Introgression as a likely cause of mtDNA paraphyly in two allopatric skippers (Lepidoptera: Hesperiidae)

Heredity

Volumn 102, Issue 6, 2009, Pages 590-599

  Zakharov, E V ^a,b   Lobo, N F ^a   Nowak, C ^a,c   Hellmann, J J ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b UNIVERSITY OF GUELPH   (Canada)

^c SENCKENBERG RESEARCH INSTITUTE   (Germany)

Author keywords

Allopatric distribution; Erynnis horatius; Erynnis propertius; Introgression; MtDNA; Organelle capture

Indexed keywords

MITOCHONDRIAL DNA;

ALLOPATRY; BUTTERFLY; DIVERGENCE; GENE TRANSFER; GENOMICS; HYBRIDIZATION; INTERSPECIFIC INTERACTION; INTROGRESSION; MITOCHONDRIAL DNA;

ANIMAL; ARTICLE; CLASSIFICATION; FEMALE; GENETIC VARIABILITY; GENETICS; INBREEDING; LEPIDOPTERA; MALE; MOLECULAR EVOLUTION; PHYLOGENY;

ANIMALS; DNA, MITOCHONDRIAL; EVOLUTION, MOLECULAR; FEMALE; GENETIC VARIATION; INBREEDING; LEPIDOPTERA; MALE; PHYLOGENY;

ANIMALIA; ERYNNIS; HESPERIIDAE; LEPIDOPTERA;

EID: 67349260399     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/hdy.2009.26     Document Type: Article

References (68)

1. Akaike H (1974). A new look at the statistical model identification. IEEE Trans Autom Contr 19: 716-723.
2. Andrews TD, Jermiin LS, Easteal S (1998). Accelerated evolution of cytochrome b in simian primates: adaptative evolution in concert with other mitochondrial proteins? J Mol Evol 47: 249-257.
3. Avise JC (2000). Phylogeography: The History and Formation of Species. Harvard University Press: Cambridge, MA.
4. Avise JC, Arnold RM, Ball RM, Bermingham E, Lamb T, Neigel JE et al. (1987). Instraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18: 489-522.
5. Avise JC, Walker D (1998). Pleistocene phylogeographic effects on avian populations and the speciation process. Proc R Soc Lond B Biol Sci 265: 457-463.
6. Babik W, Branicki W, Crnobrnja-Isailovic J, Cogalniceanu D, Sas I, Olgun K et al. (2005). Phylogeography of two European newt species - discordance between mtDNA and morphology. Mol Ecol 14: 2475-2491.
7. Baker JM, López-Medrano E, Navarro-Sigüenza AG, Rojas-Soto OR, Omland KE (2003). Recent speciation in the Orchard Oriole group: divergence of Icterus spurius spurius and Icterus spurius fuertesi. Auk 120: 848-859.
8. Ballard JWO (2000). When one is not enough: introgression of mitochondrial DNA in Drosophila. Mol Biol Evol 17: 1126-1130.
9. Ballard JWO, James AC (2004). Differential fitness of mitochondrial DNA in perturbation cage studies correlates with global abundance and population history in Drosophila simulans. Proc R Soc Lond B Biol Sci 271: 1197-1201.
10. Ballard JWO, Rand DM (2005). The population biology of mitochondrial DNA and its phylogenetic implications. Annu Rev Ecol Syst 36: 621-642.
11. Ballard JWO, Whitlock MC (2004). The incomplete natural history of mitochondria. Mol Ecol 13: 729-744.
12. Begun DJ, Holloway AK, Stevens K, Hillier LW, Poh YP, Hahn MW et al. (2007). Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol 5: e310. doi:10.1371/journal.pbio.0050310.
13. Bensasson D, Zhang D-X, Hartl DL, Hewitt GM (2001). Mitochondrial pseudogenes: evolution's misplaced witness. Trends Ecol Evol 16: 314-321.
14. Borisenko AV, Lim BK, Ivanova NV, Hanner RH, Hebert PDN (2008). DNA barcoding in surveys of small mammal communities: a field study in Suriname. Mol Ecol Resour 8: 471-479.
15. Brower AVZ, DeSalle R (1998). Patterns of mitochondrial versus nuclear DNA sequence divergence among nymphalid butterflies: the utility of wingless as a source of characters for phylogenetic inference. Insect Mol Biol 7: 1-10.
16. Burns JM (1964). Evolution in Skipper Butterflies of the genus Erynnis. Univ Calif Publ Entomol 37: 214pp.
17. Chan KMA, Levin SA (2005). Leaky prezygotic isolation and porous genomes: rapid introgression of maternally inherited DNA. Evolution 59: 720-729.
18. Clark AG (1990). Inference of haplotypes from PCR-amplified samples of diploid populations. Mol Biol Evol 7: 111-122.
19. Clary DO, Wolstenholme DR (1985). The mitochondrial DNA molecular of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol 22: 252-271.
20. de Stordeur E (1997). Nonrandom partition of mitochondria in heteroplasmic Drosophila. Heredity 79: 615-623.
21. Dean MD, Ballard JWO (2004). Linking phylogenetics with population genetics to reconstruct the geographic origin of a species. Mol Phylogenet Evol 32: 998-1009.
22. Donnelly P, Pinto J, Girod R, Besansky NJ, Lehmann T (2004). Revisiting the role of introgression vs shared ancestral polymorphisms as key processes in shaping genetic diversity in the recently separated sibling species of the Anopheles gambiae complex. Heredity 92: 61-68.
23. Dowling TW, Secor CL (1997). The role of hybridization and introgression in the diversification of animals. Annu Rev Ecol Syst 28: 593-619.
24. Forbes WTM (1936). The persius group of Thanaos (Lepidoptera, Hesperiidae). Psyche 43: 104-113.
25. Forister ML, Nice CC, Fordyce JA, Gompert Z, Shapiro AM (2008). Considering evolutionary processes in the use of single-locus genetic data for conservation, with examples from the Lepidoptera. J Insect Conserv 12: 37-51.
26. Funk DJ, Omland KE (2003). Species-level paraphyly and polyphyly: frequency, causes, consequences, with insights from animal mitochondrial DNA. Annu Rev Ecol Syst 34: 397-423.
27. Gompert Z, Fordyce JA, Forister ML, Shapiro AM, Nice CC (2006). Homoploid hybrid speciation in an extreme habitat. Science 314: 1923-1925.
28. Haldane JBS (1922). Sex ratio and unisexual sterility in hybrid animals. J Genet 12: 101-109.
29. Hariri AR, Werren JH, Wilkinson GS (1998). Distribution and reproductive effects of Wolbachia in stalk-eyed flies (Diptera: Diopsidae). Heredity 81: 254-260.
30. Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003a). Biological identification through DNA barcodes. Proc R Soc Lond B Biol Sci 270: 313-321.
31. Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004). Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA 101: 14812-14817.
32. Hebert PDN, Ratnasingham S, deWaard JR (2003b). Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond B 270(Suppl): S96-S99.
33. Huelsenbeck JP, Bollback JP (2001). Empirical and hierarchical Bayesian estimation of ancestral states. Syst Biol 50: 351-366.
34. Huelsenbeck JP, Ronquist F (2001). MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17: 754-755.
35. Hurst GDD, Jiggins FM (2005). Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc R Soc Lond B Biol Sci 272: 1525-1534.
36. Jiggins FM (2003). Male-killing Wolbachia and mitochondrial DNA: selective sweeps, hybrid introgression and parasite population dynamics. Genetics 164: 5-12.
37. Meglécz E, Petenian F, Danchin E, D'Acier AC, Rasplus JY, Faure E (2004). High similarity between flanking regions of different microsatellites detected within each of two species of Lepidoptera: Parnassius apollo and Euphydryas aurinia. Mol Ecol 13: 1693-1700.
38. Melo-Ferreira J, Boursot P, Suchentrunk F, Alves PC (2005). Invasion from the cold past: extensive introgression of mountain hare (Lepus timidus) mitochondrial DNA into three other hare species in northern Iberia. Mol Ecol 14: 2459-2464.
39. Morinaka S, Minaka N, Sekiguchi M, Erniwati E, Prijono SN, Ginarsa IK et al. (2000). Molecular phylogeny of birdwing butterflies of the tribe Troidini (Lepidoptera: Papilionidae)-using all species of the genus Ornithoptera. Biogeography 2: 103-111.
40. Narita S, Numura M, Kato Y, Fukatsu T (2006). Genetic structure of sibling butterfly species affected by Wolbachia infection sweep: evolutionary and biogeographical implications. Mol Ecol 15: 1095-1108.
41. Nazari V, Zakharov EV, Sperling FAH (2007). Phylogeny, historical biogeography, and taxonomic ranking of Parnas-siinae (Lepidoptera, Papilionidae) based on morphology and seven genes. Mol Phylogenet Evol 42: 131-156.
42. Nylander JAA (2004). MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre: Uppsala University.
43. Opler PA, Pavulaan H, Stanford RE, Pogue M coordinators (2006). Butterflies and moths of North America. Bozeman, MT: Mountain Prairie Information Node.http://www. butterfliesandmoths.org/.
44. Pelham JP (2008). A catalogue of the Butterflies of the United States and Canada. J Res Lepid 40: xiv +658 pp.
45. Peters JL, Zhuravlev Y, Fefelov I, Logie A, Omland K (2007). Nuclear loci and coalescent methods support ancient hybridization as cause of mitochondrial paraphyly between gadwall and falcated duck (Anas spp.). Evolution 61: 1992-2006.
46. Prager EM, Wilson AC (1975). Slow evolutionary loss of the potential for interspecific hybridization in birds: a manifestation of slow regulatory evolution. Proc Natl Acad Sci USA 72: 200-204.
47. Pritchard JK, Stephens M, Donnelly P (2000). Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
48. Regier JC, Cook CP, Mitter C, Hussey A (2008). A phylogenetic study of the bombycoid complex (Lepidoptera) using five protein-coding nuclear genes, with comments on the problem of macrolepidopteran phylogeny. Syst Entomol 33: 175-189.
49. Rokas A, Ladoukakis E, Zouros E (2003). Animal mitochondrial DNA recombination revisited. Trends Ecol Evol 18: 411-417.
50. Rubinoff D, Holland BS (2005). Between two extremes: mitochondrial DNA is neither the panacea nor the nemesis of phylogenetic and taxonomic inference. Syst Biol 54: 952-961.
51. Schwarz D, Matta BM, Shakir-Botteri NL, McPheron BA (2005). Host shift to an invasive plant triggers rapid animal hybrid speciation. Nature 436: 546-549.
52. Scriber JM, Ording GJ (2005). Ecological speciation without host plant specialization; possible origins of a recently described cryptic Papilio species. Entomol Exp Appl 115: 247-263.
53. Shaw KL (2002). Conflict between nuclear and mitochondrial DNA phylogenies of a recent species radiation: what mtDNA reveals and conceals about modes of speciation in Hawaiian crickets. Proc Natl Acad Sc USA 99: 16122-16127.
54. Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994). Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved PCR primers. Ann Entomol Soc Am 87: 651-701.
55. Slate J, Phua SH (2003). Patterns of linkage disequilibrium in mitochondrial DNA of 16 ruminant populations. Mol Ecol 12: 597-608.
56. Snook RR, Cleland SY, Wolfner MF, Karr TL (2000). Offsetting effects of Wolbachia infection and heat shock on sperm production in Drosophila simulans: analyses of fecundity, fertility and accessory gland proteins. Genetics 155: 167-178.
57. Stephens M, Donnelly P (2003). A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73: 1162-1169.
58. Stephens M, Smith NJ, Donnelly P (2001). A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68: 978-989.
59. Swofford DL (1998). PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods). Sinauer Associates: Sunderland, MA.
60. Thalmann O, Hebler J, Poinar HN, Pääbo S, Vigilant L (2004). Unreliable mtDNA data due to nuclear insertions: a cautionary tale from analysis of humans and other great apes. Mol Ecol 13: 321-335.
61. Turelli M, Hoffmann AA, Mckechnie W (1992). Dynamics of cytoplasmic incompatibility and mtDNA variation in natural Drosophila simulans populations. Genetics 132: 713-723.
62. Wahlberg N, Oliveira R, Scott J (2003). Phylogenetic relationships of Phyciodes butterfly species (Lepidoptera: Nympha-lidae): complex mtDNA variation and species delimitations. Syst Entomol 28: 257-273.
63. Wiemers M, Fiedler K (2007). Does the DNA barcoding gap exist? - A case study in blue butterflies (Lepidoptera: Lycaenidae). Front Zool 4: 8.
64. Winterton SL, Wiegmann BM, Schlinger EI (2007). Phylogeny and Bayesian divergence time estimations of small-headed flies (Diptera: Acroceridae) using multiple molecular markers. Mol Phylogenet Evol 43: 808-832.
65. Zakharov EV, Hellmann JJ (2008). Genetic differentiation across a latitudinal gradient in two co-occurring butterfly species: revealing population differences in a context of climate change. Mol Ecol 17: 189-208.
66. Zakharov EV, Hellmann JJ, Romero-Severson J (2007). Microsatellite loci in the Propertius duskywing, Erynnis propertius (Lepidoptera: Hesperiidae), and related species. Mol Ecol Notes 7: 266-268.
67. Zhang DX (2004). Lepidopteran microsatellite DNA: redundant but promising. Trends Ecol Evol 19: 507-509.
68. Zink RM, Barrowclough GF (2008). Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17: 2107-2121.