterourus appalachiensis (Papilionidae: Papilioninae), a new swallowtail butterfly from the Appalachian region of the United States. Taxonomic Rep 3:1–20

    Google Scholar 

  • Putnam AS, Scriber JM, Andolfatto P (2007) Discordant divergence times among Z chromosome regions between two ecologically distinct swallowtail butterfly species. Evolution 61:912–927

    Article  CAS  PubMed  Google Scholar 

  • Rockey SJ, Hainze JH, Scriber JM (1987) Evidence of a sex-linked diapause response in Papilio glaucus subspecies and their hybrids. Physiol Entomol 12:181–184

    Article  Google Scholar 

  • Roelofs W, Glover T, Tang XH, Streng I, Robbins P, Eckenrode C, Lofstedt C, Bengtsson B (1987) Sex pheromone production and perception in European corn borer moths is determined by both autosomal and sex-linked genes. Proc Natl Acad Sci USA 84:7585–7589

    Article  CAS  PubMed  Google Scholar 

  • Roelofs WL, Liu W, Hao G, Jiao H, Rooney AP, Linn CE Jr (2002) Evolution of moth sex pheromones via ancestral genes. Proc Natl Acad Sci USA 99:13621–13626

    Article  CAS  PubMed  Google Scholar 

  • Rothschild W, Jordan K (1906) A revision of the American Papilios. Nov Zool 13:411–752

    Google Scholar 

  • Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8:336–352

    Article  Google Scholar 

  • Santos H, Rousselet J, Magnoux E, Paiva MR, Branco M, Kerdelhue C (2007) Genetic isolation through time: allochronic differentiation of a phenotypically atypical population of the pine processionary moth. Proc R Soc Lond Ser B 274:935–941

    Article  CAS  Google Scholar 

  • Schwarz D, Matta BJ, Shakir-Botteri NL, McPheron BA (2005) Host shift to an invasive plant triggers rapid animal hybrid speciation. Nature 436:546–549

    Article  CAS  PubMed  Google Scholar 

  • Schwartz MD, Ahas R, Aasa A (2006) Onset of spring starting earlier across the Northern Hemisphere. Glob Change Biol 12:343–351

    Article  Google Scholar 

  • Schwarz D, Shoemaker KD, Botteri NL, McPheron BA (2007) A novel preference for an invasive plant as a mechanism for animal hybrid speciation. Evolution 61:245–256

    Article  PubMed  Google Scholar 

  • Scriber JM (1982) Food plants and speciation in the Papilio glaucus group. In: Visser JH, Minks AK (eds) Proceedings of the 5th international symposium on insect plant relationships, PUDOC, Wageningen, pp 307–314

  • Scriber JM (1990) Interaction of introgression from Papilio glaucus canadensis and diapause in producing ‘spring form’ Eastern tiger swallowtail butterflies, P. glaucus. Gt Lakes Entomol 23:127–138

    Google Scholar 

  • Scriber JM (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 HV (ed) 1. Insect life-cycle polymorphism: theory, evolution and ecological consequences for seasonality and diapause control. Kluwer, Dordrecht, pp 17–133

  • Scriber JM, Lederhouse RC (1992) The thermal environment as a resource dictating geographic patterns of feeding specialization of insect herbivores. In: Hunter MR, Ohgushi T, Price PW (eds) Effects of resource distribution on animal-plant interactions. Academic Press, New York, pp 429–466

    Google Scholar 

  • Scriber JM, Ording GJ (2005) Ecological speciation without host plant specialization: possible origins of a recently described cryptic Papilio species (Lepidoptera: Papilionidae). Entomol Exp Appl 115:247–263

    Article  Google Scholar 

  • Scriber JM, Giebink BL, 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

    Article  Google Scholar 

  • Scriber JM, Hagen RH, Lederhouse RC (1996) Genetics of mimicry in the tiger swallowtail butterflies, Papilio glaucus and P. canadensis. (Lepidoptera: Papilionidae). Evolution 50:222–236

    Article  Google Scholar 

  • Scriber JM, Stump A, Deering M (2003) Hybrid zone ecology and tiger swallowtail trait clines in North America. In: Boggs C, Watt W, Ehrlich P (eds) Ecology and evolution taking flight: butterflies as model study systems. University of Chicago Press, Chicago, USA, pp 367–391

    Google Scholar 

  • Scriber JM, Ording GJ, Mercader RJ (2008) Hybrid introgression and parapatric speciation in a hybrid zone. In: Tilmon KJ (ed) Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects. University of California Press, Berkeley, pp 69–87

    Google Scholar 

  • Seehausen O (2004a) Hybridization and adaptive radiation. Trends Ecol Evol 19:198–207

    Article  PubMed  Google Scholar 

  • Seehausen O (2004b) Response to Schilthuizen et al.: Hybridization, rare alleles, and adaptive radiation. Trends Ecol Evol 19:405–406

    Article  Google Scholar 

  • Simon C, Jiaming T, Dalwadi S, Gregory S, Deniega J, Unuaschi T (2000) Genetic evidence for assortative mating between 13-year cicadas and sympatric “17-year cicadas with 13 year life cycles” provides support for allochronic speciation. Evolution 54:1326–1336

    CAS  PubMed  Google Scholar 

  • Sperling FAH, Hickey DA (1995) Amplified mitochondrial DNA as a diagnostic marker for species of conifer-feeding Choristoneura (Lepidoptera: Tortricidae). Can Entomol 127:277–288

    Article  Google Scholar 

  • Stump AD, Sperling FAH, Crim A, Scriber JM (2003) Gene flow between great lakes region populations of the Canadian tiger swallowtail butterfly, Papilio canadensis, near the hybrid zone with P. glaucus (Lepidoptera: Papiliondiae). Gt Lakes Entomol 36:41–53

    Google Scholar 

  • Tauber CA, Tauber MJ, Nechols JR (1977) Two genes control seasonal isolation in sibling species. Science 197:592–593

    Article  PubMed  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna (ISBN 3-900051-07-0)

  • Thomas Y, Bethenod MT, Pelozuelo L, Frérot B, Bourguet D (2003) Genetic isolation between two sympatric host-plantraces of the European corn borer, Ostrinia nubilalis Hübner. I. Sex pheromone, moth emergence timing, and parasitism. Evolution 57:261–273

    PubMed  Google Scholar 

  • Via S, Hawthorne DJ (2002) Genetic architecture of ecological specialization and incipient speciation in divergent races of pea aphids. Am Nat 159:S76–S88

    Article  PubMed  Google Scholar 

  • Vines TH, Schluter D (2006) Strong assortative mating between allopatric sticklebacks as a byproduct of adaptation to different environments. Proc R Soc Lond Ser B 273:911–916

    Article  Google Scholar 

  • Wiklund C (2003) Sexual selection and the evolution of butterfly mating systems. In: Boggs CL, Watt WB, Ehrlich PR (eds) Butterflies: ecology and evolution taking flight. University of Chicago Press, Chicago, pp 67–90

    Google Scholar 

  • Wood TK, Keese M (1990) Host-plant-induced assortative mating in Enchenopa treehoppers. Evolution 44:619–628

    Article  Google Scholar 

  • Wood TK, Tilmon KJ, Shantz AB, Harris CK, Pesek J (1999) The role of host plant fidelity in initiating insect race formation. Evol Ecol Res 1:317–332

    Google Scholar 

  • Xie X, Rull J, Michel AP, Velez S, Forbes AA, Lobo NL, Aluja M, Feder JL (2007) Hawthorne infesting populations of Rhagoletis pomonella in Mexico and speciation mode plurality. Evolution 61:1091–1105

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported in part by the College of Natural Science and the Michigan Agricultural Experiment Station (project no. 1644), and the National Science Foundation (DEB-0716683). Thanks are extended to various students and research assistants, including Mark and Jessica Deering, Jen Donovan, Barb Gary, Holly Hereau, Angeline Kosnik, Matt Lehnert, Emily Maher, Michelle Oberlin, Laura Palombi, and Aram Stump. Special thanks to Bill Houtz, James Maudsley, Howard Romack, Harry Pavulaan and David Wright for providing eastern specimens. Drs Jim Smith and Jessica Hellmann provided guidance and lab facilities for mtDNA analyses. Matthew Aardema was supported in part by a Scriber Scholars award in Butterfly Biology and Conservation [Department of Entomology, Michigan State University (MSU)], an MSU Plant Sciences Fellowship, and an National Science Foundation (NSF) research experience for undergraduates (NSF-REU, DEB-0821958) award.

Author information

Authors and Affiliations

  1. Department of Entomology, Michigan State University, 243 Natural Sciences Building, East Lansing, MI, 48824, USA

    Gabriel James Ording, Rodrigo J. Mercader, Matthew L. Aardema & J. M. Scriber

  2. Center for Integrative Studies, General Science, Michigan State University, 334 N Kedzie Hall, East Lansing, MI, 48824-1311, USA

    Gabriel James Ording

Authors
  1. Gabriel James Ording
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rodrigo J. Mercader
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matthew L. Aardema
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. M. Scriber
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gabriel James Ording.

Additional information

Communicated by Matthias Schaefer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ording, G.J., Mercader, R.J., Aardema, M.L. et al. Allochronic isolation and incipient hybrid speciation in tiger swallowtail butterflies. Oecologia 162, 523–531 (2010). https://doi.org/10.1007/s00442-009-1493-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-009-1493-8

Keywords

Search

Navigation