Sex chromosome mosaicism and hybrid speciation among tiger swallowtail butterflies

Krushnamegh Kunte, Cristina Shea, Matthew Aardema, J. Mark Scriber, Thomas E. Juenger, Lawrence E. Gilbert, Marcus R. Kronforst

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Hybrid speciation, or the formation of a daughter species due to interbreeding between two parental species, is a potentially important means of diversification, because it generates new forms from existing variation. However, factors responsible for the origin and maintenance of hybrid species are largely unknown. Here we show that the North American butterfly Papilio appalachiensis is a hybrid species, with genomic admixture from Papilio glaucus and Papilio canadensis. Papilio appalachiensis has a mosaic phenotype, which is hypothesized to be the result of combining sex-linked traits from P. glaucus and P. canadensis. We show that P. appalachiensis' Z-linked genes associated with a cooler thermal habitat were inherited from P. canadensis, whereas its W-linked mimicry and mitochondrial DNA were inherited from P. glaucus. Furthermore, genome-wide AFLP markers showed nearly equal contributions from each parental species in the origin of P. appalachiensis, indicating that it formed from a burst of hybridization between the parental species, with little subsequent backcrossing. However, analyses of genetic differentiation, clustering, and polymorphism based on molecular data also showed that P. appalachiensis is genetically distinct from both parental species. Population genetic simulations revealed P. appalachiensis to be much younger than the parental species, with unidirectional gene flow from P. glaucus and P. canadensis into P. appalachiensis. Finally, phylogenetic analyses, combined with ancestral state reconstruction, showed that the two traits that define P. appalachiensis' mosaic phenotype, obligatory pupal diapause and mimicry, evolved uniquely in P. canadensis and P. glaucus, respectively, and were then recombined through hybridization to form P. appalachiensis. These results suggest that natural selection and sex-linked traits may have played an important role in the origin and maintenance of P. appalachiensis as a hybrid species. In particular, ecological barriers associated with a steep thermal cline appear to maintain the distinct, mosaic genome of P. appalachiensis despite contact and occasional hybridization with both parental species.

Original languageEnglish
Article numbere1002274
JournalPLoS Genetics
Volume7
Issue number9
DOIs
StatePublished - 1 Sep 2011

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Papilio glaucus
Papilionidae
Butterflies
Sex Chromosomes
Mosaicism
sex chromosomes
butterfly
chromosome
Papilio
hybridization
Hot Temperature
Maintenance
Genome
Phenotype
Inbreeding
Gene Flow
Genetic Selection
Population Genetics
heat
phenotype

Cite this

Kunte, K., Shea, C., Aardema, M., Scriber, J. M., Juenger, T. E., Gilbert, L. E., & Kronforst, M. R. (2011). Sex chromosome mosaicism and hybrid speciation among tiger swallowtail butterflies. PLoS Genetics, 7(9), [e1002274]. https://doi.org/10.1371/journal.pgen.1002274
Kunte, Krushnamegh ; Shea, Cristina ; Aardema, Matthew ; Scriber, J. Mark ; Juenger, Thomas E. ; Gilbert, Lawrence E. ; Kronforst, Marcus R. / Sex chromosome mosaicism and hybrid speciation among tiger swallowtail butterflies. In: PLoS Genetics. 2011 ; Vol. 7, No. 9.
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abstract = "Hybrid speciation, or the formation of a daughter species due to interbreeding between two parental species, is a potentially important means of diversification, because it generates new forms from existing variation. However, factors responsible for the origin and maintenance of hybrid species are largely unknown. Here we show that the North American butterfly Papilio appalachiensis is a hybrid species, with genomic admixture from Papilio glaucus and Papilio canadensis. Papilio appalachiensis has a mosaic phenotype, which is hypothesized to be the result of combining sex-linked traits from P. glaucus and P. canadensis. We show that P. appalachiensis' Z-linked genes associated with a cooler thermal habitat were inherited from P. canadensis, whereas its W-linked mimicry and mitochondrial DNA were inherited from P. glaucus. Furthermore, genome-wide AFLP markers showed nearly equal contributions from each parental species in the origin of P. appalachiensis, indicating that it formed from a burst of hybridization between the parental species, with little subsequent backcrossing. However, analyses of genetic differentiation, clustering, and polymorphism based on molecular data also showed that P. appalachiensis is genetically distinct from both parental species. Population genetic simulations revealed P. appalachiensis to be much younger than the parental species, with unidirectional gene flow from P. glaucus and P. canadensis into P. appalachiensis. Finally, phylogenetic analyses, combined with ancestral state reconstruction, showed that the two traits that define P. appalachiensis' mosaic phenotype, obligatory pupal diapause and mimicry, evolved uniquely in P. canadensis and P. glaucus, respectively, and were then recombined through hybridization to form P. appalachiensis. These results suggest that natural selection and sex-linked traits may have played an important role in the origin and maintenance of P. appalachiensis as a hybrid species. In particular, ecological barriers associated with a steep thermal cline appear to maintain the distinct, mosaic genome of P. appalachiensis despite contact and occasional hybridization with both parental species.",
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Kunte, K, Shea, C, Aardema, M, Scriber, JM, Juenger, TE, Gilbert, LE & Kronforst, MR 2011, 'Sex chromosome mosaicism and hybrid speciation among tiger swallowtail butterflies', PLoS Genetics, vol. 7, no. 9, e1002274. https://doi.org/10.1371/journal.pgen.1002274

Sex chromosome mosaicism and hybrid speciation among tiger swallowtail butterflies. / Kunte, Krushnamegh; Shea, Cristina; Aardema, Matthew; Scriber, J. Mark; Juenger, Thomas E.; Gilbert, Lawrence E.; Kronforst, Marcus R.

In: PLoS Genetics, Vol. 7, No. 9, e1002274, 01.09.2011.

Research output: Contribution to journalArticleResearchpeer-review

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