Genetic and phenotypic divergence between low- and high-altitude populations of two recently diverged cinnamon teal subspecies

Evolution

Volumn 67, Issue 1, 2013, Pages 170-184

  Wilson, Robert E ^a,b   Peters, Jeffrey L ^b   McCracken, Kevin G ^a  

^a UNIVERSITY OF ALASKA MUSEUM   (United States)

^b WRIGHT STATE UNIVERSITY   (United States)

Author keywords

Andes; Gene flow; Hemoglobin; Hypoxia; Morphology; Waterfowl

Indexed keywords

HEMOGLOBIN; MITOCHONDRIAL DNA; OXYGEN;

ALTITUDE; AMINO ACID; ASYMMETRY; BODY SIZE; COLONIZATION; DIVERGENCE; GENE FLOW; GENETIC MARKER; HYPOXIA; MITOCHONDRIAL DNA; MORPHOLOGY; NATURAL SELECTION; PHENOTYPIC PLASTICITY; POLYMORPHISM; SPATIAL VARIATION; SUBSPECIES; WATERFOWL;

AIR; ALTITUDE; ANIMAL; ARTICLE; BODY SIZE; COLD; DUCK; ECOSYSTEM; GENETIC VARIABILITY; GENETICS; GENOTYPE; INTRON; MOLECULAR EVOLUTION; PHENOTYPE; POPULATION; SOUTH AMERICA; SPECIES DIFFERENTIATION;

AIR; ALTITUDE; ANIMALS; BODY SIZE; COLD TEMPERATURE; DNA, MITOCHONDRIAL; DUCKS; ECOSYSTEM; EVOLUTION, MOLECULAR; GENETIC SPECIATION; GENETIC VARIATION; GENOTYPE; HEMOGLOBINS; INTRONS; OXYGEN; PHENOTYPE; POPULATION; SOUTH AMERICA;

ANDES;

ANAS CYANOPTERA; ANATIDAE; CINNAMOMUM VERUM;

EID: 84871988925     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2012.01740.x     Document Type: Article

References (99)

1. Bandelt, H. J., P. Forster, B. C. Sykes, and M. B. Richards. 1995. Mitochondrial portraits of human populations. Genetics 141:743-753.
2. Bears, H., M. C. Drever, and K. Martin. 2008. Comparative morphology of dark-eyed juncos Junco hyemalis breeding at two elevations: a common aviary experiment. J. Avian Biol. 39:152-162.
3. st tell us? Trends Ecol. Evol. 20:435-440.
4. Bergmann, C. 1847. Ueber die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Gott. Studien 3:595-708.
5. Blake, E. R. 1977. Manual of Neotropical birds. Vol. 1. Univ. Chicago Press, Chicago, IL.
6. Bottema, C. D. K., G. Sarkar, J. D. Cassady, S. Ii, C. M. Dutton, and S. S. Sommer. 1993. Polymerase chain-reaction amplification of specific alleles: a general method of detection of mutations, polymorphisms, and haplotypes. Methods Enzymol. 218:388-402.
7. Braunitzer, G., and I. Hiebl. 1988. Molekulare Aspekte der Höohenatmung von Vögeln. Hämoglobine der Streifengans (Anser indicus), der Andengans (Chloephaga melanoptera) und des Sperbergeiers (Gyps rueppellii). Naturwissenschaften 75:280-287.
8. Bulgarella, M., R. E. Wilson, C. Kopuchian, T. H. Valqui, and K. G. McCracken. 2007. Elevational variation in body size of crested ducks (Lophonetta specularioides) from the central high Andes, Mendoza, and Patagonia. Ornit. Neotrop. 18:587-602.
9. Bulgarella, M., J. L. Peters, C. Kopuchian, T. Valqui, R. E. Wilson, and K. G. McCracken. 2012. Multilocus coalescent analysis of haemoglobin differentiation between low- and high-altitude populations of crested ducks (Lophonetta specularioides). Mol. Ecol. 21:350-368.
10. Cadena, C. D., K. H. Kozak, J. P. Gómez, J. L. Parra, C. M. McCain, R. C. K. Bowie, A. C. Carnaval, C. Moritz, C. Rahbek, T. E. Roberts et al. 2012. Latitude, elevational climatic zonation and speciation in New World vertebrates. Proc. R. Soc., Lond. B Biol. Sci. 279:194-201.
11. Carey, C. 1994. Structural and physiological differences between montane and lowland avian eggs and embryos. J. Biosci. 19:429-440.
12. Cheviron, Z. A. and R. T. Brumfield. 2009. Migration-selection balance and local adaptation of mitochondrial haplotypes in rufous-collared sparrows (Zonatrichia capensis) along an elevational gradient. Evolution 63:1593-1605.
13. Delacour, J. 1956. The waterfowl of the world. Country Life Limited, London, UK.
14. Diamond, J. M. 1986. Evolution of ecological segregation in the New Guinea montane avifauna. Pp. 98-125 in J. M. Diamond and T. J. Case, eds. Community ecology. Harper and Row, New York.
15. Emelianov, I., F. Marec, and J. Mallet. 2004. Genomic evidence for divergence with gene flow in host races of the larch budmoth. Proc. R. Soc. Lond. B 271:97-105.
16. Endler, J. A. 1986. Natural selection in the wild. Princeton Univ. Press, Princeton, NJ.
17. Excoffier, L., G. Laval, and S. Schneider. 2005. Arlequin ver. 3.0: an integrated software package for G population genetics data analysis. Evol. Bioinform. Online 1:47-50.
18. Fjeldså, J. 1985. Origin, evolution, and status of the avifauna of Andean wetlands. Ornithol. Monogr. 36:85-112.
19. Fu, Y. X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selections. Genetics 147:915-925.
20. Garant D., S. E. Forde, and A. P. Hendry. 2007. The multifarious effects of dispersal and gene flow on contemporary adaptation. Funct. Ecol. 21:434-443.
21. Hendry, A. P., P. Nosil, and L. Riesenberg. 2007. The speed of ecological speciation. Funct. Ecol. 21:455-464.
22. Hey, J. 2005. On the number of New World founders: a population genetic portrait of the peopling of the Americas. PLoS Biol. 3:e193.
23. Hey, J., and R. Nielsen. 2004. Multilocus methods of estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747-760.
24. Hiebl, I., G. Braunitzer, and D. Schneeganss. 1987. The primary structures of the major and minor hemoglobin components of adult Andean Goose (Chloephaga melanoptera, Anatidae): the mutation Leu → Ser in position 55 of the β-chains. Biol. Chem. Hoppe-Seyler 368:1559-1569.
25. Hillier, L. W., W. Miller, E. Birney, W. Warren, R. C. Hardison, C. P. Ponting, P. Bork, D. W. Burt, M. A. M. Groenen, M. E. Delany et al. 2004. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:695-716.
26. Hopkins, S. R., and F. L. Powell. 2001. Common themes of adaptation to hypoxia. Insights from comparative physiology. Adv. Exp. Med. Biol. 502:153-167.
27. Hudson, R. R. 2002. Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18:337-338.
28. James, F. C. 1970. Geographic size variation in birds and its relationship to climate. Ecology 51:365-390.
29. Jessen T. H, R. E. Weber, G. Fermi, J. Tame, and G. Braunitzer. 1991. Adaptation of bird hemoglobins to high-altitudes-demonstration of molecular mechanism by protein engineering. Proc. Natl. Acad. Sci. USA 88:6519-6522.
30. Johnson, K. P., and M. D. Sorenson. 1999. Phylogeny and bio-geography of dabbling ducks (Genus: Anas): a comparison of molecular and morphological evidence. Auk 116:792-805.
31. Johnson, P. A., F. C. Hoppensteadt, J. J. Smith, and G. L. Bush. 1996. Conditions for sympatric speciation: a diploid model incorporating habitat fidelity and non-habitat assortative mating. Evol. Ecol. 10:187-205.
32. Kuhner, M. K. 2006. LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22:768-770.
33. Larsson, K. 1993. Inheritance of body size in the barnacle goose under different environmental conditions. J. Evol. Biol. 6:195-208.
34. León-Velarde, F., and C. Monge-C. 2004. Avian embryos in hypoxic environment. Respir. Physiol. Neurobiol. 141:331-343.
35. León-Velarde, F., D. Espinoza, C. Monge, C. de Muizon. 1991. A genetic response to high-altitude hypoxia: high hemoglobin-oxygen affinity in chicken (Galllus gallus) from the Peruvian Andes. Compres Rendu de l'Acadamie des Sciences 313:401-406.
36. León-Velarde, F., C. de Muizon, J. A. Palacios, D. Clark, and C. Monge. 1996. Hemoglobin affinity and structure in high-altitude and sea-level carnivores in Peru. Comp. Biochem. Physiol. A Physiol. 113:407-411.
37. Lewontin, R. C., and J. Krakauer. 1973. Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics 74:175-195.
38. Maddison, W. P. 1997. Gene trees in species trees. Syst. Biol. 46:523-536.
39. Mayr, E. 1963. Animal species and evolution. Belknap Press of Harvard Univ. Press, Cambridge, MA.
40. McCracken, K. G., M. Bulgarella, K. P. Johnson, M. K. Kuhner, J. Trucco, T. H. Valqui, R. E. Wilson, and J. L. Peters. 2009a. Gene flow in the face of countervailing selection: adaptation to high-altitude hypoxia in the βA hemoglobin subunit of yellow-billed pintails. Mol. Biol. Evol. 26:815-827.
41. McCracken, K. G., C. P. Barger, M. Bulgarella, K. P. Johnson, M. K. Kuhner, A. V. Moore, J. L. Peters, J. Trucco, T. H. Valqui, K. Winker et al. 2009b. Signatures of high-altitude adaptation in the major hemoglobin of five species of Andean dabbling ducks. Am. Nat. 174:631-650.
42. McCracken, K. G., C. P. Barger, M. Bulgarella, K. P. Johnson, S. A. Sonsthagen, J. Trucco, T. H. Valqui, R E. Wilson, K. Winker, and M. D. Sorenson. 2009c. Parallel evolution in the major hemoglobin genes of eight species of Andean waterfowl. Mol. Ecol. 18:3992-4005.
43. McKay, J. K., and R. G. Latta. 2002. Adaptive population divergence: markers, QTL and traits. Trends Ecol. Evol. 17:285-291.
44. Merilä, J. 1997. Quantitative trait and allozyme divergence in the greenfinch (Carduelis chloris, Aves: Fringillidae). Biol. J. Linn. Soc. 61:243-266.
45. Merilä, J., and P. Crnokrak. 2001. Comparison of genetic differentiation at marker loci and quantitative traits. J. Evol. Biol. 14:892-903.
46. Merilä, J., and L. Gustafsson. 1993. Inheritance of size and shape in a natural population of collared flycatchers, Ficedulla albicollis. J. Evol. Biol. 6:375-395.
47. Milá, B., R. K. Wayne, P. Fitze, and T. B. Smith. 2009. Divergence with gene flow and fine-scale phylogenetical structure in the wedge-billed woodcreeper, Glyphorynchus spirurus, a Neotropical rainforest bird. Mol. Ecol. 18:2979-2995.
48. Monge, C., and F. León-Velarde. 1991. Physiological adaptation to high altitude: oxygen transport in mammals and birds. Physiol. Rev. 71:1135-1172.
49. Nosil, P., S. P. Egan, and D. J. Funk. 2008. Heterogeneous genomic differentiation between walking-stick ecotypes: "isolation by adaptation" and multiple roles for divergent selection. Evolution 62:316-336.
50. Peng, Y., Z. Yang, H. Zhang, C. Cui, X. Qi, X. Luo, X. Tao, T. Wu, Ouzhuluobu, Basang et al. 2011. Genetic variations in Tibetan populations and high-altitude adaptation at the Himalayas. Mol. Biol. Evol. 28:1075-1081.
51. Perutz, M. F. 1990. Mechanisms regulating the reactions of human hemoglobin with oxygen and carbon-monoxide. Ann. Rev. Physiol. 52:1-25.
52. Peters, J. L., W. Gretes, and K. E. Omland. 2005. Late Pleistocene divergence between eastern and western populations of wood ducks (Aix sponsa) inferred by the 'isolation with migration' coalescent method. Mol. Ecol. 14:3407-3418.
53. Peters, J. L., Y. Zhuravlev, I. Fefelov, A. Logie, and K. E. Omland. 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.
54. Peters, J. L., Y. N. Zhuravlev, I. Fefelov, E. M. Humphries, and K. E. Omland. 2008. Multilocus phylogeography of a Holarctic duck: colonization of North America from Eurasia by gadwall (Anas strepera). Evolution 62:1469-1483.
55. Peters, J. L., T. E. Roberts, K. Winker, and K. G. McCracken. 2012. Heterogeneity in genetic diversity among non-coding loci fails to fit neutral coalescent models of population history. PLoS One 7:e31972.
56. Posada, D., and K. A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818.
57. Pritchard, J. K., M. Stephens, and P. Donnelly. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
58. Rambaut, A. 2007. Se-Al 2.0a11. Univ. of Oxford, Oxford, UK.
59. Rasner C. A., P. Yeh, L. S. Eggert, K. E. Hunt, D. S. Woodruff, and T. D. Price. 2004. Genetic and morphological evolution following a founder event in the dark-eyed junco, Junco hyemalis thurberi. Mol. Ecol. 13:671-681.
60. Ribeiro, Â. M., P. Lloyd, and R. C. K. Bowie. 2011. A tight balance between natural selection and gene flow in a southern African arid-zone endemic bird. Evolution 65:3499-3514.
61. Richmond, A. D., and T. Price. 1992. Evolution of ecological differences in the Old World leaf warblers. Nature 355:817-821.
62. Ridgely, R. S., T. F. Allnutt, T. Brooks, D. K. McNicol, D. W. Mehlman, B. E. Young, and J. R. Zook. 2003. Digital distribution maps of the birds of the Western Hemisphere, version 1.0. NatureServe, Arlington, VA.
63. Rising, J. D., and K. M. Somers. 1989. The measurements of overall body size in birds. Auk 106:666-674.
64. Rogers, A. R., and H. Harpending. 1992. Population growth makes waves in the distribution of pairwise genetic differences. Mol. Biol. Evol. 9:552-569.
65. Rose, P. M., and D. A. Scott. 1997. Waterfowl population estimates, 2nd ed. Wetlands International, Wageningen, Netherlands.
66. Rozas, J., J. C. Sanchez-DelBarrio, X. Messeguer, and R. Rozas. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496-2497.
67. Rundle, H. D., and P. Nosil. 2005. Ecological speciation. Ecol. Lett. 8:336-352.
68. Schluter, D. 2001. Ecology and the origin of species. Trends Ecol. Evol. 16:372-380.
69. Schmidt-Nielsen, K., and J. L. Larimer. 1958. Oxygen dissociation curves of mammalian blood in relation to body size. Am. J. Physiol. 195:424-428.
70. Scott, G. R., S. Egginton, J. G. Richards, and W. K. Milsom. 2009. Evolution of muscle phenotype for extreme high altitude flight in the bar-headed goose. Proc. R. Soc. Lond. B 276:3645-3653.
71. Scott, G. R., P. M. Schulte, S. Egginton, A. L. M. Scott, J. G. Richards, and W. K. Milsom. 2011. Molecular evolution of cytochrome c oxidase underlies high-altitude adaptation in the bar-headed goose. Mol. Biol. Evol. 28:351-363.
72. Sæther, S. A., P. Fiske, J. A. Kålås, A. Kuresoo, L. Luigujõe, S. B. Piertney, T. Sahlman, and J. Höglund. 2007. Inferring local adaptation from QST-FST comparisons: neutral genetic and quantitative trait variation in European populations of great snipe. J. Evol. Biol. 20:1563-1576.
73. Servedio, M. R., and M. A. F. Noor. 2003. The role of reinforcement in speciation: theory and data. Annu. Rev. Ecol. Evol. Syst. 34:339-364.
74. Slatkin, M. 1987. Gene flow and the geographic structure of natural populations. Science 236:787-792.
75. Snyder, L. L., and H. G. Lumsden. 1951. Variation in Anas cyanoptera. Occas. Pap. R. Ont. Mus. of Zool. 10:1-18.
76. Sorenson, M. D., and R. C. Fleischer. 1996. Multiple independent transpositions of mitochondrial DNA control region sequences to the nucleus. Proc. Natl. Acad. Sci. USA 93:15239-15243.
77. Sorenson, M. D., J. C. Ast, D. E. Dimcheff, T. Yuri, and D. P. Mindell. 1999. Primers for a PCR-based approach to mitochondrial genome sequencing in birds and other vertebrates. Mol. Phylogenet. Evol. 12:105-114.
78. Stephens, M., N. Smith, and P. Donnelly. 2001. A new statistical method for haplotype reconstruction from population data. Am. J. Hum. Genet. 68:978-989.
79. Storz, J. F. 2002. Contrasting patterns of divergence in quantitative traits and neutral DNA markers: analysis of clinal variation. Mol. Ecol. 11:2537-2551.
80. Storz, J. F. 2010. Genes for high altitudes. Science 329:40-41.
81. Storz, J., A. M. Runck, H. Moriyama, R. E. Weber, and A. Fago. 2010. Genetic differences in hemoglobin function between highland and lowland deer mice. J. Exp. Biol. 213:2165-2574.
82. Tajima, F. 1989. The effect of change in population size on DNA polymorphism. Genetics 123:597-601.
83. Tucker, V. A. 1968. Respiratory physiology of house sparrows in relation to high-altitude flight. J. Exp. Biol. 48:55-66.
84. Via, S. 2009. Natural selection in action during speciation. Proc. Natl. Acad. Sci. USA 106:9939-9946.
85. Visschedijk, A. H. J., A. Ar, H. Rahn, and J. Piiper. 1980. The independent effects of atmospheric pressure and oxygen partial pressure on gas exchange of the chicken embryo. Respir. Physiol. Neurobiol. 39:33-44.
86. Vuilleumier, F. 1986. Origins of the tropical avifaunas of the high Andes. Pp. 586-622 in F. Vuilleumier and M. Monasterio, eds. High altitude tropical biogeography. Oxford Univ. Press and American Museum of Natural History, New York.
87. Weber, R. E. 2007. High-altitude adaptations in vertebrate hemoglobins. Respir. Physiol. Neurobiol. 158:132-142.
88. 55-Ser): functions related to high-altitude respiration in geese. J. Appl. Physiol. 75:2646-2655.
89. Weber, R. E., H. Ostojic, A. Fago, S. Dewilde, M. V. Hauwaert, L. Moens, and C. Monge. 2002. Novel mechanism for high-altitude adaptation in hemoglobin of the Andean frog Telmatobius peruvianus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283:1052-1060.
90. West-Eberhard, M. J. 1983. Sexual selection, social competition, and speciation. Quart. Rev. Biol. 58:155-183.
91. Wetlands International. 2002. Waterbird population estimates, 3rd ed. Wetlands International Global series No. 12. Wageningen, Netherlands.
92. Whitlock, M. C. 1999. Neutral additive genetic variance in a metapopulation. Genet. Res. 74:215-221.
93. ST. Mol. Ecol. 17:1885-1896.
94. Wilson, G. A., and B. Rannala. 2003. Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177-1191.
95. Wilson, R. E., T. H. Valqui, and K. G. McCracken. 2010. Ecogeographic variation in cinnamon teal (Anas cyanoptera) along elevational and latitudinal gradients. Ornithol. Monogr. 67:141-161.
96. Wright, S. 1931. Evolution in Mendelian populations. Genetics 16:97-159.
97. Wright, S. 1951. The genetical structure of populations. Ann. Eugen. 15:323-354.
98. Wu, C. I. 2001. The genic view of the process of speciation. J. Evol. Biol. 14:851-865.
99. Yi, X., Y. Liang, E. Huerta-Sanchez, X. Jin, Z. X. P. Cuo, J. E. Pool, X. Xu, H. Jiang, N. Vinckenbosch, T. S. Korneliussen et al. 2010. Sequencing of 50 human exomes reveals adaptation to high altitude. Science 329:75-78.