Skip to main content Skip to main navigation menu Skip to site footer
Type: Monograph
Published: 2018-10-12
Page range: 1–87
Abstract views: 216
PDF downloaded: 73

Alternative facts: a reconsideration of putatively natural interspecific hybrid specimens in the genus Heliconius (Lepidoptera: Nymphalidae)

Evolution and Ecology Group, Department of Biology, Middle Tennessee State University, Murfreesboro, TN 37132 USA.
Lepidoptera hybridization introgression gene flow species boundary hybrid speciation

Abstract

Mallet et al. (2007 BMC Evolutionary Biology, 7, 28) employed a database of putative interspecific hybrid specimens of the genus Heliconius to advance a hypothesis of "the species boundary as a continuum." Here, each of those specimens, as well as subsequently documented specimens, is individually reassessed regarding its phenotype, potential parentage and chain of custody in collections. Using a quantified scale of reliability, most of the specimens are interpreted differently than Mallet et al.'s identifications, and the actual number of interspecific hybrids is estimated to be much smaller than they proposed. To be specific, of 163 putative hybrid specimens examined, 11% suffered from ambiguous identity, 5% from confounding issues with their data labels, 50% were arguably intraspecific (depending upon alternative species concepts), and 22% were almost certainly reared, commercial specimens. Only eleven of the specimens meet the criteria established here to be legitimate and reliable interspecific hybrids, and all of those are between closely-related species. This result has potentially important implications for current hypotheses of frequent genomic introgression of wing pattern alleles among Heliconius clades.

 

References

  1. Ackery, P.R. & Smiles, R.L. (1976) An illustrated list of the type-specimens of the Heliconiinae (Lepidoptera: Nymphalidae) in the British Museum (Natural History). Bulletin of the British Museum (Natural History) Entomology, 32, 171–214.

    Arias, C.F., Giraldo, N., McMillan, W.O., Lamas M., G., Jiggins, C.D. & Salazar, C. (2017) A new subspecies in a Heliconius butterfly adaptive radiation (Lepidoptera: Nymphalidae). Zoological Journal of the Linnean Society, 180, 805–818.
    https://doi.org/10.1093/zoolinnean/zlw010

    Arias, C.F., Salazar, C., Rosales, C., Kronforst, M.R., Linares, M., Bermingham, E. & McMillan, W.O. (2014) Phylogeography of Heliconius cydno and its closest relatives: disentangling their origin and diversification. Molecular Ecology, 23, 4137–4152.
    https://doi.org/10.1111/mec.12844

    Aspöck, H. (1996 [1997]) Ruth Holzinger 1921-1995. Zeitschrift der Arbeisgemeinschaft Österreichischer Entomologen 48, 65–72.

    Bates, H.W. (1862) Contributions to an insect fauna of the Amazon Valley. Lepidoptera: Heliconidae. Transactions of the Linnean Society, 23, 495–566.

    Beltrán, M., Jiggins, C.D., Brower, A.V.Z., Bermingham, E. & Mallet, J. (2007) Do pollen feeding, pupal-mating and larval gregariousness have a single origin in Heliconius butterflies? Inferences from multilocus DNA sequence data. Biological Journal of the Linnean Society, 92, 221–239.
    https://doi.org/10.1111/j.1095-8312.2007.00830.x

    Brower, A.V.Z. (1994a) Phylogeny of Heliconius butterflies inferred from mitochondrial DNA sequences (Lepidoptera: Nymphalidae). Molecular Phylogenetics and Evolution, 3, 159–174.
    https://doi.org/10.1006/mpev.1994.1018

    Brower, A.V.Z. (1994b) Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proceedings of the National Academy of Sciences, USA, 91, 6491–6495.
    https://doi.org/10.1073/pnas.91.14.6491

    Brower, A.V.Z. (1996a) Parallel race formation and the evolution of mimicry in Heliconius butterflies: a phylogenetic hypothesis from mitochondrial DNA sequences. Evolution, 50, 195–221.
    https://doi.org/10.1111/j.1558-5646.1996.tb04486.x

    Brower, A.V.Z. (1996b) A new mimetic species of Heliconius (Lepidoptera: Nymphalidae), from southeastern Colombia, as revealed by cladistic analysis of mitochondrial DNA sequences. Zoological Journal of the Linnean Society, 116, 317–332.
    https://doi.org/10.1111/j.1096-3642.1996.tb00126.x

    Brower, A.V.Z. (2000) On the validity of Heliconius tristero and Heliconius melpomene mocoa Brower, with notes on species concepts in Heliconius Kluk (Lepidoptera: Nymphalidae). Proceedings of the Entomological Society of Washington, 102, 678–687.

    Brower, A.V.Z. (2011) Hybrid speciation in Heliconius butterflies? A review and critique of the evidence. Genetica, 139, 589–609.
    https://doi.org/10.1007/s10709-010-9530-4

    Brower, A.V.Z. (2013) Introgression of wing pattern alleles and speciation via homoploid hybridization in Heliconius butterflies: a review of evidence from the genome. Proceedings of the Royal Society of London B 280, 20122302.
    https://doi.org/10.1098/rspb.2012.2302

    Brower, A.V.Z. & Egan, M.G. (1997) Cladistics of Heliconius butterflies and relatives (Nymphalidae: Heliconiiti): the phylogenetic position of Eueides based on sequences from mtDNA and a nuclear gene. Proceedings of the Royal Society of London B, 264, 969–977.
    https://doi.org/10.1098/rspb.1997.0134

    Brower, A.V.Z. & Garzón-Orduña, I.J. (2018) Missing data, clade support and "reticulation": the molecular systematics of Heliconius and related genera (Lepidoptera: Nymphalidae) re-examined. Cladistics, 34, 151–166.
    https://doi.org/10.1111/cla.12198

    Brown, K.S. Jr. (1976) An illustrated key to the silvaniform Heliconius (Lepidoptera: Nymphalidae) with descriptions of new subspecies. Transactions of the American Entomological Society, 102, 373–483.

    Brown, K.S. Jr. (1979) Ecologia Geográfica e Evolução nas Florestas Neotropicais. Universidade Estadual de Campinas, Campinas, xxxi + 260 +120 pp.

    Brown, K.S. Jr. (1981) The biology of Heliconius and related genera. Annual Reviews of Entomology, 26, 427–456.
    https://doi.org/10.1146/annurev.en.26.010181.002235

    Brown, K.S. Jr. & Fernández Yepez, F. (1985) Los Heliconii (Lepidoptera, Nymphalidae) de Venezuela. Boletín Entomologica de Venezuela., New Series, 3, 29–76.

    Cast, M. & Le Crom, J.-F. (2012) Heliconius melpomene dans le valée de la Magdalena (Colombie): Révision et desciption d'une nouvelle sous-espèce polymporphique Heliconius melpomene martinae nova ssp. (Lepidoptera: Nymphalidae; Heliconiinae). Lépidoptères—Revue des Lépidoptéristes de France, 21, 96–101.

    Coyne, J.A. & Orr, H.A. (2004) Speciation. Sinauer Associates, Sunderland, MA, 545 pp.

    Dasmahapatra, K.K., Silva-Vasquez, A., Chung, J.W. & Mallet, J. (2007) Genetic analysis of a wild-caught hybrid between non-sister Heliconius butterfly species. Biology Letters (Royal Society), 3, 660–663.
    https://doi.org/10.1098/rsbl.2007.0401

    Eltringham, H. (1916) On specific and mimetic relationships in the genus Heliconius, L. Transactions of the Entomological Society of London, 1916, 101–148.
    https://doi.org/10.1111/j.1365-2311.1916.tb03123.x

    Enciso-Romero, J., Pardo-Díaz, C., Martin, S.H., Arias, C.F., Linares, M., McMillan, W.O., Jiggins, C.D. & Salazar, C.A. (2017) Evolution of novel mimicry rings facilitated by adaptive introgression in tropical butterflies. Molecular Ecology, 26, 5160–5172.
    https://doi.org/10.1111/mec.14277

    Garzón-Orduña, I.J. & Brower, A.V.Z. (2018) Quantified reproductive isolation in Heliconius butterflies: implications for introgression and hybrid speciation. Ecology and Evolution 3, 1186–1195.
    https://doi.org/10.1002/ece3.3729

    Gilbert, L.E. (2003) Adaptive novelty through introgression in Heliconius wing patterns: evidence for a shared genetic "tool box" from synthetic hybrid zones and a theory of diversification. In: Boggs, C.L., Watt, W.B. & Ehrlich, P.R. (Eds.), Butterflies: Ecology and evolution taking flight. University of Chicago Press, Chicago, pp. 281–318.

    Giraldo, N., Salazar, C.A., Jiggins, C.D., Bermingham, E., & Linares, M. 2008. Two sisters in the same dress: Heliconius cryptic species. BMC Evolutionary Biology, 8, 324.
    https://doi.org/10.1186/1471-2148-1188-1324.

    Hines, H.M., Counterman, B.A., Papa, R., Albuquerque de Moura, P., Cardoso, M.Z., Linares, M., Mallet, J., Reed, R.D., Jiggins, C.D., Kronforst, M.R. & McMillan, W.O. (2011) Wing patterning gene redefines the mimetic history of Heliconius butterflies. Proceedings of the National Academy of Sciences, USA, 108, 19666–19671 and supplements.
    https://doi.org/10.1073/pnas.1110096108

    Holzinger, H. & Holzinger, R. (1968) Heliconius cydno gerstneri, n. ssp. und zwei neue Formen von H. cydno cydnides Stgr. (Lep., Nymph.). Zeitschrift der Arbeitsgemeinschaft Österreich Entomologen, 20, 17–21.

    International Commission on Zoological Nomenclature (1999) International Code of Zoological Nomenclature. International Trust for Zoological Nomenclature and the British Museum (Natural History), London, xxix + 306 pp.

    Jiggins, C.D. (2017) The ecology and evolution of Heliconius butterflies. Oxford University Press, Oxford, 277 pp.

    Jiggins, C.D., Mávarez, J., Beltrán, M., McMillan, W.O., Johnston, J.S. & Bermingham, E. (2005) A genetic linkage map of the mimetic butterfly Heliconius melpomene. Genetics, 171, 557–570.
    https://doi.org/10.1534/genetics.104.034686

    Jiggins, C.D., McMillan, W.O., Neukirchen, W. & Mallet, J. (1996) What can hybrid zones tell us about speciation? The case of Heliconius erato and H. himera (Lepidoptera: Nymphalidae). Biological Journal of the Linnean Society, 59, 221–242.
    https://doi.org/10.1006/bijl.1996.0063

    Johnson, K. & Matusik, D. (1986) A new white-and-black subspecies of Protesilaus euryleon (Papilionidae). Journal of the Lepidopterists' Society, 41, 70–74.

    Kapan, D.D. (2001) Three-butterfly system provides a field test of Müllerian mimicry. Nature, 409, 338–340.
    https://doi.org/10.1038/35053066

    König, F. (1986) Ein Heliconius erato himera-Hybrid aus Nord-Peru (Lepidoptera, Heliconiinae). Zeitschrift Arbeitsgemeinschaft Österreich Entomologen, 38, 49–50.

    Kozak, K.M., Wahlberg, N., Neild, A.F.E., Dasmahapatra, K.K., Mallet, J. & Jiggins, C.D. (2015) Multilocus species trees show the recent adaptive radiation of the mimetic Heliconius butterflies. Systematic Biology, 64, 505–524.
    https://doi.org/10.1093/sysbio/syv007

    Kronforst, M.R., Young, L.G., Gilbert, L.E. (2007) Reinforcement of mate preference among hybridizing Heliconius butterflies. Journal of Evolutionary Biology, 20, 278–285.
    https://doi.org/10.1111/j.1420-9101.2006.01198.x

    Kronforst, M.R., Young, L.G., Blume, L.M. & Gilbert, L.E. 2006b. Multilocus analyses of admixture and introgression among hybridizing Heliconius butterflies. Evolution, 60, 1254–1268.
    https://doi.org/10.1111/j.0014-3820.2006.tb01203.x

    Kronforst, M.R., Young, L.G., Kapan, D.D., McNeely, C., O'Neill, R.J. & Gilbert, L.E. (2006a) Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless. Proceedings of the National Academy of Sciences, USA, 103, 6575–6580.
    https://doi.org/10.1073/pnas.0509685103

    Lamas, G. (1998) Comentarios taxonómicos y nomenclaturales sobre Heliconiini neotropicales con designación de lectotipos y descripción de cuatro subespecies nuevas (Lepidoptera: Nymphalidae: Heliconiinae). Revista Peruana de Entomologia, 40, 111–125.

    Lamas, G. (Ed.) (2004) Atlas of Neotropical Lepidoptera. Checklist: Part 4A Hesperioidea—Papilionoidea. Scientific Publishers/Association of Tropical Lepidoptera, Gainesville, xxxvi +439 pp.

    Lamas, G. & Jiggins, C.D. (2017) Taxonomic list. In: Jiggins, C.D. (Ed.), The ecology and evolution of Heliconius butterflies. Oxford University Press, Oxford, pp. 214–244.

    Linares, M. (1997) Origin of neotropical mimetic biodiversity from a three-way hybrid zone of Heliconius cydno butterflies. In: Ulrich, H. (Ed.), Tropical biodiversity and systematics. Proceedings of the International Symposium on Biodiversity and Systematics in Tropical Ecosystems, Bonn, 1994. Zoologisches Forschung Institut und Museum Alexander Koenig, Bonn, pp. 93–108.

    Lödl, M., Keber A. & Gaal, S. (1997) Die Heliconius-Sammlung von Ruth und Helmuth Holzinger—nunmehr integrierter Bestandteil der Lepidoptera-Sammlung des Naturhistorischen Museums Wien (Insecta: Lepidoptera: Nymphalidae: Heliconiinae). Entomologisches Nachrichtenblatt, New Series, 4, 1–6.

    Mallet, J. (1993) Speciation, raciation and color pattern evolution in Heliconius butterflies: evidence from hybrid zones. In Harrison, R.G. (Ed.), Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford, pp. 226–260

    Mallet, J. (1995) A species definition for the Modern Synthesis. Trends in Ecology and Evolution, 10, 294–298.
    https://doi.org/10.1016/0169-5347(95)90031-4

    Mallet, J. (2005) Hybridization as invasion of the genome. Trends in Ecology and Evolution, 20, 229–237.
    https://doi.org/10.1016/j.tree.2005.02.010

    Mallet, J. (2008) Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation. Philosophical Transactions of the Royal Society of London B, 363, 2971–2986.
    https://doi.org/10.1098/rstb.2008.0081

    Mallet, J. & Barton, N.H. (1989) Strong natural selection in a warning-color hybrid zone. Evolution 43, 421–431.
    https://doi.org/10.1111/j.1558-5646.1989.tb04237.x

    Mallet, J., Beltrán, M., Neukirchen, W. & Linares, M. (2007) Natural hybridization in heliconiine butterflies: the species boundary as a continuum. BMC Evolutionary Biology, 7, 28.
    https://doi.org/10.1186/1471-2148-7-28

    Mallet, J., Besansky, N.J. & Hahn, M.W. (2015) How reticulated are species? BioEssays, 38, 140–149.
    https://doi.org/10.1002/bies.201500149

    Mallet, J., McMillan, W.O. & Jiggins, C.D. (1998) Mimicry and warning color at the boundary between races and subspecies. In: Howard, D.J. & Berlocher, S.H. (Eds.), Endless forms. Oxford University Press, Oxford, pp. 390–403.

    Mávarez, J., Salazar, C.A., Bermingham, E., Salcedo, C., Jiggins, C.D. & Linares, M. (2006) Speciation by hybridization in Heliconius butterflies. Nature, 441, 868–871 + 811 supplementary pages.
    https://doi.org/ 10.1038/nature04738

    Mayr, E. (1942) Systematics and the Origin of Species. Columbia University Press, New York. 334 pp.

    de la Maza, R. (1991) Mariposas Mexicanas. 2nd Edition. Fondo de Cultura Económica S. A. de C. V., Mexico, D. F., 304 pp.

    Mazo-Vargas, A., Concha, C., Livraghi, L., Massardo, D., Wallbank, R.W.R., Zhang, L., Papador, J.D., Martinez-Najera, D., Jiggins, C.D., Kronforst, M.R., Breuker, C.J., Reed, R.D., Patel, N.H., McMillan, W.O. & Martin, A. (2017) Macroevolutionary shifts of WntA function potentiate butterfly wing-pattern diversity. Proceedings of the National Academy of Sciences, USA 114, 107021–10706.
    https://doi.org/10.1073/pnas.1708149114

    Mérot, C., Mávarez, J., Evin, A., Dasmahapatra, K.K., Mallet, J., Lamas, G. & Joron, M. (2013) Genetic differentiation without mimicry shift in a pair of hybridizing Heliconius species (Lepidoptera: Nymphalidae). Biological Journal of the Linnean Society, 109, 830–847.
    https://doi.org/10.1111/bij.12091

    Mérot, C., Salazar, C., Merrill, R.M., Jiggins, C.D. & Joron, M. (2017) What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies. Proceedings of the Royal Society of London B, 284, 20170335.
    https://doi.org/10.1098/rspb.2017.0335

    Nadeau, N.J., Whibley, A.C., Jones, R.T., Davey, J.W., Dasmahapatra, K.K., Baxter, S.W., Quail, M.A., Joron, M., ffrench-Constant, R.H., Blaxter, M.L., Mallet, J. & Jiggins, C.D. (2012) Genomic islands of divergence in hybridizing butterflies identified by large-scale targeted sequencing. Philosophical Transactions of the Royal Society of London B, 367, 343–353.
    https://doi.org/10.1098/rstb.2011.0198

    Naisbit, R.E., Jiggins, C.D. & Mallet, J. (2003) Mimicry: developmental genes that contribute to speciation. Evolution and Development, 5, 269–280.
    https://doi.org/10.1046/j.1525-142X.2003.03034.x

    Posla-Fuentes, M. (1993) Nueva forma de Heliconius cydno (Lepidoptera: Heliconidae) en el Río Sarapiquí, Costa Rica. Revista de Biologia Tropical, 41, 889–890.

    Posla-Fuentes, M. (1993) An unusual form of Heliconius cydno from Costa Rica (Lepidoptera: Nymphalidae: Heliconiinae). Tropical Lepidoptera, 4, 92.

    Poulton, E.B. (1890) The colours of animals. Kegan Paul, Trench, Trübner & Co., London, 360 pp.

    Punnett, R.C. (1915) Mimicry in butterflies. Cambridge University Press, Cambridge, 188 pp.

    Reed, R.D., Papa, R., Martin, A., Hines, H.M., Counterman, B.A., Pardo-Diaz, C., Jiggins, C.D., Chamberlain, N.L., Kronforst, M.R., Chen, R., Halder, G., Nijhout, H.F. & McMillan, W.O. (2011) optix drives the repeated convergent evolution of butterfly mimicry. Science, 333, 1137–1141.
    https://doi.org/10.1126/science.1208227

    Rosser, N., Phillimore, A.B., Huertas, B., Willmott, K.R. & Mallet J. (2012) Testing historical explanations for gradients in species richness in heliconiine butterflies of tropical America. Biological Journal of the Linnean Society, 105, 479–497.
    https://doi.org/10.1111/j.1095-8312.2011.01814.x

    Salazar, C.A., Jiggins, C.D., Taylor, J.E., Kronforst, M.R. & Linares, M. (2008) Gene flow and genealogical history of Heliconius heurippa. BMC Evolutionary Biology, 8, 132.
    https://doi.org/10.1186/1471-2148-8-132

    Salazar Escobar, J.A. (1993) Notes on some populations of Heliconius heurippa in Colombia (Lepidoptera: Nymphalidae: Heliconiinae). Tropical Lepidoptera, 4, 119–121.

    Schaus, W. (1913) New subspecies of Rhopalocera from Costa Rica. Proceedings of the Zoological Society of London, 1913, 339–367, pls. L–LIV.

    Sheppard, P.M., Turner, J.R.G., Brown, K.S. Jr., Benson, W.W. & Singer, M.C. (1985) Genetics and the evolution of Muellerian mimicry in Heliconius butterflies. Philosophical Transactions of the Royal Society of London B, 308, 433–613.
    https://doi.org/10.1098/rstb.1985.0066

    Supple, M.A., Papa, R., Hines, H.M., McMillan, W.O. & Counterman, B.A. (2015) Divergence with gene flow across a speciation continuum in Heliconius butterflies. BMC Evolutionary Biology, 15, 204.
    https://doi.org/10.1186/s12862-015-0486-y

    Van Belleghem, S.M., Rastas, P., Papanicolaou, A., Martin, S.H., Arias, C.F., Supple, M.A., Hanly, J.J., Mallet, J., Lewis, J. J., Hines, H.M., Ruiz, M., Salazar, C., Linares, M., Moreira, G.R.P. , Jiggins, C.D., Counterman, B.A., McMillan, W.O. & Papa, R. (2017) Complex modular architecture around a simple toolkit of wing pattern genes. Nature Ecology and Evolution, 1, 0052.
    https://doi.org/10.1038/s41559-016-0052

    Wahlberg, N. & Brower, A.V.Z. (2009) Nymphalidae Rafinesque 1815. Brush-footed Butterflies. Version 15 September 2009 (under construction). The Tree of Life Web Project. Available from: http://tolweb.org/Nymphalidae/12172/2009.09.15 (accessed 11 October 2017)

    Zhang, W., Dasmahapatra, K.K., Mallet, J., Moreira, G.R.P. & Kronforst, M.R. (2016) Genome-wide introgression among distantly-related Heliconius butterfly species. Genome Biology, 17, 25.
    https://doi.org/10.1186/s13059-016-0889-0