In the shadow of phylogenetic uncertainty: The recent diversification of Lysandra butterflies through chromosomal change

Molecular Phylogenetics and Evolution

Volumn 69, Issue 3, 2013, Pages 469-478

  Talavera, Gerard ^a,b,c   Lukhtanov, Vladimir A ^b,d   Rieppel, Lukas ^c,e   Pierce, Naomi E ^c   Vila, Roger ^a  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

^c HARVARD UNIVERSITY   (United States)

^d ZOOLOGICAL INSTITUTE   (Russian Federation)

^e BROWN UNIVERSITY   (United States)

Author keywords

Chromosomal evolution; Hybridization; Incomplete lineage sorting; Lepidoptera; Speciation; Species trees

Indexed keywords

LEPIDOPTERA; LYCAENIDAE; LYSANDRA; LYSANDRA BELLARGUS; LYSANDRA CORIDON; LYSANDRA OSSMAR; LYSANDRA SYRIACA; MYA; PAPILIONOIDEA; POLYOMMATINAE;

ANIMAL; ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; BUTTERFLY; CHROMOSOMAL EVOLUTION; CHROMOSOMAL INSTABILITY; CHROMOSOME; CLASSIFICATION; DNA SEQUENCE; GENETIC MARKER; GENETICS; HYBRIDIZATION; INCOMPLETE LINEAGE SORTING; KARYOTYPE; LEPIDOPTERA; MALE; MITOCHONDRION; MOLECULAR EVOLUTION; PHYLOGENY; SPECIES DIFFERENTIATION; SPECIES TREES;

CHROMOSOMAL EVOLUTION; HYBRIDIZATION; INCOMPLETE LINEAGE SORTING; LEPIDOPTERA; SPECIATION; SPECIES TREES;

ANIMALS; BAYES THEOREM; BUTTERFLIES; CHROMOSOMAL INSTABILITY; CHROMOSOMES; EVOLUTION, MOLECULAR; GENETIC MARKERS; HYBRIDIZATION, GENETIC; KARYOTYPE; MALE; MITOCHONDRIA; MODELS, GENETIC; PHYLOGENY; SEQUENCE ANALYSIS, DNA;

EID: 84884589888     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2013.08.004     Document Type: Article

References (62)

1. Ané C., Larget B., Baum D.A., Smith S.D., Rokas A. Bayesian estimation of concordance among gene trees. Mol. Biol. Evol. 2007, 24:412-426.
2. Baker R.J., Bickham J.W. Speciation by monobrachial centric fusion. Proc. Natl. Acad. Sci. USA 1986, 83:8245-8248.
3. Berthier P., Excoffier L., Ruedi M. Recurrent replacement of mtDNA and cryptic hybridization between two sibling bat species Myotis myotis and Myotis blythii. Proc. R. Soc. B 2006, 273:3101-3109.
4. Bossu C.M., Near T.J. Gene trees reveal repeated instances of mitochondrial DNA introgression in orangethroat darters (Percidae: Etheostoma). Syst. Biol. 2009, 58:114-129.
5. Bouckaert R.R. DensiTree: making sense of sets of phylogenetic trees. Bioinformatics 2010, 26:1372-1373.
6. Bryant D., Moulton V. Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol. Biol. Evol. 2004, 21:255-265.
7. Buckley T.R., Cordeiro M., Marshall D.C., Simon C. Differentiating between hypotheses of lineage sorting and introgression in New Zealand alpine cicadas (Maoricicada Dugdale). Syst. Biol. 2006, 55:411-425.
8. Coutsis J., de Prins J., de Prins W. The chromosome number and karyotype of the two morphs of Polyommatus (Lysandra) coridon from Greece (Lepidoptera:Lycaenidae). Phegea 2001, 29:63-71.
9. De Bast B. La notion d'espéce dans le genre Lysandra Hemming, 1933 (Lepidoptera Lycaenidae). Linn. Belg. 1985, 10:98-110.
10. de Lesse H. Spéciation et variation chromosomique chez les Lépidoptères Rhopalocères. Ann. Sci. Nat. 1960, 2:1-223.
11. de Lesse H. Les nombres des chromosomes dans le groupe de Lysandra coridon (Lep. Lycaenidae). Ann. Soc. Entomol. Fr. 1969, 5:469-532.
12. Descimon H., Mallet J. Bad species. Ecology of Butterflies in Europe 2009, Cambridge University Press, Cambridge. J. Settele, T.G. Shreeve, M. Konvicka, H. Van Dyck (Eds.).
13. Dincǎ V., Zakharov E.V., Hebert P.D.N., Vila R. Complete DNA barcode reference library for a country's butterfly fauna reveals high performance for temperate Europe. Proc. R. Soc. B 2011, 278:347-355.
14. Edwards S.V. Is a new and general theory of molecular systematics emerging?. Evolution 2009, 63:1-19.
15. Faria R., Navarro A. Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol. Evol. 2010, 25:660-669.
16. Ferris S.D., Sage R.D., Huangj C.M., Nielsen J.T., Ritte U., Wilson A.C. Flow of mitochondrial DNA across species boundary. Proc. Natl. Acad. Sci. USA 1983, 80:2290-2294.
17. Gauthier O., Lapointe F.J. Seeing the trees for the network: consensus, information content, and superphylogenies. Syst. Biol. 2007, 56:345-355.
18. Gil-T F. A natural hybrid of Polyommatus bellargus (Rottemburg, 1775)×P. albicans (Herrich-Schäffer, 1852) and notes about a probable hybrid of P. punctifera (Oberthür, 1876)×P. albicans (Lepid.: Lycaenidae). Nachr. Ent. Ver. Apollo 2007, 28:11-13.
19. Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 2010, 59:307-321.
20. Heled J., Drummond A. Bayesian inference of species trees from multilocus data. Mol. Biol. Evol. 2010, 27:570-580.
21. Hesselbarth, G., Van Oorschot, H., Wagener, S., 1995. Die Tagfalter der Türkei unter Berücksichtigung der angrenzenden Länder.
22. Jin G., Nakhleh L., Snir S., Tuller T. Maximum likelihood of phylogenetic networks. Bioinformatics 2006, 22:2604-2611.
23. Joly S. JML: testing hybridization from species trees. Mol. Ecol. Resour. 2012, 12:179-184.
24. Joly S., McLenachan P.A., Lockhart P.J. A statistical approach for distinguishing hybridization and incomplete lineage sorting. Am. Nat. 2009, 174:e54-e70.
25. Kandul N.P., Coleman J.W.S., Lukhtanov V.A., Dantchenko D.A., Sekercioglu C., Haig D., Pierce N.E. Phylogeny of Agrodiaetus Hübner 1822 (Lepidoptera: Lycaenidae) inferred from mtDNA sequences of COI and COII, and Nuclear Sequences of EF1-α: karyotype diversification and species radiation. Syst. Biol. 2004, 53:278-298.
26. Kandul N.P., Lukhtanov V.A., Pierce N.P. Karyotypic diversity and speciation in Agrodiaetus butterflies. Evolution 2007, 61:546-558.
27. King M. Species Evolution: The Role of Chromosomal Change 1993, Cambridge University Press, Cambridge.
28. Kubatko L.S. Identifying hybridization events in the presence of coalescence via model selection. Syst. Biol. 2009, 58:478-488.
29. Lelièvre, T., 1992. Phylogénie des Polyommatinae et structure génétique de six espèces du genre Lysandra Hemming (Lepidptères Lycaenidae). Thèse doctorat, Université de Provence, 219 pp.
30. Lorković Z. Die Chromosomenzahlen in der Spermatogenese der Tagfalter. Chromosoma 1941, 2:155-191.
31. Lorković Z. Chromosomen-Vervielfachung bei Schmetterlingen und ein neuer Fall fünffacher Zahl. Rev. Suisse Zool. 1949, 56:243-249.
32. Lorković, Z., 1990. The butterfly chromosomes and their application in systematics and phylogeny. In: Kudrna, O. (Ed.), Butterflies of Europe 2. Aula-Verlag, Wiesbaden, pp. 332-396.
33. Lukhtanov V.A., Dantchenko A.V. Principles of highly ordered metaphase I bivalent arrangement in spermatocytes of Agrodiaetus (Lepidoptera). Chromosome Res. 2002, 10:5-20.
34. Lukhtanov V.A., Kuznetsova V.G. What genes and chromosomes say about the origin and evolution of insects and other arthropods. Russ. J. Genet. 2010, 46:1115-1121.
35. Lukhtanov V.A., Kandul N.P., Plotkin J.B., Dantchenko A.V., Haig D., Pierce N.E. Reinforcement of pre-zygotic isolation and karyotype evolution in Agrodiaetus butterflies. Nature 2005, 436:385-389.
36. Lukhtanov V.A., Vila R., Kandul N.P. Rearrangement of the Agrodiaetus dolus species group (Lepidoptera, Lycaenidae) using a new cytological approach and molecular data. Insect Syst. Evol. 2006, 37:325-334.
37. Lukhtanov V.A., Shapoval N.A., Dantchenko A.V. Agrodiaetus shahkuhensis sp. n. (Lepidoptera, Lycaenidae), a cryptic species from Iran discovered by using molecular and chromosomal markers. Comp. Cytogenet. 2008, 2:99-114.
38. Lukhtanov V.A., Dinca V., Talavera G., Vila R. Unprecedented within-species chromosome number cline in the Wood White butterfly Leptidea sinapis and its significance for karyotype evolution and speciation. BMC Evol. Biol. 2011, 11:109.
39. Lyapunova E.A., Bakloushinskaya I.Y., Saidov A.S., Saidov K.K. Dynamics of chromosome variation in mole voles Ellobius tancrei (Mammalia, Rodentia) in Pamiro-Alai in the period from 1982 to 2008. Russ. J. Genet. 2010, 46:566-571.
40. Magallon S., Sanderson M.J. Absolute diversification rates in angiosperm clades. Evolution 2000, 55:1762-1780.
41. Mallet J. Hybrid speciation. Nature 2007, 446:279-283.
42. Melo-Ferreira J., Boursot P., Carneiro M., Esteves P.J., Farelo L., Alves P.C. Recurrent introgression of mitochondrial DNA among hares (Lepus spp.) revealed by species-tree inference and coalescent simulations. Syst. Biol. 2012, 61:367-381.
43. Mensi P., Lattes A., Salvidio S., Balleto E. Taxonomy, evolutionary biology and biogeography of South West European Polyommatus coridon (Lepidoptera: Lycaenidae). Zool. J. Linn. Soc. 1988, 93:259-271.
44. Pino Pérez J.J., Pino Pérez R. Una población de Lysandra coridon (Poda, 1761) en la costa de A Coruña, Galicia (NW de España). Bol. BIGA 2013, 1:49-52.
45. Posada D. JModelTest: phylogenetic model averaging. Mol. Biol. Evol. 2008, 25:1253-1256.
46. Quek S.P., Davies S.J., Itino T., Pierce N.E. Codiversification in an ant-plant mutualism: stem texture and the evolution of host use in Crematogaster (Formicidae: Myrmicinae) inhabitants of Macaranga (Euphorbiaceae). Evolution 2004, 58:554-570.
47. Rambaut A., Grassly N.C. Seq-Gen: an application for the monte carlo simulation of DNA sequence evolution along phylogenetic trees. Comput. Appl. Biosci. 1997, 13:235-238.
48. Rieppel, L., 2012. Karyotype evolution and phylogeography in Lysandra coridon (Lycaenidae). Master's Thesis. Harvard University, Department of Organismic and Evolutionary Biology.
49. Robinson R. Lepidoptera Genetics 1971, Pergamon Press, Oxford.
50. Roca A.L., Georgiadis N., O'Brien S.J. Cytonuclear genomic dissociation in African elephant species. Nat. Genet. 2005, 37:96-100.
51. Ruedi M., Smith M.F., Patton J.L. Phylogenetic evidence of mitochondrial DNA introgression among pocket gophers in New Mexico (family Geomyidae). Mol. Ecol. 1997, 6:453-462.
52. Schurian K.G. Revision der Lysandra-Gruppe des Genus Polyommatus Latr. (Lepidoptera: Lycaenidae). Neue Entomol. Nachr. 1989, 24:1-181.
53. Spinks P.Q., Shaffer H.B. Conflicting mitochondrial and nuclear phylogenies for the widely disjunct ewmys (Testudines: Emydidae) species complex, and what they tell us about biogeography and hybridization. Syst. Biol. 2009, 58:1-20.
54. Stekolnikov A.A., Ivanov V.A., Kuznetzov V.I., Lukhtanov V.A. Evolution of the chromosome mechanism, wing articulation, male genitalia and phylogeny of Butterflies (Lepidoptera: Hesperioidea, Papilionoidea). Entomol. Obozrenie 2000, 79:123-149.
55. Stradomsky B.V., Shchurov V.I. Notes on the status of the Caucasia taxa of the group Polyommatus (Meleageria) coridon (sensu de Lesse) with description of a new species from the high-mountain area of West Caucasia (Lepidoptera: Lycaenidae). Phegea 2005, 33:69-75.
56. Talavera G., Lukhtanov V.A., Pierce N.E., Vila R. Establishing criteria for higher-level classification using molecular data: the systematics of Polyommatus blue butterflies (Lepidoptera, Lycaenidae). Cladistics 2013, 29:166-192.
57. Vershinina A.O., Lukhtanov V.A. Geographical distribution of the cryptic species Agrodiaetus alcestis alcestis, A. alcestis karacetinae and A. demavendi (Lepidoptera, Lycaenidae) revealed by cytogenetic analysis. Comp. Cytogenet. 2010, 4:1-11.
58. Vila R., Lukhtanov V.A., Talavera G., Gil T.F., Pierce N.E. How common are dot-like distribution ranges? Taxonomical oversplitting in Western European Agrodiaetus (Lepidoptera, Lycaenidae) revealed by chromosomal and molecular markers. Biol. J. Linn. Soc. 2010, 101:130-154.
59. Vila R., Bell C.D., Macniven R., Goldman-Huertas B., Ree R.H., Marshall C.R., Bálint Z., Johnson K., Benyamini D., Pierce N.E. Phylogeny and palaeoecology of Polyommatus blue butterflies show Beringia was a climate-regulated gateway to the New World. Proc. R. Soc. B 2011, 278:2737-2744.
60. White M.J.D. Animal Cytology and Evolution 1973, Cambridge University Press, Cambridge.
61. Wiemers, M., 2003. Chromosome Differentiation and the Radiation of the Butterfly Subgenus Agrodiaetus (Lepidoptera: Lycaenidae: Polyommatus) - A Molecular Phylogenetic Approach. PhD Thesis, University of Bonn. <>. http://hss.ulb.uni-bonn.de/2003/0278/0278.htm.
62. Wolf K.W. The structure of condensed chromosomes in mitosis and meiosis of insects. Int. J. Insect Morphol. Embryol. 1996, 25:37-62.