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PLOS ONE  2011 

Mitochondrial DNA Signature for Range-Wide Populations of Bicyclus anynana Suggests a Rapid Expansion from Recent Refugia

DOI: 10.1371/journal.pone.0021385

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This study investigates the genetic diversity, population structure and demographic history of the afrotropical butterfly Bicyclus anynana using mitochondrial DNA (mtDNA). Samples from six wild populations covering most of the species range from Uganda to South Africa were compared for the cytochrome c oxidase subunit gene (COI). Molecular diversity indices show overall high mtDNA diversity for the populations, but low nucleotide divergence between haplotypes. Our results indicate relatively little geographic population structure among the southern populations, especially given the extensive distributional range and an expectation of limited gene flow between populations. We implemented neutrality tests to assess signatures of recent historical demographic events. Tajima's D test and Fu's FS test both suggested recent population growth for the populations. The results were only significant for the southernmost populations when applying Tajima's D, but Fu's FS indicated significant deviations from neutrality for all populations except the one closest to the equator. Based on our own findings and those from pollen and vegetation studies, we hypothesize that the species range of B. anynana was reduced to equatorial refugia during the last glacial period, and that the species expanded southwards during the past 10.000 years. These results provide crucial background information for studies of phenotypic and molecular adaptation in wild populations of B. anynana.


[1]  Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236: 787–792. doi:10.1126/science.3576198.
[2]  Avise JC (2000) Phylogeography: the history and formation of species. Cambridge: Harvard University Press. 447 p.
[3]  Oostra V, de Jong MA, Invergo B, Kesbeke FMNH, Wende F, et al. (2010) Translating environmental gradients into discontinuous reaction norms via hormone signalling in a polyphenic butterfly. Proc R Soc B. doi:10.1098/rspb.2010.1560.
[4]  de Jong MA, Kesbeke FMNH, Brakefield PM, Zwaan BJ (2010) Geographic variation in thermal plasticity of life history and wing pattern in Bicyclus anynana. Clim Res 43: 91–102. doi:10.3354/cr00881.
[5]  Brakefield PM (2010) Radiations of Mycalesine butterflies and opening up their exploration of morphospace. Am Nat 176: S77–S87. doi:10.1086/657059.
[6]  Condamin M (1973) Monographie du genre Bicyclus (Lepidoptera Satyridae). Mémoires de l'Institute Fondamental d'Afrique Noire 88: 1–324.
[7]  Brakefield PM, Reitsma N (1991) Phenotypic plasticity, seasonal climate and the population biology of Bicyclus butterflies (Satyridae) in Malawi. Ecol Entomol 16: 291–303. doi:10.1111/j.1365-2311.1991.tb00220.x.
[8]  Brakefield PM, Gates J, Keys D, Kesbeke F, Wijngaarden PJ, et al. (1996) Development, plasticity and evolution of butterfly eyespot patterns. Nature 384: 236–242. doi:10.1038/384236a0.
[9]  Moritz C, Dowling TE, Brown WM (1987) Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Annu Rev Ecol Syst 18: 269–292. doi:10.1146/
[10]  Harrison RG (1989) Animal mitochondrial DNA as a genetic marker in population and evolutionary biology. Trends Ecol Evol 4: 6–11. doi:10.1016/0169-5347(89)90006-2.
[11]  Caterino MS, Soowon C, Sperling FAH (2000) The current state of insect molecular systematics: a thriving tower of Babel. Annu Rev Entomol 45: 1–54. doi:10.1146/annurev.ento.45.1.1.
[12]  Wahlberg N, Wheat CW (2008) Genomic outposts serve the phylogenomic pioneers: designing novel nuclear markers for genomic DNA extractions of Lepidoptera. Syst Biol 57: 231–242. doi:10.1080/10635150802033006.
[13]  Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid S 41: 95–98.
[14]  Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10: 564–567. doi:10.1111/j.1755-0998.2010.02847.x.
[15]  Nei M (1987) Molecular evolutionary genetics. New York: Colombia University Press. 512 p.
[16]  Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479–491.
[17]  Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19: 2092–2100.
[18]  Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915–925.
[19]  Vandewoestijne S, Baguette M, Brakefield PM, Saccheri IJ (2004) Phylogeography of Aglais urticae (Lepidoptera) based on DNA sequences of the mitochondrial COI gene and control region. Mol Phylogenet Evol 31: 630–646. doi:10.1016/j.ympev.2003.09.007.
[20]  Valade R, Kenis M, Hernandez-Lopez A, Augustin S, Mari Mena N, et al. (2009) Mitochondrial and microsatellite DNA markers reveal a Balkan origin for the highly invasive horse-chestnut leaf miner Cameraria ohridella (Lepidoptera, Gracillariidae). Mol Ecol 18: 3458–3470. doi:10.1111/j.1365-294X.2009.04290.x.
[21]  Brower AVZ, Boyce TM (1991) Mitochondrial DNA variation in monarch butterflies. Evolution 45: 1281–1286.
[22]  Estoup A, Solignac M, Cornuet JM, Goudet J, Scholl A (1996) Genetic differentiation of continental and island populations of Bombus terrestris (Hymenoptera: Apidae) in Europe. Mol Ecol 5: 19–31. doi:10.1111/j.1365-294X.1996.tb00288.x.
[23]  Freeland JR, May M, Lodge R, Conrad KF (2003) Genetic diversity and widespread haplotypes in a migratory dragonfly, the common green darner Anax junius. Ecol Entomol 28: 413–421. doi:10.1046/j.1365-2311.2003.00521.x.
[24]  Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.
[25]  Ruiz-Pesini E, Mishmar D, Brandon M, Procaccio V, Wallace DC (2004) Effects of purifying and adaptive selection on regional variation in human mtDNA. Science 303: 223–226. doi:10.1126/science.1088434.
[26]  Prentice IC, Jolly D (2000) Mid-Holocene and glacial-maximum vegetation geography of the northern continents and Africa. J Biogeogr 27: 507–519. doi:10.1046/j.1365-2699.2000.00425.x.
[27]  Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405: 907–913. doi:10.1038/35016000.
[28]  Flenley JR (1998) Tropical forests under the climates of the last 30,000 years. Climate Change 39: 177–197. doi:10.1023/A:1005367822750.
[29]  Elenga H, Peyron O, Bonnefille R, Prentice IC, Jolly D, et al. (2000) Pollen-based biome reconstructions for southern Europe and Africa 18,000 yr bp. J Biogeogr 27: 621–634. doi:10.1046/j.1365-2699.2000.00430.x.
[30]  Hamilton A, Taylor D, Howard P (2001) Hotspots in African forests as Quaternary refugia. In: Weber W, White LJT, Vedder A, Naughton-Treves L, editors. African rain forest ecology and conservation: an interdisciplinary perspective. New Haven: Yale University Press. pp. 183–206.
[31]  Douglass JF, Miller LD (2003) Afrotropical skippers (Lepidoptera: Hesperioidea) and the emergence of the combined refugium theory. Bulletin of the Allyn Museum 143: 1–18.


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