Spatiotemporal dynamics in butterfly hybrid zones
Ananda R. Pereira Martins, Natalie B. Warren, W. Owen McMillan, Rowan D. H. Barrett
Evaluating whether hybrid zones are stable or mobile can provide novel insights for evolution and conservation biology. Butterflies exhibit high sensitivity to environmental changes and represent an important model system for the study of hybrid zone origins and maintenance. Here, we review the literature exploring butterfly hybrid zones, with a special focus on their spatiotemporal dynamics and the potential mechanisms that could lead to their movement or stability. We then compare different lines of evidence used to investigate hybrid zone dynamics and discuss the strengths and weaknesses of each approach. Our goal with this review is to reveal general conditions associated with the stability or mobility of butterfly hybrid zones by synthesizing evidence obtained using different types of data sampled across multiple regions and spatial scales. Finally, we discuss spatiotemporal dynamics in the context of a speciation/divergence continuum, the relevance of hybrid zones for conservation biology, and recommend key topics for future investigation.
butterflies / human impacts / hybrid zones / movement / spatiotemporal dynamics / stability
[1] |
Abbott,R., Albach, D., Ansell,S., Arntzen,J.W., Baird,S.J.E., Bierne,N. et al. (2013) Hybridization and speciation. Journal of Evolutionary Biology, 26, 229–246.
|
[2] |
Abbott,R.J. (2017) Plant speciation across environmental gradients and the occurrence and nature of hybrid zones: hybrid zones and plant speciation. Journal of Systematics and Evolution, 55, 238–258.
|
[3] |
Abdelaziz,M., Muñoz-Pajares, A.J., Berbel,M., García-Muñoz,A., Gómez,J.M. and Perfectti, F. (2021) Asymmetric reproductive barriers and gene flow promote the rise of a stable hybrid zone in the Mediterranean high mountain. Frontiers in Plant Science, 12, 687094.
|
[4] |
Arias,C.F., Muñoz, A.G., Jiggins,C.D., Mavárez,J., Bermingham, E. and Linares,M. (2008) A hybrid zone provides evidence for incipient ecological speciation in Heliconius butterflies. Molecular Ecology, 17, 4699–4712.
|
[5] |
Arnold,M.L. and Martin, N.H. (2009) Adaptation by introgression. Journal of Biology, 8, 82.
|
[6] |
Augustijnen,H., Patsiou, T. and Lucek,K. (2022) Secondary contact rather than coexistence-Erebia butterflies in the Alps. Evolution; Internation Journal of Organic Evolution, 76, 2669–2686.
|
[7] |
Bainbridge,H.E., Brien,M.N., Morochz,C., Salazar, P.A., Rastas,P. and Nadeau,N.J. (2020) Limited genetic parallels underlie convergent evolution of quantitative pattern variation in mimetic butterflies. Journal of Evolutionary Biology, 33, 1516–1529.
|
[8] |
Barton,N.H. (1983) Multilocus Clines. Evolution; Internation Journal of Organic Evolution, 37, 454–471.
|
[9] |
Barton,N.H. (1979) The dynamics of hybrid zones. Heredity, 43, 341–359.
|
[10] |
Barton,N.H. and Gale, K.S. (1993) Genetic analysis of hybrid zones. In Hybrid Zones and the Evolutionary Process (ed. R.G.Harrison), pp. 13–45. Oxford University Press, New York.
|
[11] |
Barton,N.H. and Hewitt, G.M. (1989) Adaptation, speciation and hybrid zones. Nature, 341, 497–503.
|
[12] |
Barton,N.H. and Hewitt, G.M. (1985) Analysis of hybrid zones. Annual Review of Ecology and Systematics, 16, 113–148.
|
[13] |
Barton,N.H. and Shpak, M. (2000) The effect of epistasis on the structure of hybrid zones. Genetical Research, 75, 179–198.
|
[14] |
Bates,H.W. (1862) XXXII. Contributions to an insect fauna of the Amazon Valley. Lepidoptera: Heliconidae. Transactions of the Linnean Society of London, 23, 495–566.
|
[15] |
Benson,W.W. (1978) Resource partitioning in passion vine butterflies. Evolution; Internation Journal of Organic Evolution, 32, 493–518.
|
[16] |
Bierne,N., Gagnaire, P.A. and David,P. (2013) The geography of introgression in a patchy environment and the thorn in the side of ecological speciation. Current Zoology, 59, 72–86.
|
[17] |
Blum,M.J. (2008) Ecological and genetic associations across a Heliconius hybrid zone. Journal of Evolutionary Biology, 21, 330–341.
|
[18] |
Blum,M.J. (2002) Rapid movement of a Heliconius hybrid zone: evidence for phase III of Wright's shifting balance theory? Evolution; Internation Journal of Organic Evolution, 56, 1992–1998.
|
[19] |
Boggs,C.L., Watt,W.B. and Ehrlich,P.R. (2003) Butterflies: Ecology and Evolution Taking Flight. University of Chicago Press, Chicago.
|
[20] |
Bonebrake,T.C., Ponisio, L.C., Boggs,C.L. and Ehrlich,P.R. (2010) More than just indicators: a review of tropical butterfly ecology and conservation. Biological Conservation, 143, 1831–1841.
|
[21] |
Boyd,B.M., Boyd,B.M., Austin,G.T. and Murphy, D.D. (1999) Hybridization of Limenitis in the Western Great Basin (Lepidoptera: Nymphalidae). Holarctic Lepidoptera, 6, 37–74.
|
[22] |
Braby,M.F., Eastwood, R. and Murray,N. (2012) The subspecies concept in butterflies: has its application in taxonomy and conservation biology outlived its usefulness? Biological Journal of the Linnean Society, 106, 699–716.
|
[23] |
Bridle,J.R., Baird,S.J.E. and Butlin,R.K. (2001) Spatial structure and habitat variation in a grasshopper hybrid zone. Evolution; Internation Journal of Organic Evolution, 55, 1832–1843.
|
[24] |
Brooks,S.J., Self,A., Toloni,F. and Sparks, T. (2014) Natural history museum collections provide information on phenological change in British butterflies since the late-nineteenth century. International Journal of Biometeorology, 58, 1749–1758.
|
[25] |
Brown,K.S. (1991) Conservation of neotropical environments: insects as indicators. In The Conservation of Insects and their Habitats (eds. N.M.Collins & J.A.Thomas), pp. 349–404. Royal Entomological Society of London Symposium 1989, London.
|
[26] |
Buerkle,C.A. and Lexer, C. (2008) Admixture as the basis for genetic mapping. Trends in Ecology & Evolution, 23, 686–694.
|
[27] |
Buggs,R.J.A. (2007) Empirical study of hybrid zone movement. Heredity, 99, 301–312.
|
[28] |
Burton,R.S. and Barreto, F.S. (2012) A disproportionate role for mtDNA in Dobzhansky-Muller incompatibilities? Molecular Ecology, 21, 4942–4957.
|
[29] |
Capblancq,T., Després, L. and Mavárez,J. (2020) Genetic, morphological and ecological variation across a sharp hybrid zone between two alpine butterfly species. Evolutionary Applications, 13, 1435–1450.
|
[30] |
Capblancq,T., Després, L., Rioux,D. and Mavárez,J. (2015) Hybridization promotes speciation in Coenonympha butterflies. Molecular Ecology, 24, 6209–6222.
|
[31] |
Capblancq,T., Mavárez, J., Rioux,D. and Després,L. (2019) Speciation with gene flow: Evidence from a complex of alpine butterflies (Coenonympha, Satyridae). Ecology and Evolution, 9, 6444–6457.
|
[32] |
Concha,C., Wallbank, R.W.R., Hanly,J.J., Fenner,J., Livraghi, L., Rivera,E.S. et al. (2019) Interplay between developmental flexibility and determinism in the evolution of mimetic Heliconius wing patterns. Current Biology, 29, 3996–4009.
|
[33] |
Cordell,H.J. (2002) Epistasis: what it means, what it doesn't mean, and statistical methods to detect it in humans. Human Molecular Genetics, 11, 2463–2468.
|
[34] |
Currat,M., Ruedi,M., Petit,R.J. and Excoffier, L. (2008) The hidden side of invasions: massive introgression by local genes. Evolution; Internation Journal of Organic Evolution, 62, 1908–1920.
|
[35] |
Curry,C.M. (2015) An integrated framework for hybrid zone models. Evolutionary Biology, 42, 359–365.
|
[36] |
Dasmahapatra,K.K., Blum, M.J., Aiello,A., Hackwell,S., Bermingham, E.P. and Mallet,J. (2002) Inferences from a rapidly moving hybrid zone. Evolution; Internation Journal of Organic Evolution, 56, 741–753.
|
[37] |
Dasmahapatra,K.K., Lamas, G., Simpson,F. and Mallet,J. (2010) The anatomy of a ‘suture zone’ in Amazonian butterflies: a coalescent-based test for vicariant geographic divergence and speciation. Molecular Ecology, 19, 4283–4301.
|
[38] |
De Queiroz,K. (2007) Species concepts and species delimitation. Systematic Biology, 56, 879–886.
|
[39] |
Descimon,H. and Mallet, J. (2009) Bad species. In Ecology of Butterflies in Europe (eds. J.Settele, T.G. Shreeve, M.Konvicka & V.H.Dyck), pp. 219–249. Cambridge University Press, Cambridge.
|
[40] |
Devitt,T.J., Baird,S.J. and Moritz,C. (2011) Asymmetric reproductive isolation between terminal forms of the salamander ring species Ensatina eschscholtzii revealed by fine-scale genetic analysis of a hybrid zone. BMC Evolutionary Biology, 11, 245.
|
[41] |
Dincă,V., Dapporto, L. and Vila,R. (2011) A combined genetic-morphometric analysis unravels the complex biogeographical history of Polyommatus icarus and Polyommatus celina Common Blue butterflies. Molecular Ecology, 20, 3921–3935.
|
[42] |
Dupuis,J.R. and Sperling, F.A.H. (2016) Hybrid dynamics in a species group of swallowtail butterflies. Journal of Evolutionary Biology, 29, 1932–1951.
|
[43] |
Duputié,A., Zimmermann, N.E. and Chuine,I. (2014) Where are the wild things? Why we need better data on species distribution. Global Ecology and Biogeography, 23, 457–467.
|
[44] |
Durrett,R., Buttel, L. and Harrison,R. (2000) Spatial models for hybrid zones. Heredity, 84, 9–19.
|
[45] |
Edelman,N.B. and Mallet, J. (2021) Prevalence and adaptive impact of introgression. Annual Review of Genetics, 55, 265–283.
|
[46] |
Endler,J.A. (1977) Geographic Variation, Speciation, and Clines. Princeton University Press, New Jersey.
|
[47] |
Freitas,A.V.L., Santos, J.P., Rosa,A.H.B., Iserhard,C.A., Richter, A., Siewert,R.R. et al. (2021) Sampling methods for butterflies (Lepidoptera). In Measuring Arthropod Biodiversity (eds. J.C.Santos & G.W.Fernandes), pp. 101–123. Springer Cham, Switzerland.
|
[48] |
Gauthier,J., Silva,D.L., Gompert,Z., Whibley, A., Houssin,C., Le Poul,Y. et al. (2020) Contrasting genomic and phenotypic outcomes of hybridization between pairs of mimetic butterfly taxa across a suture zone. Molecular Ecology, 29, 1328–1343.
|
[49] |
Gay,L., Crochet, P.A., Bell,D.A. and Lenormand,T. (2008) Comparing clines on molecular and phenotypic traits in hybrid zones: a window on tension zone models. Evolution; Internation Journal of Organic Evolution, 62, 2789–2806.
|
[50] |
Getz,W.M., Marshall, C.R., Carlson,C.J., Giuggioli,L., Ryan,S.J., Romañach,S.S. et al. (2018) Making ecological models adequate. Ecology Letters, 21, 153–166.
|
[51] |
Gilbert,L.E. and Singer, M.C. (1975) Butterfly ecology. Annual Review of Ecology and Systematics, 6, 365–397.
|
[52] |
Gompert,Z. and Buerkle, C.A. (2009) A powerful regression-based method for admixture mapping of isolation across the genome of hybrids. Molecular Ecology, 18, 1207–1224.
|
[53] |
Gompert,Z., Lucas,L.K., Fordyce,J.A., Forister,M.L. and Nice, C.C. (2010) Secondary contact between Lycaeides idas and L. melissa in the Rocky Mountains: extensive admixture and a patchy hybrid zone. Molecular Ecology, 19, 3171–3192.
|
[54] |
Gompert,Z., Mandeville, E.G. and Buerkle,C.A. (2017) Analysis of population genomic data from hybrid zones. Annual Review of Ecology, Evolution, and Systematics, 48, 207–229.
|
[55] |
Guillera-Arroita,G., Lahoz-Monfort, J.J., Elith,J., Gordon,A., Kujala, H., Lentini,P.E. et al. (2015) Is my species distribution model fit for purpose? Matching data and models to applications. Global Ecology and Biogeography, 24, 276–292.
|
[56] |
Hällfors,M.H., Heikkinen, R.K., Kuussaari,M., Lehikoinen,A., Luoto,M., Pöyry,J. et al. (2023) Recent range shifts of moths, butterflies, and birds are driven by the breadth of their climatic niche. Evolution Letters, qrad004.
CrossRef
Google scholar
|
[57] |
Hanly,J.J., Wallbank, R.W.R., McMillan,W.O. and Jiggins,C.D. (2019) Conservation and flexibility in the gene regulatory landscape of heliconiine butterfly wings. EvoDevo, 10, 15.
|
[58] |
Harr,B. (2006) Genomic islands of differentiation between house mouse subspecies. Genome Research, 16, 730–737.
|
[59] |
Harrison,R.G. (1989) Animal mitochondrial DNA as a genetic marker in population and evolutionary biology. Trends in Ecology & Evolution, 4, 6–11.
|
[60] |
Harrison,R.G. and Bogdanowicz, S.M. (1997) Patterns of variation and linkage disequilibrium in a field cricket hybrid zone. Evolution; Internation Journal of Organic Evolution, 51, 493–505.
|
[61] |
Harrison,R.G. and Larson, E.L. (2016) Heterogeneous genome divergence, differential introgression, and the origin and structure of hybrid zones. Molecular Ecology, 25, 2454–2466.
|
[62] |
Harrison,R.G. and Larson, E.L. (2014) Hybridization, Introgression, and the Nature of Species Boundaries. Journal of Heredity, 105, 795–809.
|
[63] |
Harrison,R.G. and Rand, D.M. (1989) Mosaic hybrid zones and the nature of species boundaries. In Speciation and Its Consequences (eds. D.Otte & J.A.Endler), pp. 111–134. Sinauer Association, Sunderland.
|
[64] |
Hewitt,G.M. (1988) Hybrid zones-natural laboratories for evolutionary studies. Trends in Ecology & Evolution, 3, 158–167.
|
[65] |
Hewitt,G.M. (2011) Quaternary phylogeography: the roots of hybrid zones. Genetica, 139, 617–638.
|
[66] |
Hewitt,G.M. (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society, 58, 247–276.
|
[67] |
Hill,G.M., Kawahara, A.Y., Daniels,J.C., Bateman,C.C. and Scheffers, B.R. (2021) Climate change effects on animal ecology: butterflies and moths as a case study. Biological Reviews, 96, 2113–2126.
|
[68] |
Jay,P., Leroy,M., Le Poul,Y., Whibley, A., Arias,M., Chouteau,M. et al. (2022) Association mapping of colour variation in a butterfly provides evidence that a supergene locks together a cluster of adaptive loci. Philosophical Transactions of the Royal Society B, 377, 20210193.
|
[69] |
Jiggins,C.D., Estrada, C. and Rodrigues,A. (2004) Mimicry and the evolution of premating isolation in Heliconius melpomene Linnaeus. Journal of Evolutionary Biology, 17, 680–691.
|
[70] |
Jiggins,C.D. and Mallet, J. (2000) Bimodal hybrid zones and speciation. Trends in Ecology & Evolution, 15, 250–255.
|
[71] |
Jiggins,C.D., McMillan, W.O., Neukirchen,W. and 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.
|
[72] |
Jørgensen,S.E. and Fath, B.D. (2011) Introduction. In Developments in Environmental Modelling (eds. S.E.Jørgensen & B.D.Fath), pp. 1–18. Elsevier, Amsterdam.
|
[73] |
Kivisild,T., Shen,P., Wall,D.P., Do, B., Sung,R., Davis,K. et al. (2006) The role of selection in the evolution of human mitochondrial genomes. Genetics, 172, 373–387.
|
[74] |
Kral,K., Harmon, J., Limb,R. and Hovick,T. (2018) Improving our science: the evolution of butterfly sampling and surveying methods over time. Journal of Insect Conservation, 22, 1–14.
|
[75] |
Kronforst,M.R., Hansen, M.E.B., Crawford,N.G., Gallant,J.R., Zhang,W., Kulathinal,R.J. et al. (2013) Hybridization reveals the evolving genomic architecture of speciation. Cell Reports, 5, 666–677.
|
[76] |
Kunte,K., Shea,C., Aardema,M.L., Scriber,J.M., Juenger, T.E., Gilbert,L.E. et al. (2011) Sex chromosome mosaicism and hybrid speciation among Tiger Swallowtail Butterflies. PLoS Genetics, 7, e1002274.
|
[77] |
Larson,E.L., White,T.A., Ross,C.L. and Harrison, R.G. (2014) Gene flow and the maintenance of species boundaries. Molecular Ecology, 23, 1668–1678.
|
[78] |
Lewis,J.J. and Van Belleghem, S.M. (2020) Mechanisms of change: a population-based perspective on the roles of modularity and pleiotropy in diversification. Frontiers in Ecology and Evolution, 8, 261.
|
[79] |
Livraghi,L., Hanly,J.J., Van Bellghem,S.M., Montejo-Kovacevich,G., van der Heijden,E.S., Loh,L.S. et al. (2021) Cortex cis-regulatory switches establish scale colour identity and pattern diversity in Heliconius. eLife, 10, e68549.
|
[80] |
Lucek,K., Butlin, R.K. and Patsiou,T. (2020) Secondary contact zones of closely-related Erebia butterflies overlap with narrow phenotypic and parasitic clines. Journal of Evolutionary Biology, 33, 1152–1163.
|
[81] |
Mallet,J. (1986) Hybrid zones of Heliconius butterflies in Panama and the stability and movement of warning colour clines. Heredity, 56, 191–202.
|
[82] |
Mallet,J. (2005) Hybridization as an invasion of the genome. Trends in Ecology & Evolution, 20, 229–237.
|
[83] |
Mallet,J. (1993) Speciation, raciation, and color pattern evolution in Heliconius butterflies: evidence from hybrid zones. In Hybrid Zones and the Evolutionary Process (ed. R.G.Harrison), pp. 226–260. Oxford University Press, New York.
|
[84] |
Mallet,J. (2007) Subspecies, semispecies, superspecies. Encyclopedia of Biodiversity, 5, 523–526.
|
[85] |
Mallet,J. and Barton, N. (1989) Inference from clines stabilized by frequency-dependent selection. Genetics, 122, 967–976.
|
[86] |
Mallet,J., Barton, N., Lamas,G.M., Santisteban,J.C., Muedas, M.M. and Eeley,H. (1990) Estimates of selection and gene flow from measures of cline width and linkage disequilibrium in Heliconius hybrid zones. Genetics, 124, 921–936.
|
[87] |
Mallet,J., Beltrán, M., Neukirchen,W. and Linares,M. (2007) Natural hybridization in heliconiine butterflies: the species boundary as a continuum. BMC Evolutionary Biology, 7, 28.
|
[88] |
Mallet,J., Wynne,I.R. and Thomas,C.D. (2011) Hybridisation and climate change: brown argus butterflies in Britain (Polyommatus subgenus Aricia). Insect Conservation and Diversity, 4, 192–199.
|
[89] |
Marabuto,E., Nunes,M.S., Martins,R., Mendes, R., Moreira-Pinhal,T.C., Raimundo,J. et al. (2023) Integrative analysis reveals the divergence and speciation between sister Sooty Copper butterflies Lycaena bleusei and L. tityrus. Molecular Phylogenetics and Evolution, 180, 107699.
|
[90] |
Martelli,F., Paradiso, F., Ghidotti,S., Viterbi,R., Cerrato, C. and Bonelli,S. (2022) Invasion patterns and niche comparison of the butterfly Cacyreus marshalli among native and non-native range. Biological Invasions, 24, 3935–3952.
|
[91] |
Matute,D.R., Butler, I.A., Turissini,D.A. and Coyne,J.A. (2010) A test of the snowball theory for the rate of evolution of hybrid incompatibilities. Science, 329, 1518–1521.
|
[92] |
Mayr,E. (1966) Animal Species and Evolution. Belknap Press of Harvard University Press, Cambridge.
|
[93] |
Mayr,E. (1970) Populations, Species, and Evolution: An Abridgment of Animal Species and Evolution. Belknap Press of Harvard University Press, Cambridge.
|
[94] |
Mayr,E. (1982) The Growth of Biological Thought: Diversity, Evolution, and Inheritance. Belknap Press of Harvard University Press, Cambridge.
|
[95] |
McMillan,W.O., Jiggins, C.D. and Mallet,J. (1997) What initiates speciation in passion-vine butterflies? Proceedings of the National Academy of Sciences USA, 94, 8628–8633.
|
[96] |
Meier,J.I., Salazar, P.A., Kučka,M., Davies,R.W., Dréau, A., Aldás,I. et al. (2021) Haplotype tagging reveals parallel formation of hybrid races in two butterfly species. Proceedings of the National Academy of Sciences USA, 118, e2015005118.
|
[97] |
Merow,C., Smith,M.J. and Silander,J.A. (2013) A practical guide to MaxEnt for modeling species’ distributions: what it does, and why inputs and settings matter. Ecography, 36, 1058–1069.
|
[98] |
Merrill,R.M., Dasmahapatra, K.K., Davey,J.W., Dell'Aglio,D.D., Hanly,J.J., Huber,B. et al. (2015) The diversification of Heliconius butterflies: what have we learned in 150 years? Journal of Evolutionary Biology, 28, 1417–1438.
|
[99] |
Merrill,R.M., Naisbit, R.E., Mallet,J. and Jiggins,C.D. (2013) Ecological and genetic factors influencing the transition between host-use strategies in sympatric Heliconius butterflies. Journal of Evolutionary Biology, 26, 1959–1967.
|
[100] |
Mishmar,D., Ruiz-Pesini, E., Golik,P., Macaulay,V., Clark,A.G., Hosseini,S. et al. (2003) Natural selection shaped regional mtDNA variation in humans. Proceedings of the National Academy of Sciences USA, 100, 171–176.
|
[101] |
Monteiro,A. (2015) Origin, development, and evolution of butterfly eyespots. Annual Review of Entomology, 60, 253–271.
|
[102] |
Morales-Rozo,A., Tenorio, E.A., Carling,M.D. and Cadena,C.D. (2017) Origin and cross-century dynamics of an avian hybrid zone. BMC Evolutionary Biology, 17, 257.
|
[103] |
Morris,J., Navarro, N., Rastas,P., Rawlins,L.D., Sammy,J., Mallet,J. et al. (2019) The genetic architecture of adaptation: convergence and pleiotropy in Heliconius wing pattern evolution. Heredity, 123, 138–152.
|
[104] |
Moyle,L.C. and Nakazato, T. (2010) Hybrid incompatibility “Snowballs” between Solanum species. Science, 329, 1521–1523.
|
[105] |
Muñoz,A.G., Salazar, C., Castaño,J., Jiggins,C.D. and Linares, M. (2010) Multiple sources of reproductive isolation in a bimodal butterfly hybrid zone. Journal of Evolutionary Biology, 23, 1312–1320.
|
[106] |
Nordborg,M. and Tavaré, S. (2002) Linkage disequilibrium: what history has to tell us. Trends in Genetics, 18, 83–90.
|
[107] |
Nosil,P., Funk,D.J. and Ortiz-Barrientos,D. (2009) Divergent selection and heterogeneous genomic divergence. Molecular Ecology, 18, 375–402.
|
[108] |
Orteu,A. and Jiggins, C.D. (2020) The genomics of coloration provides insights into adaptive evolution. Nature Reviews Genetics, 21, 461–475.
|
[109] |
Pardo-Diaz,C., Salazar, C., Baxter,S.W., Merot,C., Figueiredo-Ready, W., Joron,M. et al. (2012) Adaptive introgression across species boundaries in Heliconius butterflies. PLoS Genetics, 8, e1002752.
|
[110] |
Parmesan,C. (2003) Butterflies as bioindicators for climate change effects. In Butterflies: Ecology and Evolution Taking Flight (eds. C.L.Boggs, W.B.Watt & P.R. Ehrlich), pp. 541–560. University of Chicago Press, Chicago.
|
[111] |
Peck,S.L. (2004) Simulation as experiment: a philosophical reassessment for biological modeling. Trends in Ecology & Evolution, 19, 530–534.
|
[112] |
Pereira Martins,A.R., Martins, L.P., Ho,W., McMillan,W.O., Ready,J.S. and Barrett,R.D.H. (2022) Scale-dependent environmental effects on phenotypic distributions in Heliconius butterflies. Ecology and Evolution, 12, e9286.
|
[113] |
Phillips,P.C. (2008) Epistasis—the essential role of gene interactions in the structure and evolution of genetic systems. Nature Reviews Genetics, 9, 855–867.
|
[114] |
Polechová,J. and Barton, N. (2011) Genetic drift widens the expected cline but narrows the expected cline width. Genetics, 189, 227–235.
|
[115] |
Porter,A. (1997) The Pieris napi/bryoniae hybrid zone at Pont de Nant, Switzerland: broad overlap in the range of suitable host plants. Ecological Entomology, 22, 189–196.
|
[116] |
Porter,A.H., Wenger, R., Geiger,H., Scholl,A. and Shapiro, A.M. (1997) The Pontia daplidice-edusa hybrid zone in Northwestern Italy. Evolution; Internation Journal of Organic Evolution, 51, 1561–1573.
|
[117] |
Remington,C.L. (1968) Suture-zones of hybrid interaction between recently joined biotas. In Evolutionary Biology (eds. T.Dobzhansky, M.K.Hecht & W.C.Steere), pp. 321–428. Springer International Publishing, Boston.
|
[118] |
Riemsdijk,I., Butlin, R.K., Wielstra,B. and Arntzen,J.W. (2019) Testing an hypothesis of hybrid zone movement for toads in France. Molecular Ecology, 28, 1070–1083.
|
[119] |
Ross,C.L. and Harrison, R.G. (2002) A fine-scale spatial analysis of the mosaic hybrid zone between Gryllus firmus and Gryllus pennsylvanicus. Evolution; Internation Journal of Organic Evolution, 56, 2296–2312.
|
[120] |
Rosser,N., Dasmahapatra, K.K. and Mallet,J. (2014) Stable Heliconius butterfly hybrid zones are correlated with a local rainfall peak at the edge of the Amazon basin. Evolution; Internation Journal of Organic Evolution, 68, 3470–3484.
|
[121] |
Rosser,N., Shirai, L.T., Dasmahapatra,K.K., Mallet,J. and Freitas, A.V.L. (2021) The Amazon river is a suture zone for a polyphyletic group of co-mimetic heliconiine butterflies. Ecography, 44, 177–187.
|
[122] |
Rossi,M., Hausmann, A.E., Thurman,T.J., Montgomery,S.H., Papa,R., Jiggins,C.D. et al. (2020) Visual mate preference evolution during butterfly speciation is linked to neural processing genes. Nature Communications, 11, 4763.
|
[123] |
Roux,C., Fraïsse, C., Romiguier,J., Anciaux,Y., Galtier, N. and Bierne,N. (2016) Shedding light on the grey zone of speciation along a continuum of genomic divergence. PLoS Biology, 14, e2000234.
|
[124] |
Ruiz-Pesini,E. and Wallace, D.C. (2006) Evidence for adaptive selection acting on the tRNA and rRNA genes of human mitochondrial DNA. Human Mutation, 27, 1072–1081.
|
[125] |
Ryan,S.F., Deines, J.M., Scriber,J.M., Pfrender,M.E., Jones,S.E., Emrich,S.J. et al. (2018) Climate-mediated hybrid zone movement revealed with genomics, museum collection, and simulation modeling. Proceedings of the National Academy of Sciences USA, 115, E2284–E2291.
|
[126] |
Ryan,S.F., Fontaine, M.C., Scriber,J.M., Pfrender,M.E., O'Neil, S.T. and Hellmann,J.J. (2017) Patterns of divergence across the geographic and genomic landscape of a butterfly hybrid zone associated with a climatic gradient. Molecular Ecology, 26, 4725–4742.
|
[127] |
Savolainen,O., Lascoux, M. and Merilä,J. (2013) Ecological genomics of local adaptation. Nature Reviews Genetics, 14, 807–820.
|
[128] |
Scriber,J. (2002) Latitudinal and local geographic mosaics in host plant preferences as shaped by thermal units and voltinism in Papilio spp. (Lepidoptera). European Journal of Entomology, 99, 225–239.
|
[129] |
Scriber,J., Elliot, B., Maher,E., McGuire,M. and Niblack, M. (2014) Adaptations to “Thermal Time” Ccnstraints in Papilio: latitudinal and local size clines differ in response to regional climate change. Insects, 5, 199–226.
|
[130] |
Scriber,J.M. (1990) Interaction of introgression from Papilio Glaucus Canadensis and diapause in producing “Spring Form” Eastern Tiger Swallowtail Butterflies, P. Glaucus (Lepidoptera: Palilionidae). The Great Lakes Entomologist, 23, 127–138.
|
[131] |
Scriber,J.M., Keefover, K. and Nelson,S. (2002) 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.
|
[132] |
Sequeira,F., Bessa-Silva, A., Tarroso,P., Sousa-Neves,T., Vallinoto, M., Gonçalves,H. et al. (2020) Discordant patterns of introgression across a narrow hybrid zone between two cryptic lineages of an Iberian endemic newt. Journal of Evolutionary Biology, 33, 202–216.
|
[133] |
Slatkin,M. (2008) Linkage disequilibrium—understanding the evolutionary past and mapping the medical future. Nature Reviews Genetics, 9, 477–485.
|
[134] |
Smadja,C.M. and Butlin, R.K. (2011) A framework for comparing processes of speciation in the presence of gene flow. Molecular Ecology, 20, 5123–5140.
|
[135] |
Stankowski,S., Shipilina, D. and Westram,A.M. (2021) Hybrid zones. eLS, 2, 1–16.
|
[136] |
Stump,A.D., Sperling, F.A.H., Crim,A. and Scriber,J.M. (2003) Gene flow between Great Lakes region populations of the Canadian Tiger Swallowtail Butterfly, Papilio canadensis, near the hybrid zone with P. glaucus (Lepidoptera: Papilionidae). The Great Lakes Entomologist, 36, 41–53.
|
[137] |
Supple,M.A., Papa,R., Hines,H.M., McMillan, W.O. and Counterman,B.A. (2015) Divergence with gene flow across a speciation continuum of Heliconius butterflies. BMC Evolutionary Biology, 15, 204.
|
[138] |
Szymura,J.M. and Barton, N.H. (1986) Genetic analysis of a hybrid zone between the Fire-Bellied Toads, Bombina bombina and B. variegata, near Cracow in Southern Poland. Evolution; Internation Journal of Organic Evolution, 40, 1141–1159.
|
[139] |
Szymura,J.M. and Barton, N.H. (1991) The genetic structure of the hybrid zone between the Fire-Bellied Toads Bombina bombina and B. variegata: comparisons between transects and between loci. Evolution; Internation Journal of Organic Evolution, 45, 237–261.
|
[140] |
Taylor,S.A., Larson, E.L. and Harrison,R.G. (2015) Hybrid zones: windows on climate change. Trends in Ecology & Evolution, 30, 398–406.
|
[141] |
Thomas,J.A. (2016) Butterfly communities under threat. Science, 353, 216–218.
|
[142] |
Thomas,J.A. (2005) Monitoring change in the abundance and distribution of insects using butterflies and other indicator groups. Philosophical Transactions of the Royal Society B, 360, 339–357.
|
[143] |
Thurman,T.J., Szejner-Sigal, A. and McMillan,W.O. (2019) Movement of a Heliconius hybrid zone over 30 years: a Bayesian approach. Journal of Evolutionary Biology, 32, 974–983.
|
[144] |
Toews,D.P.L. and Brelsford, A. (2012) The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology, 21, 3907–3930.
|
[145] |
Turner,T.L., Hahn,M.W. and Nuzhdin,S.V. (2005) Genomic islands of speciation in Anopheles gambiae. PLoS Biology, 3, e285.
|
[146] |
Van Belleghem,S.M., Cole, J.M., Montejo-Kovacevich,G., Bacquet,C.N., McMillan,W.O., Papa,R. et al. (2021) Selection and isolation define a heterogeneous divergence landscape between hybridizing Heliconius butterflies. Evolution; Internation Journal of Organic Evolution, 75, 2251–2268.
|
[147] |
Van Belleghem,S.M., Rastas, P., Papanicolaou,A., Martin,S.H., Arias,C.F., Supple,M.A. et al. (2017) Complex modular architecture around a simple toolkit of wing pattern genes. Nature Ecology & Evolution,
CrossRef
Google scholar
|
[148] |
Van Belleghem,S.M., Ruggieri, A.A., Concha,C., Livraghi,L., Hebberecht, L., Rivera,E.S. et al. (2023) High level of novelty under the hood of convergent evolution. Science, 379, 1043–1049.
|
[149] |
Van Belleghem,S.M.V., Roman, P.A.A., Gutierrez,H.C., Counterman,B.A. and Papa, R. (2020) Perfect mimicry between Heliconius butterflies is constrained by genetics and development. Proceedings of the Royal Society B, 287, 20201267.
|
[150] |
Vines,T.H., Kohler, S.C., Thiel,M., Ghira,I., Sands,T.R., MacCallum,C.J. et al. (2003) The maintenance of reproductive isolation in a mosaic hybrid zone between the fire-bellied toads Bombina bombina and B. variegata. Evolution; Internation Journal of Organic Evolution, 57, 1876–1888.
|
[151] |
Wang,L., Luzynski, K., Pool,J.E., Janoušek,V., Dufková, P., Vyskočilová, M.M. et al. (2011) Measures of linkage disequilibrium among neighbouring SNPs indicate asymmetries across the house mouse hybrid zone. Molecular Ecology, 20, 2985–3000.
|
[152] |
Wang,S., Rohwer, S., Delmore,K. and Irwin,D.E. (2019) Cross-decades stability of an avian hybrid zone. Journal of Evolutionary Biology, 32, 1242–1251.
|
[153] |
WattW.B. and Boggs C.L. (2003) Synthesis: Butterflies as model systems in ecology and evolution—present and future. In Butterflies: Ecology and Evolution Taking Flight (eds. Boggs, C.L., Watt,W.B. & P.R.Ehrlich), pp. 603–613. University of Chicago Press, Chicago.
|
[154] |
Wielstra,B. (2019) Historical hybrid zone movement: More pervasive than appreciated. Journal of Biogeography, 46, 1300–1305.
|
[155] |
Wisz,M.S., Pottier, J., Kissling,W.D., Pellissier,L., Lenoir, J., Damgaard,C.F. et al. (2013) The role of biotic interactions in shaping distributions and realised assemblages of species: implications for species distribution modelling. Biological Reviews, 88, 15–30.
|
[156] |
Wolf,J.B.W. and Ellegren, H. (2017) Making sense of genomic islands of differentiation in light of speciation. Nature Reviews Genetics, 18, 87–100.
|
[157] |
Wu,C.I. (2001) The genic view of the process of speciation. Journal of Evolutionary Biology, 14, 851–865.
|
[158] |
Xiong,T. and Mallet, J. (2022) On the impermanence of species: the collapse of genetic incompatibilities in hybridizing populations. Evolution; Internation Journal of Organic Evolution, 76, 2498–2512.
|
[159] |
Zhang,L., Chaturvedi, S., Nice,C.C., Lucas,L.K. and Gompert, Z. (2022) Population genomic evidence of selection on structural variants in a natural hybrid zone. Molecular Ecology, 32, 1497–1514.
|
[160] |
Zhang,L., Thibert-Plante, X., Ripa,J., Svanbäck,R. and Brännström, Å. (2019) Biodiversity loss through speciation collapse: mechanisms, warning signals, and possible rescue. Evolution; Internation Journal of Organic Evolution, 73, 1504–1516.
|
[161] |
Zhang,Y., Teng,D., Lu,W., Liu, M., Cao,L., Southcott,L. et al. (2021) A widely diverged locus involved in locomotor adaptation in Heliconius butterflies. Science Advances, 7, eabh2340.
|
[162] |
Zieliński,P., Dudek, K., Arntzen,J.W., Palomar,G., Niedzicka, M., Fijarczyk,A. et al. (2019) Differential introgression across new hybrid zones: evidence from replicated transects. Molecular Ecology, 28, 4811–4824.
|
/
〈 | 〉 |