BMC Evolutionary Biology | |
The evolutionary genetics of highly divergent alleles of the mimicry locus in Papilio dardanus | |
Alfried P Vogler2  Chris D Jiggins1  Martijn JTN Timmermans2  Martin J Thompson1  | |
[1] Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK;Department of Life Sciences, Imperial College London, South Kensington Campus, London SW7 2AZ, United Kingdom | |
关键词: Molecular evolution; Phylogenetics; Engrailed; Supergene; Balanced polymorphism; Mimicry; | |
Others : 1118062 DOI : 10.1186/1471-2148-14-140 |
|
received in 2014-02-25, accepted in 2014-06-19, 发布年份 2014 | |
【 摘 要 】
Background
The phylogenetic history of genes underlying phenotypic diversity can offer insight into the evolutionary origin of adaptive traits. This is especially true where single genes have large phenotypic effects, for example in determining polymorphic mimicry in butterflies. Here, we characterise the evolutionary history of two candidate genes for the mimicry switch in the polymorphic Batesian mimic Papilio dardanus coding for the transcription factors engrailed and invected.
Results
We show that phased haplotypes associated with the dominant morphs f. poultoni and f. planemoides are phylogenetically highly divergent, in particular at non-synonymous sites. Some non-synonymous changes are shared between the divergent alleles suggesting either convergence or a shared ancestry. Gene trees for invected do not show this pattern. Despite their great divergence, all engrailed alleles of P. dardanus were monophyletic with respect to alleles of closely related species. Phylogenetic analyses therefore reveal no evidence for introgression from other species. A McDonald-Kreitman test conducted on a population sample from South Africa confirms a significant excess of intraspecific non-synonymous diversity in P. dardanus engrailed, suggesting long-term balanced polymorphism at this locus.
Conclusions
The divergence between engrailed haplotypes suggests an evolutionary history distorted by selection with multiple changes reflecting recurrent selective sweeps. The high level of intraspecific polymorphism observed is characteristic of balancing selection on this locus, as expected if the gene engrailed is under phenotypic selection for the maintenance of multiple mimetic morphs. Non-synonymous changes in key functional portions of a major transcription factor are likely to be deleterious but if maintained in a dominant allele at low frequency, heterozygosity would reduce the associated genetic load.
【 授权许可】
2014 Thompson et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150206020443755.pdf | 1919KB | download | |
Figure 7. | 52KB | Image | download |
Figure 6. | 67KB | Image | download |
Figure 5. | 72KB | Image | download |
Figure 4. | 39KB | Image | download |
Figure 3. | 40KB | Image | download |
Figure 2. | 33KB | Image | download |
Figure 1. | 72KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.
Figure 7.
【 参考文献 】
- [1]Joron M, Jiggins CD, Papanicolaou A, McMillan WO: Heliconius wing patterns: an evo-devo model for understanding phenotypic diversity. Heredity 2006, 97:157-167.
- [2]Nielsen R: Molecular signatures of natural selection. Annu Rev Genet 2005, 39:197-218.
- [3]Thompson MJ, Jiggins CD: Supergenes and their role in evolution. Heredity 2014, 113(1):1-8.
- [4]Carroll SB: Evolution at two levels: on genes and form. PLoS Biol 2005, 3:e245.
- [5]Rebeiz M, Pool JE, Kassner VA, Aquadro CF, Carroll SB: Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science 2009, 326:1663-7.
- [6]Prud’homme B, Gompel N, Carroll SB: Emerging principles of regulatory evolution. Proc Natl Acad Sci U S A 2007, 104(Suppl 1):8605-12.
- [7]van’t Hof AE, Edmonds N, Dalíková M, Marec F, Saccheri IJ: Industrial melanism in British peppered moths has a singular and recent mutational origin. Science 2011, 332:958-960.
- [8]Counterman B, Araujo-Perez F, Hines HM, Baxter SW, Morrison CM, Lindstrom DP, Papa R, Ferguson LC, Joron M, Ffrench-Constant RH, Smith CP, Nielsen DM, Chen R, Jiggins CD, Reed RD, Halder G, Mallet J, McMillan WO: Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in Heliconius erato. PLoS Genet 2010, 6:e1000796.
- [9]Baxter SW, Nadeau NJ, Maroja LS, Wilkinson P, Counterman B, Dawson A, Beltrán M, Perez-Espona S, Chamberlain NL, Ferguson LC, Clark R, Davidson C, Glithero R, Mallet J, McMillan WO, Kronforst MR, Joron M, Ffrench-Constant RH, Jiggins CD: Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene clade. PLoS Genet 2010, 6:e1000794.
- [10]The Heliconius Genome Consortium:: Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 2012, 487:94-8.
- [11]Naisbit RE, Jiggins CD, Mallet J: Mimicry: developmental genes that contribute to speciation. Evol Dev 2007, 5:269-80.
- [12]Kunte K, Zhang W, Tenger-Trolander A, Palmer DH, Martin A, Reed RD, Mullen SP, Kronforst MR: Doublesex is a mimicry supergene. Nature 2014, 507:229-32.
- [13]Hines HM, Counterman BA, Papa R, Albuquerque de Moura P, Cardoso MZ, Linares M, Mallet J, Reed RD, Jiggins CD, Kronforst MR, McMillan WO: Wing patterning gene redefines the mimetic history of Heliconius butterflies. Proc Natl Acad Sci U S A 2011, 108:19666-71.
- [14]Pardo-Diaz C, Salazar C, Baxter SW, Merot C, Figueiredo-Ready W, Joron M, McMillan WO, Jiggins CD: Adaptive introgression across species boundaries in Heliconius butterflies. PLoS Genet 2012, 8:e1002752.
- [15]Stern DL: The genetic causes of convergent evolution. Nat Rev Genet 2013, 14:751-764.
- [16]Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G, Dickson M, Grimwood J, Schmutz J, Myers RM, Schluter D, Kingsley DM: Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 2005, 307:1928-33.
- [17]Nijhout HF: Polymorphic mimicry in Papilio dardanus: mosaic dominance, big effects, and origins. Evol Dev 2003, 5:579-92.
- [18]Thompson MJ, Timmermans MJTN: Characterising the phenotypic diversity of Papilio dardanus wing patterns using an extensive museum collection. Plos one 2014, 9(5):e96815. doi:10.1371/journal.pone.0096815
- [19]Clarke CA, Sheppard PM: The genetics of Papilio dardanus Brown. I. Race cenea from South Africa. Genetics 1959, 44:1347-1358.
- [20]Clarke CA, Sheppard PM: The genetics of Papilio dardanus Brown. II. Races dardanus, polytrophus, meseres, and tibullus. Genetics 1960, 45:439-457.
- [21]Clarke CA, Sheppard PM: The genetics of Papilio dardanus Brown. III. Race antinorii from Abyssinia and race meriones from Madagascar. Genetics 1960, 45:683-698.
- [22]Clarke CA, Sheppard PM: The genetics of Papilio dardanus Brown. IV. Data on race ochracea, race flavicornis, and further information on races polytrophus and dardanus. Genetics 1962, 47:909-920.
- [23]Clarke CA, Sheppard PM: The genetics of some mimetic forms of Papilio dardanus Brown, and Papilio glaucus Linn. J Genet 1959, 56:236-259.
- [24]Clark R, Brown SM, Collins SC, Jiggins CD, Heckel DG, Vogler AP: Colour pattern specification in the mocker swallowtail Papilio dardanus: the transcription factor invected is a candidate for the mimicry locus H. Proc R Soc B Biol Sci 2008, 275:1181-1188.
- [25]Timmermans MJTN, Baxter SW, Clark R, Heckel DGG, Vogel H, Collins S, Papanicolaou A, Fukova I, Joron M, Thompson MJ, Jiggins CD, ffrench-Constant RH, Vogler AP: Comparative genomics of the mimicry switch in Papilio dardanus. Proc R Soc B Biol Sci 2014, 281(1787):20140465. doi:10.1098/rspb.2014.0465
- [26]Peel AD, Telford MJ, Akam M: The evolution of hexapod engrailed-family genes: evidence for conservation and concerted evolution. Proc R Soc B Biol Sci 2006, 273:1733-42.
- [27]Clark R, Vogler AP: A phylogenetic framework for wing pattern evolution in the mimetic mocker swallowtail Papilio dardanus. Mol Ecol 2009, 18:3872-84.
- [28]Thompson MJ, Vane-Wright RI, Timmermans MJTN: Hybrid origins: DNA techniques confirm that Papilio nandina is a species hybrid (Papilionidae). J Lepid Soc 2011, 65:199-201.
- [29]Thomsen PF, Elias S, Gilbert TM, Haile J, Munch K, Kuzmina S, Froese DG, Sher A, Holdaway RN, Willerslev E: Non-destructive sampling of ancient insect DNA. PLoS One 2009, 4:e5048.
- [30]Kronforst MR: Primers for the amplification of nuclear introns in Heliconius butterflies. Mol Ecol Notes 2005, 5(1):158-162.
- [31]Barraclough TG, Hogan JE, Vogler AP: Testing whether ecological factors promote cladogenesis in a group of tiger beetles (Coleoptera: Cicindelidae). Proc R Soc B Biol Sci 1999, 266:1061-1067.
- [32]Drummond A, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A: Geneious v5.3. 2010. Available from http://www.geneious.com webcite
- [33]Katoh K, Misawa K, Kuma K, Miyata T: MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002, 30:3059-66.
- [34]Hey J, Wakeley J: A coalescent estimator of the population recombination rate. Genetics 1997, 145:833-846.
- [35]Sturrock S, Meintjes P: The Geneious 6.0.3 Read Mapper.
- [36]McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA: The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010, 20:1297-303.
- [37]DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, McKenna A, Fennell TJ, Kernytsky AM, Sivachenko AY, Cibulskis K, Gabriel SB, Altshuler D, Daly MJ: A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 2011, 43:491-8.
- [38]Posada D: jModelTest: phylogenetic model averaging. Mol Biol Evol 2008, 25:1253-6.
- [39]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
- [40]Swofford DL: Phylogenetic Analysis Using Parsimony (*and Other Methods). 2003.
- [41]Stephens M, Smith NJ, Donnelly P: A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 2001, 68:978-89.
- [42]Stephens M, Scheet P: Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation. Am J Hum Genet 2005, 76:449-62.
- [43]Kosakovsky Pond SL, Frost SDW, Muse SV: HyPhy: hypothesis testing using phylogenies. Bioinformatics 2005, 21:676-9.
- [44]Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-2.
- [45]Zakharov EV, Caterino MS, Sperling FAH: Molecular phylogeny, historical biogeography, and divergence time estimates for swallowtail butterflies of the genus Papilio (Lepidoptera: Papilionidae). Syst Biol 2004, 53:193-215.
- [46]Caterino MS, Sperling FAH: Papilio phylogeny based on mitochondrial cytochrome oxidase I and II genes. Mol Phylogenet Evol 1999, 11:122-37.
- [47]Poulton EB: The most interesting butterfly in the world. J East African Nat Hist Soc 1924, 20:4-22.
- [48]Ford EB: The genetics of Papilio dardanus Brown (Lep.). Trans R Entomol Soc London 1936, 85:435-466.
- [49]Turner JRG: Geographical variation and evolution in the males of the butterfly Papilio dardanus Brown (Lepidoptera: Papilionidae). Trans R Entomol Soc London 1963, 115:239-259.
- [50]McDonald JH, Kreitman M: Adaptive protein evolution at the Adh locus in Drosophila. Nature 1991, 351:652-654.
- [51]Copley RR: The EH1 motif in metazoan transcription factors. BMC Genomics 2005, 6:169.
- [52]Smith ST, Jaynes JB: A conserved region of engrailed, shared among all en-, gsc-, Nk1-, Nk2-and msh-class homeoproteins, mediates active transcriptional repression in vivo. Development 1996, 122:3141.
- [53]Jiménez G, Paroush Z, Ish-Horowicz D: Groucho acts as a corepressor for a subset of negative regulators, including Hairy and Engrailed. Genes Dev 1997, 11:3072-3082.
- [54]Kapan DD: Three-butterfly system provides a test of Müllerian mimicry. Nature 2001, 409:18-20.
- [55]Llaurens V, Billiard S, Castric V, Vekemans X: Evolution of dominance in sporophytic self-incompatibility systems: I. Genetic load and coevolution of levels of dominance in pollen and pistil. Evolution 2009, 63:2427-37.
- [56]Clarke B: Frequency-dependent selection for the dominance of rare polymorphic genes. Evolution 1964, 18:364-369.
- [57]Darlington CD, Mather K: Elements of Genetics. London: George Allen & Unwin Ltd; 1949.
- [58]Charlesworth D, Charlesworth B: Mimicry: the hunting of the supergene. Curr Biol 2011, 21:R846-8.
- [59]Joron M, Frezal L, Jones RT, Chamberlain NL, Lee SF, Haag CR, Whibley AC, Becuwe M, Baxter SW, Ferguson LC, Wilkinson P, Salazar C, Davidson C, Clark R, Quail MA, Beasley H, Glithero R, Lloyd C, Sims S, Jones MC, Rogers J, Jiggins CD, Ffrench-Constant RH: Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 2011, 477:203-6.
- [60]Huynh LY, Maney DL, Thomas JW: Chromosome-wide linkage disequilibrium caused by an inversion polymorphism in the white-throated sparrow (Zonotrichia albicollis). Heredity 2010, 106:537-546.
- [61]Wang J, Wurm Y, Nipitwattanaphon M, Riba-Grognuz O, Huang Y-C, Shoemaker D, Keller L: A Y-like social chromosome causes alternative colony organization in fire ants. Nature 2013, 493:664-8.