What does mitogenomics tell us about the evolutionary history of the Drosophila buzzatii cluster (repleta group)?


Autoři: Nicolás Nahuel Moreyra aff001;  Julián Mensch aff001;  Juan Hurtado aff001;  Francisca Almeida aff001;  Cecilia Laprida aff001;  Esteban Hasson aff001
Působiště autorů: Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Autónoma de Buenos Aires, Argentina aff001;  Instituto de Ecología, Genética y Evolución de Buenos Aires, Consejo Nacional de Investigaciones Científicas y Técnicas, Ciudad Autónoma de Buenos Aires, Argentina aff002;  Instituto de Estudios Andinos, CONICET/UBA, Ciudad Autónoma de Buenos Aires, Argentina aff003
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0220676

Souhrn

The Drosophila repleta group is an array of more than 100 species endemic to the “New World”, many of which are cactophilic. The ability to utilize decaying cactus tissues as breeding and feeding sites is a key aspect that allowed the successful diversification of the repleta group in American deserts and arid lands. Within this group, the Drosophila buzzatii cluster is a South American clade of seven closely related species in different stages of divergence, making them a valuable model system for evolutionary research. Substantial effort has been devoted to elucidating the phylogenetic relationships among members of the D. buzzatii cluster, including molecular phylogenetic studies that have generated ambiguous results where different tree topologies have resulted dependent on the kinds of molecular marker used. Even though mitochondrial DNA regions have become useful markers in evolutionary biology and population genetics, none of the more than twenty Drosophila mitogenomes assembled so far includes this cluster. Here, we report the assembly of six complete mitogenomes of five species: D. antonietae, D. borborema, D. buzzatii, two strains of D. koepferae and D. seriema, with the aim of revisiting phylogenetic relationships and divergence times by means of mitogenomic analyses. Our recovered topology using complete mitogenomes supports the hypothesis of monophyly of the D. buzzatii cluster and shows two main clades, one including D. buzzatii and D. koepferae (both strains), and the other containing the remaining species. These results are in agreement with previous reports based on a few mitochondrial and/or nuclear genes, but conflict with the results of a recent large-scale nuclear phylogeny, indicating that nuclear and mitochondrial genomes depict different evolutionary histories.

Klíčová slova:

Animal phylogenetics – Drosophila melanogaster – Invertebrate genomics – Mitochondria – Paleogenetics – Phylogenetic analysis – Phylogenetics – Sequence alignment


Zdroje

1. Hahn C, Bachmann L, Chevreux B. Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads—A baiting and iterative mapping approach. Nucleic Acids Res. 2013;41(13): e129–e129. doi: 10.1093/nar/gkt371 23661685

2. Tian Y, Smith DR. Recovering complete mitochondrial genome sequences from RNA-Seq: A case study of Polytomella non-photosynthetic green algae. Mol Phylogenet Evol. 2016;98: 57–62. doi: 10.1016/j.ympev.2016.01.017 26860338

3. Smith DR. The past, present and future of mitochondrial genomics: Have we sequenced enough mtDNAs? Brief Funct Genomics. 2016;15(1): 47–54. doi: 10.1093/bfgp/elv027 26117139

4. Osigus HJ, Eitel M, Bernt M, Donath A, Schierwater B. Mitogenomics at the base of Metazoa. Mol Phylogenet Evol. 2013;69: 339–351. doi: 10.1016/j.ympev.2013.07.016 23891951

5. Roos J, Aggarwal RK, Janke A. Extended mitogenomic phylogenetic analyses yield new insight into crocodylian evolution and their survival of the Cretaceous-Tertiary boundary. Mol Phylogenet Evol. 2007;45: 663–673. doi: 10.1016/j.ympev.2007.06.018 17719245

6. Finstermeier K, Zinner D, Brameier M, Meyer M, Kreuz E, Hofreiter M, et al. A Mitogenomic Phylogeny of Living Primates. PLoS ONE. 2013;8(7): e69504. doi: 10.1371/journal.pone.0069504 23874967

7. Saitoh K, Sado T, Mayden RL, Hanzawa N, Nakamura K, Nishida M, et al. Mitogenomic Evolution and Interrelationships of the Cypriniformes (Actinopterygii: Ostariophysi): The First Evidence Toward Resolution of Higher-Level Relationships of the World’s Largest Freshwater Fish Clade Based on 59 Whole Mitogenome Sequences. J Mol Evol. 2006;63: 826–841. doi: 10.1007/s00239-005-0293-y 17086453

8. Zhang P, Liang D, Mao RL, Hillis DM, Wake DB, Cannatella DC. Efficient Sequencing of Anuran mtDNAs and a Mitogenomic Exploration of the Phylogeny and Evolution of Frogs. Mol Biol Evol. 2013;30(8): 1899–1915. doi: 10.1093/molbev/mst091 23666244

9. Montooth KL, Abt DN, Hofmann JW, Rand DM. Comparative genomics of Drosophila mtDNA: novel features of conservation and change across functional domains and lineages. J Mol Evol. 2009;69(1): 94. doi: 10.1007/s00239-009-9255-0 19533212

10. Cameron SL. Insect Mitochondrial Genomics: Implications for Evolution and Phylogeny. Annu Rev Entomol. 2001;59(1): 95–117.

11. Duchêne S, Archer FI, Vilstrup J, Caballero S, Morin PA. Mitogenome Phylogenetics: The Impact of Using Single Regions and Partitioning Schemes on Topology, Substitution Rate and Divergence Time Estimation. PLoS ONE. 2011;6(11): e27138. doi: 10.1371/journal.pone.0027138 22073275

12. Rohland N, Malaspinas AS, Pollack JL, Slatkin M, Matheus P, Hofreiter M. Proboscidean mitogenomics: chronology and mastodon as outgroup. PLoS Biol. 2007;5: e207. doi: 10.1371/journal.pbio.0050207 17676977

13. Willerslev E, Gilbert T, Binladen J, Ho SYW, Campos PF, Ratan A, et al. Analysis of complete mitochondrial genomes from extinct and extant Rhinoceroses reveals lack of phylogenetic resolution. BMC Evol Biol. 2009;9: 95. doi: 10.1186/1471-2148-9-95 19432984

14. Knaus BJ, Cronn R, Liston A, Pilgrim K, Schwartz MK. Mitochondrial genome sequences illuminate maternal lineages of conservation concern in a rare carnivore. BMC Ecol. 2011;11: 10. doi: 10.1186/1472-6785-11-10 21507265

15. Luo A, Zhang A, Ho SYW, Xu W, Zhang Y, Shi W, et al. Potential efficacy of mitochondrial genes for animal DNA barcoding: a case study using eutherian mammals. BMC Genomics. 2011;12: 84. doi: 10.1186/1471-2164-12-84 21276253

16. Pacheco MA, Battistuzzi FU, Lentino M, Aguilar R, Kumar S, Escalante AA. Evolution of modern birds revealed by mitogenomics: timing the radiation and origin of major orders. Mol Biol Evol. 2011;28: 1927–1942. doi: 10.1093/molbev/msr014 21242529

17. Balloux F. The worm in the fruit of the mitochondrial DNA tree. Heredity. 2010;104: 419–420. doi: 10.1038/hdy.2009.122 19756036

18. Pamilo P, Nei M. Relationships between gene trees and species trees. Mol Biol Evol. 1988;5(5): 568–583. doi: 10.1093/oxfordjournals.molbev.a040517 3193878

19. Maddison WP. Gene trees in species trees. Syst Biol. 1997;46(3): 523–536.

20. Zachos FE. Gene trees and species trees–mutual influences and interdependences of population genetics and systematics. J Zool Syst Evol Res. 2009;47(3): 209–218.

21. Bächli G. [Internet]. TaxoDros: the database on taxonomy of Drosophilidae, v. 1.04. Database 2011/1. Available from: https://www.taxodros.uzh.ch/.

22. Markow TA, O’Grady P. Reproductive ecology of Drosophila. Funct Ecol. 2008;22(5): 747–759.

23. Markow TA, O’Grady P. Drosophila: A guide to species identification and use. Elsevier; 2005.

24. O’Grady PM, DeSalle R. Phylogeny of the genus Drosophila. Genetics. 2018;209(1): 1–25. doi: 10.1534/genetics.117.300583 29716983

25. Markow TA. Host use and host shifts in Drosophila. Curr Opin Insect Sci. 2019;31: 139–145. doi: 10.1016/j.cois.2019.01.006 31109667

26. Oliveira DCSG, Almeida FC, O’Grady PM, Armella MA, DeSalle R, Etges WJ. Monophyly, divergence times, and evolution of host plant use inferred from a revised phylogeny of the Drosophila repleta species group. Mol Phylogenet Evol. 2012;64(3): 533–544. doi: 10.1016/j.ympev.2012.05.012 22634936

27. Morales-Hojas R, Vieira J. Phylogenetic Patterns of Geographical and Ecological Diversification in the Subgenus Drosophila. PLoS ONE. 2012;7(11): e49552. doi: 10.1371/journal.pone.0049552 23152919

28. Heed WB. Ecology and genetics of Sonoran desert Drosophila. In: Brussard PF, editors. Ecological Genetics: The Interface. Proceedings in Life Sciences. Springer, New York, NY; 1978. pp. 109–126.

29. Barker JS, Starmer W. Ecological Genetics and Evolution: The Cactus-Yeast-Drosophila Model System. Academic Pr; 1982.

30. Heed WB, Mangan RL. Community ecology of Sonoran Desert Drosophila. In: Asburner M., Carson H., Thompson J. N., editors. The genetics and biology of Drosophila. Academic, London; 1986. pp. 311–345.

31. Hasson E, Naveira H, Fontdevila A. The Breeding Sites of Argentinean Cactophilic Species of the Drosophila-Mulleri Complex (Subgenus Drosophila-Repleta Group). Rev. Chil. Hist. Nat. 1992;65(3): 319–326.

32. Fogleman JC, Danielson PB. Chemical interactions in the Cactus-Microorganism-Drosophila Model System of the Sonoran Desert. Am Zool, 2001;41(4): 877–889.

33. Guillén Y, Rius N, Delprat A, Williford A, Muyas F, Puig M, et al. Genomics of ecological adaptation in cactophilic Drosophila. Genome Biol Evol. 2014;7(1): 349–366. doi: 10.1093/gbe/evu291 25552534

34. De Panis DN, Padró J, Furió Tarí P, Tarazona S, Milla Carmona PS, Soto IM, et al. Transcriptome modulation during host shift is driven by secondary metabolites in desert Drosophila. Mol Ecol. 2016;25(18): 4534–4550. doi: 10.1111/mec.13785 27483442

35. Hasson E, De Panis D, Hurtado J, Mensch J. Host plant adaptation in cactophilic species of the Drosophila buzzatii cluster: fitness and transcriptomics. J Hered. 2019;110(1): 46–57. doi: 10.1093/jhered/esy043 30107510

36. Throckmorton LH. The Phylogeny, Ecology, and Geography of Drosophila. In: King RC, editors. Plenum Publishing Corporation, New York, New York; 1975. vol. 3, pp. 421–469.

37. Wasserman M. Evolution in the repleta group. In: Ashburner M, Carson HL, Thompson JN, editors. The genetics and Biology of Drosophila. Academic Press, London; 1982. pp. 61–139.

38. Vilela CA. A revision of the Drosophila species group. (Diptera-Drosophilidae). Rev Bras Entomol. 1983;27, 1±114.

39. Markow TA, O’Grady P. Drosophila: A guide to species identification and use. Elsevier; 2006.

40. Drosophila 12 Genomes Consortium. Evolution of genes and genomes on the Drosophila phylogeny. Nature. 2007;450(7167): 203–218. doi: 10.1038/nature06341 17994087

41. Ruiz A, Wasserman M. Evolutionary cytogenetics of the drosophila buzzatii species complex. Heredity (Edinb). 1993;70(6): 582–596.

42. Tidon-Sklorz R, Sene FM. Two new species of the Drosophila serido sibling set (Diptera, Drosophilidae). Iheringia Ser. Zool. Iheringia. 2001;(90): 141–146.

43. Vilela CR, Sene FM. Two new Neotropical species of the repleta group of the genus Drosophila (Diptera, Drosophilidae). Pap Avulsos Zool. 1977;30(20): 295–299.

44. Patterson JT, Wheeler MR. Description of new species of the subgenera Hirtodrosophila and Drosophila. University of Texas. 1942.

45. Fontdevila A, Pla C, Hasson E, Wasserman M, Sanchez A, Naveira H, et al. Drosophila koepferae: a new member of the Drosophila serido (Diptera: Drosophilidae) superspecies taxon. Ann Entomol Soc Am. 1988;81(3): 380–385.

46. Tidon-Sklorz R, De Melo Sene F. Drosophila seriema n. sp.: new member of the Drosophila serido (Diptera: Drosophilidae) superspecies taxon. Ann Entomol Soc Am. 1995;88(2): 139–142.

47. Fontdevila A. Founder Effects in Colonizing Populations: The Case of Drosophila buzzatii. In: Fontdevila A, editors. Evolutionary Biology of Transient Unstable Populations. Springer, New York, NY; 1989. pp. 74–95.

48. Manfrin MH, Sene FM. Cactophilic Drosophila in South America: A model for evolutionary studies. Genetica, 2006;126(1–2): 57–75. doi: 10.1007/s10709-005-1432-5 16502085

49. Barrios-Leal DY, Neves-Da-Rocha J, Manfrin MH. Genetics and Distribution Modeling: The Demographic History of the Cactophilic Drosophila buzzatii Species Cluster in Open Areas of South America. J Hered. 2019;110(1): 22–33. doi: 10.1093/jhered/esy042 30252085

50. Hurtado J, Almeida F, Revale S, Hasson E. Revised phylogenetic relationships within the Drosophila buzzatii species cluster (Diptera: Drosophilidae: Drosophila repleta group) using genomic data. Arthropod Systematics and Phylogeny. 2019;77(2): 239–250.

51. Hasson E, Soto IM, Carreira VP, Corio C, Soto EM, Betti M. Host plants, fitness and developmental instability in a guild of cactophilic species of the genus Drosophila. In: Santos EB, editors. Ecotoxicology research developments. Nova Science Publishers, Inc; 2009. pp. 89–109.

52. Ruiz A, Cansian AM, Kuhn GC, Alves MA, Sene FM. The Drosophila serido speciation puzzle: putting new pieces together. Genetica. 2000;108(3): 217–227. doi: 10.1023/a:1004195007178 11294608

53. Manfrin MH, de Brito ROA, Sene FM. Systematics and Evolution of the Drosophila buzzatii (Diptera: Drosophilidae) Cluster Using mtDNA. Ann Entomol Soc Am. 2001;94(3): 333–346.

54. Franco FF, Silva-Bernardi ECC, Sene FM, Hasson ER, Manfrin MH. Intra‐and interspecific divergence in the nuclear sequences of the clock gene period in species of the Drosophila buzzatii cluster. J Zool Syst Evol Res. 2010;48(4): 322–331.

55. Rodríguez-Trelles F, Alarcón L, Fontdevila A. Molecular evolution and phylogeny of the buzzatii complex (Drosophila repleta group): A maximum-likelihood approach. Mol Biol Evol. 2000;17(7): 1112–1122. doi: 10.1093/oxfordjournals.molbev.a026392 10889224

56. de Lima LG, Svartman M, Kuhn GCS. Dissecting the Satellite DNA Landscape in Three Cactophilic Drosophila Sequenced Genomes. G3 (Bethesda). 2017;7(8): 2831–2843.

57. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4): 357–359. doi: 10.1038/nmeth.1923 22388286

58. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25(16): 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943

59. Chevreux B, Pfisterer T, Drescher B, Driesel AJ, Müller WEG, Wetter T. et al. Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res. 2004;14(6): 1147–1159. doi: 10.1101/gr.1917404 15140833

60. Sievers F, Higgins DG. Clustal omega. Curr Protoc Bioinformatics. 2014;48(1): 3–13.

61. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6): 1547–1549. doi: 10.1093/molbev/msy096 29722887

62. Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, et al. MITOS: Improved de novo metazoan mitochondrial genome annotation. Mol Phylogenet Evol. 2013;69(2): 313–319. doi: 10.1016/j.ympev.2012.08.023 22982435

63. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrated genomics viewer. Nat Biotechnol. 2011;29(1): 24–26. doi: 10.1038/nbt.1754 21221095

64. Yang Z. PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007;24: 1586–1591. doi: 10.1093/molbev/msm088 17483113

65. Gouy M, Guindon S, Gascuel O. Sea view version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 2010;27(2): 221–224. doi: 10.1093/molbev/msp259 19854763

66. Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B. Partitionfinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol. 2017;34(3): 772–773. doi: 10.1093/molbev/msw260 28013191

67. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19(12): 1572–1574. doi: 10.1093/bioinformatics/btg180 12912839

68. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7. Syst Biol. 2018;67(5): 901–904. doi: 10.1093/sysbio/syy032 29718447

69. Rambaut A. FigTree: Tree Figure Drawing Tool [software]. 2007. Available online from: http://tree.bio.ed.ac.uk/software/figtree.

70. Stamatakis A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9): 1312–1313. doi: 10.1093/bioinformatics/btu033 24451623

71. Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 2018;4: vey016. doi: 10.1093/ve/vey016 29942656

72. Haag-Liautard C, Coffey N, Houle D, Lynch M, Charlesworth B, Keightley PD. Direct estimation of the mitochondrial DNA mutation rate in Drosophila melanogaster. PLoS Biol. 2008;6(8): 1706–1714.

73. Tamura K, Subramanian S, Kumar S. Temporal Patterns of Fruit Fly (Drosophila) Evolution Revealed by Mutation Clocks. Mol Biol Evol. 2014;21: 36–44.

74. D'Onorio de Meo P, D'Antonio M, Griggio F, Lupi R, Borsani M, Pavesi G, et al. MitoZoa 2.0: a database resource and search tools for comparative and evolutionary analyses of mitochondrial genomes in Metazoa. Nucleic Acids Res. 2011;40(D1): D1168–D1172.

75. Stoletzki N, Eyre-Walker A. Synonymous codon usage in Escherichia coli: selection for translational accuracy. Mol Biol Evol. 2007;24: 374–81. doi: 10.1093/molbev/msl166 17101719

76. Franco FF, Manfrin MH. Recent demographic history of cactophilic Drosophila species can be related to Quaternary palaeoclimatic changes in South America. J Biogeogr. 2013;40(1): 142–154.

77. Subramanian S. Temporal trails of natural selection in human mitogenomes. Mol Biol Evol. 2009;26: 715–717. doi: 10.1093/molbev/msp005 19150805

78. Subramanian S, Denver DR, Millar CD, Heupink T, Aschrafi A, Emslie SD, et al. High mitogenomic evolutionary rates and time dependency. Trends Genet. 2009;25: 482–486. doi: 10.1016/j.tig.2009.09.005 19836098

79. Ho SY, Lanfear R, Bormham L, Phillips MJ, Soubrier J, Rodrigo AG, et al. Time-dependent rates of molecular evolution. Mol Ecol. 2011;20: 3087–3101. doi: 10.1111/j.1365-294X.2011.05178.x 21740474

80. Ballard JWO. Comparative genomics of mitochondrial DNA in Drosophila simulans. J Mol Evol. 2000;51(1): 64–75. doi: 10.1007/s002390010067 10903373

81. Brown WM, George M, Wilson AC. Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci U S A. 1979;76(4): 1967–1971. doi: 10.1073/pnas.76.4.1967 109836

82. Toews DP, Brelsford A. The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology. 2012;21(16): 3907–3930. doi: 10.1111/j.1365-294X.2012.05664.x 22738314

83. Powell JR. Interspecific cytoplasmic gene flow in the absence of nuclear gene flow: evidence from Drosophila. Proc Natl Acad Sci U S A. 1983;80(2): 492–495. doi: 10.1073/pnas.80.2.492 6300849

84. Bachtrog D, Thornton K, Clark A, Andolfatto P. Extensive introgression of mitochondrial DNA relative to nuclear genes in the Drosophila yakuba species group. Evolution (N Y). 2006;60(2): 292–302.

85. Aubert J, Solignac M. Experimental evidence for mitochondrial DNA introgression between Drosophila species. Evolution (NY). 1990;44(5): 1272–1282.

86. Wong A, Jensen JD, Pool JE, Aquadro CF. Phylogenetic incongruence in the Drosophila melanogaster species group. Mol Phylogenet Evol. 2007;43(3): 1138–1150. doi: 10.1016/j.ympev.2006.09.002 17071113

87. Chan KMA, Levin SA. Leaky prezygotic isolation and porous genomes: rapid introgression of maternally inherited DNA. Evolution (NY). 2005;59: 720–729.

88. Keck BP, Near TJ. Geographic and temporal aspects of mitochondrial replacement in Nothonotus darters (Teleostei: Percidae: Etheostomatinae). Evolution. 2010;64(5): 1410–428. doi: 10.1111/j.1558-5646.2009.00901.x 19930456

89. Gómez GA, Hasson E. Transpecific polymorphisms in an inversion linked esterase locus in Drosophila buzzatii. Mol Biol Evol. 2003;20(3): 410–423. doi: 10.1093/molbev/msg051 12644562

90. Piccinali R, Aguadé M, Hasson E. Comparative molecular population genetics of the Xdh locus in the cactophilic sibling species Drosophila buzzatii and D. koepferae. Mol Biol Evol. 2004;21(1): 141–152. doi: 10.1093/molbev/msh006 14595098

91. Madi-Ravazzi L, Bicudo HE, Manzato JA. Reproductive compatibility and chromosome pairing in the Drosophila buzzatii complex. Cytobios. 1997;89(356): 21–30. 9297813

92. Machado LPB, Madi-Ravazzi L, Tadei WJ. Reproductive relationships and degree of synapsis in the polytene chromosomes of the Drosophila buzzatii species cluster. Braz J Biol. 2006;66(1B): 279–293. doi: 10.1590/s1519-69842006000200010 16710520

93. Soto IM, Carreira VP, Fanara JJ, Hasson E. Evolution of male genitalia: environmental and genetic factors affect genital morphology in two Drosophila sibling species and their hybrids. BMC Evol Biol. 2007;7(1): 77.

94. Soto EM, Soto IM, Carreira VP, Fanara JJ, Hasson E. Host‐related life history traits in interspecific hybrids of cactophilic Drosophila. Entomol Exp Appl. 2008;126(1): 18–27.

95. Iglesias PP, Hasson E. The role of courtship song in female mate choice in South American Cactophilic Drosophila. PLoS ONE. 2017;12(5): e0176119. doi: 10.1371/journal.pone.0176119 28467464

96. Haffer J. Speciation in Amazonian forest birds. Science. 1969;165: 131–137. doi: 10.1126/science.165.3889.131 17834730

97. Endler JA. Problems in distinguishing historical from ecological factors in biogeography. Am Zool. 1982;22(2): 441–452.

98. Rull V. Neotropical biodiversity: timing and potential drivers. Trends Ecol Evol. 2011;26(10): 508–513. doi: 10.1016/j.tree.2011.05.011 21703715

99. Hoorn C, Wesselingh FP, Ter Steege H, Bermudez MA, Mora A, Sevink J, et al. Response to Origins of Biodiversity. Science 2011;331: 399–400.

100. Lagomarsino LP, Condamine FL, Antonelli A, Mulch A, Davis CC. The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae). New Phytol. 2016;210: 1430–1442. doi: 10.1111/nph.13920 26990796

101. Lisiecki LE, Raymo ME. A Pliocene-Pleistocene stack of globally distributed benthic stable oxygen isotope records. Paleoceanography. 2005;20: 1–17.

102. Mosblech NA, Bush MB, Gosling WD, Hodell D, Thomas L, Van Calsteren P. North Atlantic forcing of Amazonian precipitation during the last ice age. Nat Geosci. 2012;5(11): 817.

103. Gosling WD, Bush MB, Hanselman JA, Chepstow-Lusty A. Glacial-interglacial changes in moisture balance and the impact on vegetation in the southern hemisphere tropical Andes (Bolivia/ Peru). Palaeogeogr Palaeoclimatol Palaeoecol. 2008;259: 35–50.

104. Quipildor VB, Kitzberger T, Ortega-Baes P, Quiroga MP, Premoli AC. Regional climate oscillations and local topography shape genetic polymorphisms and distribution of the giant columnar cactus Echinopsis terscheckii in drylands of the tropical Andes. J Biogeogr. 2017;45: 116–126.

105. Zhang S, Li T, Chang F, Yu Z, Xiong Z, Wang H. Correspondence between the ENSO-like state and glacial-interglacial condition during the past 360 kyr. Chin. J. Oceanol. Limnol. 2016;35(5): 1018–1031.

106. Fritz SC, Baker PA, Tapia P, Spanbauer T, Westover K. Evolution of the Lake Titicaca basin and its diatom flora over the last ~370,000 years. Palaeogeogr Palaeoclimatol Palaeoecol. 2012;317–318: 93–103.

107. Hughes PD, Gibbard PL. Global glacier dynamics during 100 ka Pleistocene glacial cycles. Quat Res. 2018;90(1): 222–243.

108. Friedrich T, Timmermann A, Tigchelaar M, Timm OE, Ganopolski A. Nonlinear climate sensitivity and its implications for future greenhouse warming. Sci Adv. 2016;2(11): e1501923. doi: 10.1126/sciadv.1501923 28861462

109. Petit JR, Jouzel J, Raynaud D, Barkov NI, Barnola JM, Basile I, et al. Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica. Nature. 1999;399: 429–436.

110. Rincón-Martínez D, Lamy F, Contreras S, Leduc G, Bard E, Saukel C, et al. More humid interglacials in Ecuador during the past 500 kyr linked to latitudinal shifts of the equatorial front and the Intertropical Convergence Zone in the eastern tropical Pacific. Paleoceanography. 2010;25: PA2210.


Článek vyšel v časopise

PLOS One


2019 Číslo 11