The importance of recent ice ages in speciation: A failed paradigm

Science

Volumn 277, Issue 5332, 1997, Pages 1666-1669

  Klicka, John ^a   Zink, Robert M ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

EVOLUTION; GLACIATION; PLEISTOCENE; PLEISTOCENE (LATE); SPECIATION; VERTEBRATE;

ARTICLE; BIODIVERSITY; BIRD; MITOCHONDRION; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; SPECIES; VERTEBRATE;

EID: 0030773836     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.277.5332.1666     Document Type: Article

References (55)

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5. W. J. Beecher, Ecology 36, 23 (1955); L. S. Dillon, Science 123, 167 (1956); R. K. Selander and D. R. Giller, Condor 63, 29 (1961); R. Brewer, Auk 80, 9 (1963); R. K. Selander, in The Quaternary of the United States, H. E. Wright Jr. and D. G. Frey, Eds. (Princeton Univ. Press, Princeton, NJ, 1965), pp. 527-542; R. M. Mengel, Univ. Kans. Dep. Geol. Spec. Publ. 3, 279 (1970); J. P. Hubbard, Living Bird 12, 155 (1973).
6. W. J. Beecher, Ecology 36, 23 (1955); L. S. Dillon, Science 123, 167 (1956); R. K. Selander and D. R. Giller, Condor 63, 29 (1961); R. Brewer, Auk 80, 9 (1963); R. K. Selander, in The Quaternary of the United States, H. E. Wright Jr. and D. G. Frey, Eds. (Princeton Univ. Press, Princeton, NJ, 1965), pp. 527-542; R. M. Mengel, Univ. Kans. Dep. Geol. Spec. Publ. 3, 279 (1970); J. P. Hubbard, Living Bird 12, 155 (1973).
7. W. J. Beecher, Ecology 36, 23 (1955); L. S. Dillon, Science 123, 167 (1956); R. K. Selander and D. R. Giller, Condor 63, 29 (1961); R. Brewer, Auk 80, 9 (1963); R. K. Selander, in The Quaternary of the United States, H. E. Wright Jr. and D. G. Frey, Eds. (Princeton Univ. Press, Princeton, NJ, 1965), pp. 527-542; R. M. Mengel, Univ. Kans. Dep. Geol. Spec. Publ. 3, 279 (1970); J. P. Hubbard, Living Bird 12, 155 (1973).
8. W. J. Beecher, Ecology 36, 23 (1955); L. S. Dillon, Science 123, 167 (1956); R. K. Selander and D. R. Giller, Condor 63, 29 (1961); R. Brewer, Auk 80, 9 (1963); R. K. Selander, in The Quaternary of the United States, H. E. Wright Jr. and D. G. Frey, Eds. (Princeton Univ. Press, Princeton, NJ, 1965), pp. 527-542; R. M. Mengel, Univ. Kans. Dep. Geol. Spec. Publ. 3, 279 (1970); J. P. Hubbard, Living Bird 12, 155 (1973).
9. W. J. Beecher, Ecology 36, 23 (1955); L. S. Dillon, Science 123, 167 (1956); R. K. Selander and D. R. Giller, Condor 63, 29 (1961); R. Brewer, Auk 80, 9 (1963); R. K. Selander, in The Quaternary of the United States, H. E. Wright Jr. and D. G. Frey, Eds. (Princeton Univ. Press, Princeton, NJ, 1965), pp. 527-542; R. M. Mengel, Univ. Kans. Dep. Geol. Spec. Publ. 3, 279 (1970); J. P. Hubbard, Living Bird 12, 155 (1973).
10. W. J. Beecher, Ecology 36, 23 (1955); L. S. Dillon, Science 123, 167 (1956); R. K. Selander and D. R. Giller, Condor 63, 29 (1961); R. Brewer, Auk 80, 9 (1963); R. K. Selander, in The Quaternary of the United States, H. E. Wright Jr. and D. G. Frey, Eds. (Princeton Univ. Press, Princeton, NJ, 1965), pp. 527-542; R. M. Mengel, Univ. Kans. Dep. Geol. Spec. Publ. 3, 279 (1970); J. P. Hubbard, Living Bird 12, 155 (1973).
11. R. M. Mengel, Living Bird 3, 9 (1964).
12. A. L. Rand, Evolution 2, 314 (1948).
13. R. K. Selander, in Avian Biology, D. S. Farner and J. R. King, Eds. (Academic Press, New York, 1971), vol. 1, pp. 57-147.
14. G. M. Hewitt, Biol. J. Linn. Soc. London 58, 247 (1996).
15. F. B. Gill, Ornithology (Freeman, New York, ed. 2, 1995).
16. Our conclusions rely on a molecular "clock" that is presumed to "tick" at a constant rate. The topic of molecular clocks is contentious [J. C. Avise, Molecular Markers, Natural History and Evolution (Chapman & Hall, New York, 1994)]. Caveats include (i) nucleotide substitution rate heterogeneity, presumably caused by variation in metabolic rate, body size, and generation time [A. P. Martin and S. R. Palumbi, Proc. Natl. Acad. Sci. U.S.A. 90, 4087 (1993)]; (ii) population history (frequency of bottlenecks, for example); and (iii) among-taxon variation in constraints on mutation and fixation [D. P. Mindell and C. E. Thacker, Annu. Rev. Ecol. Syst. 27, 279 (1996)]. Within-genome rate heterogeneity ("hypervariable" noncoding regions, for example) may also influence rate calculations. To mitigate these sources of bias, we confined comparisons to a single group of birds, the oscine passerines. We compare taxa only when the overall mtDNA genome was sampled with restriction fragments [restriction fragment length polymorphisms (RFLPs)] or sequence data were available for coding genes. Differences between closely related species are primarily third base position transitions, and such changes probably evolve in a clocklike manner.
17. Our conclusions rely on a molecular "clock" that is presumed to "tick" at a constant rate. The topic of molecular clocks is contentious [J. C. Avise, Molecular Markers, Natural History and Evolution (Chapman & Hall, New York, 1994)]. Caveats include (i) nucleotide substitution rate heterogeneity, presumably caused by variation in metabolic rate, body size, and generation time [A. P. Martin and S. R. Palumbi, Proc. Natl. Acad. Sci. U.S.A. 90, 4087 (1993)]; (ii) population history (frequency of bottlenecks, for example); and (iii) among-taxon variation in constraints on mutation and fixation [D. P. Mindell and C. E. Thacker, Annu. Rev. Ecol. Syst. 27, 279 (1996)]. Within-genome rate heterogeneity ("hypervariable" noncoding regions, for example) may also influence rate calculations. To mitigate these sources of bias, we confined comparisons to a single group of birds, the oscine passerines. We compare taxa only when the overall mtDNA genome was sampled with restriction fragments [restriction fragment length polymorphisms (RFLPs)] or sequence data were available for coding genes. Differences between closely related species are primarily third base position transitions, and such changes probably evolve in a clocklike manner.
18. Our conclusions rely on a molecular "clock" that is presumed to "tick" at a constant rate. The topic of molecular clocks is contentious [J. C. Avise, Molecular Markers, Natural History and Evolution (Chapman & Hall, New York, 1994)]. Caveats include (i) nucleotide substitution rate heterogeneity, presumably caused by variation in metabolic rate, body size, and generation time [A. P. Martin and S. R. Palumbi, Proc. Natl. Acad. Sci. U.S.A. 90, 4087 (1993)]; (ii) population history (frequency of bottlenecks, for example); and (iii) among-taxon variation in constraints on mutation and fixation [D. P. Mindell and C. E. Thacker, Annu. Rev. Ecol. Syst. 27, 279 (1996)]. Within-genome rate heterogeneity ("hypervariable" noncoding regions, for example) may also influence rate calculations. To mitigate these sources of bias, we confined comparisons to a single group of birds, the oscine passerines. We compare taxa only when the overall mtDNA genome was sampled with restriction fragments [restriction fragment length polymorphisms (RFLPs)] or sequence data were available for coding genes. Differences between closely related species are primarily third base position transitions, and such changes probably evolve in a clocklike manner.
19. Independent clock calibrations for a diverse array of avian taxonomic orders support a mtDNA substitution rate of 2%/My. These include: geese {Anseriformes [G. F. Shields and A. C. Wilson, J. Mol. Evol. 24, 212 (1987)], 2.0%/My}; Old-world partridges and fowl {Galliformes [E. Randi, Mol. Phylogenet. Evol. 6, 214 (1996)], 2.0%/My}; cranes {Gruiformes [C. Krajewski and D. G. King, Mol. Biol. Evol. 13, 21 (1996)], 0.7 to 1.7%/My}; albatrosses {Procellariiformes [G. B. Nunn, J. Cooper, P. Jouventin, C. J. R. Robertson, G. G. Robertson, Auk 113, 784 (1996)], 0.65%/My}; Hawaiian honeycreepers {Passeriformes [C. L. Tarr and R. C. Fleischer, ibid. 110, 825 (1993)], 2.0%/My}, and New-world quail [Galliformes (R. M. Zink, unpublished data), 2.0%/My].
20. Independent clock calibrations for a diverse array of avian taxonomic orders support a mtDNA substitution rate of 2%/My. These include: geese {Anseriformes [G. F. Shields and A. C. Wilson, J. Mol. Evol. 24, 212 (1987)], 2.0%/My}; Old-world partridges and fowl {Galliformes [E. Randi, Mol. Phylogenet. Evol. 6, 214 (1996)], 2.0%/My}; cranes {Gruiformes [C. Krajewski and D. G. King, Mol. Biol. Evol. 13, 21 (1996)], 0.7 to 1.7%/My}; albatrosses {Procellariiformes [G. B. Nunn, J. Cooper, P. Jouventin, C. J. R. Robertson, G. G. Robertson, Auk 113, 784 (1996)], 0.65%/My}; Hawaiian honeycreepers {Passeriformes [C. L. Tarr and R. C. Fleischer, ibid. 110, 825 (1993)], 2.0%/My}, and New-world quail [Galliformes (R. M. Zink, unpublished data), 2.0%/My].
21. Independent clock calibrations for a diverse array of avian taxonomic orders support a mtDNA substitution rate of 2%/My. These include: geese {Anseriformes [G. F. Shields and A. C. Wilson, J. Mol. Evol. 24, 212 (1987)], 2.0%/My}; Old-world partridges and fowl {Galliformes [E. Randi, Mol. Phylogenet. Evol. 6, 214 (1996)], 2.0%/My}; cranes {Gruiformes [C. Krajewski and D. G. King, Mol. Biol. Evol. 13, 21 (1996)], 0.7 to 1.7%/My}; albatrosses {Procellariiformes [G. B. Nunn, J. Cooper, P. Jouventin, C. J. R. Robertson, G. G. Robertson, Auk 113, 784 (1996)], 0.65%/My}; Hawaiian honeycreepers {Passeriformes [C. L. Tarr and R. C. Fleischer, ibid. 110, 825 (1993)], 2.0%/My}, and New-world quail [Galliformes (R. M. Zink, unpublished data), 2.0%/My].
22. Independent clock calibrations for a diverse array of avian taxonomic orders support a mtDNA substitution rate of 2%/My. These include: geese {Anseriformes [G. F. Shields and A. C. Wilson, J. Mol. Evol. 24, 212 (1987)], 2.0%/My}; Old-world partridges and fowl {Galliformes [E. Randi, Mol. Phylogenet. Evol. 6, 214 (1996)], 2.0%/My}; cranes {Gruiformes [C. Krajewski and D. G. King, Mol. Biol. Evol. 13, 21 (1996)], 0.7 to 1.7%/My}; albatrosses {Procellariiformes [G. B. Nunn, J. Cooper, P. Jouventin, C. J. R. Robertson, G. G. Robertson, Auk 113, 784 (1996)], 0.65%/My}; Hawaiian honeycreepers {Passeriformes [C. L. Tarr and R. C. Fleischer, ibid. 110, 825 (1993)], 2.0%/My}, and New-world quail [Galliformes (R. M. Zink, unpublished data), 2.0%/My].
23. Independent clock calibrations for a diverse array of avian taxonomic orders support a mtDNA substitution rate of 2%/My. These include: geese {Anseriformes [G. F. Shields and A. C. Wilson, J. Mol. Evol. 24, 212 (1987)], 2.0%/My}; Old-world partridges and fowl {Galliformes [E. Randi, Mol. Phylogenet. Evol. 6, 214 (1996)], 2.0%/My}; cranes {Gruiformes [C. Krajewski and D. G. King, Mol. Biol. Evol. 13, 21 (1996)], 0.7 to 1.7%/My}; albatrosses {Procellariiformes [G. B. Nunn, J. Cooper, P. Jouventin, C. J. R. Robertson, G. G. Robertson, Auk 113, 784 (1996)], 0.65%/My}; Hawaiian honeycreepers {Passeriformes [C. L. Tarr and R. C. Fleischer, ibid. 110, 825 (1993)], 2.0%/My}, and New-world quail [Galliformes (R. M. Zink, unpublished data), 2.0%/My].
24. This phenomenon is termed lineage sorting. Alternatively, haplotype trees from species isolated for a sufficient period do reflect species (taxonomic) limits (termed reciprocal monophyly).
25. Species studied traditionally have been considered sisters, although recent work has shown that some are not sisters but rather are members of species complexes. All pairs and complexes are thought to have Late Pleistocene origins (5). Three subspecies pairs are included because they qualify as phylogenetic species; their inclusion makes the tests more conservative. Nomenclature follows the most recent AOU Check-list [American Ornithologists' Union, Check-list of North American Birds (Allen Press, Lawrence, KS, ed. 6, 1983)] and subsequent supplements.
26. We compared both mtDNA coding gene sequences and RFLPs, which provide comparable estimates of songbird sequence divergence (75). A subset (n = 12; those shown in Fig. 1 with standard errors) of sequence data having an uncorrected average percent divergence of 6.3 (±0.76) has a Kimura two-parameter [S. Kumar, K. Tamura, M. Nei, MEGA: Molecular Evolutionary Genetic Analysis (Pennsylvania State Univ., University Park, PA, 1993), version 1.01] corrected distance of 6.7 (±0.86). The similarity of these values indicates little saturation.
27. R. M. Zink and R. C. Blackwell, Auk 113, 59 (1996).
28. F. B. Gill, A. M. Mostrom, A. L. Mack, Evolution 47, 195 (1993).
29. E. Bermingham, S. Rohwer, S. Freeman, C. Wood, Proc. Natl. Acad. Sci. U.S.A. 89, 6624 (1992).
30. In the following, letters a through m correspond with the molecular study references shown in Table 1: a [J. C. Avise and R. M. Zink, Auk 105, 516 (1988)]; b (76); c (79); d (R. M. Zink and R. C. Blackwell, Mol. Phylogenet. Evol., in press); e [N. K. Johnson and C. Cicero, in Acta XX Congressus International Ornithologici (New Zealand Ornithological Congress Trust Board, Wellington, New Zealand, 1990), pp. 601-610]; f [R. M. Ball Jr. and J. C. Avise, Auk 109, 626 (1992)]; g (17); h [F. B. Gill and B. Slikas, Condor 94, 20 (1992)]; i [J. D. Rising and J. C. Avise, Auk 110, 844 (1993)]; j [J. C. Avise and W. S. Nelson, Science 243, 646 (1989)];
31. In the following, letters a through m correspond with the molecular study references shown in Table 1: a [J. C. Avise and R. M. Zink, Auk 105, 516 (1988)]; b (76); c (79); d (R. M. Zink and R. C. Blackwell, Mol. Phylogenet. Evol., in press); e [N. K. Johnson and C. Cicero, in Acta XX Congressus International Ornithologici (New Zealand Ornithological Congress Trust Board, Wellington, New Zealand, 1990), pp. 601-610]; f [R. M. Ball Jr. and J. C. Avise, Auk 109, 626 (1992)]; g (17); h [F. B. Gill and B. Slikas, Condor 94, 20 (1992)]; i [J. D. Rising and J. C. Avise, Auk 110, 844 (1993)]; j [J. C. Avise and W. S. Nelson, Science 243, 646 (1989)];
32. In the following, letters a through m correspond with the molecular study references shown in Table 1: a [J. C. Avise and R. M. Zink, Auk 105, 516 (1988)]; b (76); c (79); d (R. M. Zink and R. C. Blackwell, Mol. Phylogenet. Evol., in press); e [N. K. Johnson and C. Cicero, in Acta XX Congressus International Ornithologici (New Zealand Ornithological Congress Trust Board, Wellington, New Zealand, 1990), pp. 601-610]; f [R. M. Ball Jr. and J. C. Avise, Auk 109, 626 (1992)]; g (17); h [F. B. Gill and B. Slikas, Condor 94, 20 (1992)]; i [J. D. Rising and J. C. Avise, Auk 110, 844 (1993)]; j [J. C. Avise and W. S. Nelson, Science 243, 646 (1989)];
33. In the following, letters a through m correspond with the molecular study references shown in Table 1: a [J. C. Avise and R. M. Zink, Auk 105, 516 (1988)]; b (76); c (79); d (R. M. Zink and R. C. Blackwell, Mol. Phylogenet. Evol., in press); e [N. K. Johnson and C. Cicero, in Acta XX Congressus International Ornithologici (New Zealand Ornithological Congress Trust Board, Wellington, New Zealand, 1990), pp. 601-610]; f [R. M. Ball Jr. and J. C. Avise, Auk 109, 626 (1992)]; g (17); h [F. B. Gill and B. Slikas, Condor 94, 20 (1992)]; i [J. D. Rising and J. C. Avise, Auk 110, 844 (1993)]; j [J. C. Avise and W. S. Nelson, Science 243, 646 (1989)];
34. In the following, letters a through m correspond with the molecular study references shown in Table 1: a [J. C. Avise and R. M. Zink, Auk 105, 516 (1988)]; b (76); c (79); d (R. M. Zink and R. C. Blackwell, Mol. Phylogenet. Evol., in press); e [N. K. Johnson and C. Cicero, in Acta XX Congressus International Ornithologici (New Zealand Ornithological Congress Trust Board, Wellington, New Zealand, 1990), pp. 601-610]; f [R. M. Ball Jr. and J. C. Avise, Auk 109, 626 (1992)]; g (17); h [F. B. Gill and B. Slikas, Condor 94, 20 (1992)]; i [J. D. Rising and J. C. Avise, Auk 110, 844 (1993)]; j [J. C. Avise and W. S. Nelson, Science 243, 646 (1989)];
35. In the following, letters a through m correspond with the molecular study references shown in Table 1: a [J. C. Avise and R. M. Zink, Auk 105, 516 (1988)]; b (76); c (79); d (R. M. Zink and R. C. Blackwell, Mol. Phylogenet. Evol., in press); e [N. K. Johnson and C. Cicero, in Acta XX Congressus International Ornithologici (New Zealand Ornithological Congress Trust Board, Wellington, New Zealand, 1990), pp. 601-610]; f [R. M. Ball Jr. and J. C. Avise, Auk 109, 626 (1992)]; g (17); h [F. B. Gill and B. Slikas, Condor 94, 20 (1992)]; i [J. D. Rising and J. C. Avise, Auk 110, 844 (1993)]; j [J. C. Avise and W. S. Nelson, Science 243, 646 (1989)];
36. In the following, letters a through m correspond with the molecular study references shown in Table 1: a [J. C. Avise and R. M. Zink, Auk 105, 516 (1988)]; b (76); c (79); d (R. M. Zink and R. C. Blackwell, Mol. Phylogenet. Evol., in press); e [N. K. Johnson and C. Cicero, in Acta XX Congressus International Ornithologici (New Zealand Ornithological Congress Trust Board, Wellington, New Zealand, 1990), pp. 601-610]; f [R. M. Ball Jr. and J. C. Avise, Auk 109, 626 (1992)]; g (17); h [F. B. Gill and B. Slikas, Condor 94, 20 (1992)]; i [J. D. Rising and J. C. Avise, Auk 110, 844 (1993)]; j [J. C. Avise and W. S. Nelson, Science 243, 646 (1989)];
37. l (R. M. Zink, unpublished data);
38. and m (K. Omland and S. Lanyon, unpublished data).
39. S. Freeman and R. M. Zink, Syst. Biol. 44, 409 (1995).
40. Species are younger than the ages suggested by the coalescence times of their respective haplotypes, but this bias is minimal [W. S. Moore, Evolution 49, 718 (1995)]. Edwards [in Avian Molecular Systematics and Evolution. D. P. Mindell, Ed. (Academic Press, New York, 1997), pp. 251-278)] estimated an interspecific distance correction of 350,000 years, which would have the maximum effect of shifting values in Fig. 1 one column to the left.
41. Species are younger than the ages suggested by the coalescence times of their respective haplotypes, but this bias is minimal [W. S. Moore, Evolution 49, 718 (1995)]. Edwards [in Avian Molecular Systematics and Evolution. D. P. Mindell, Ed. (Academic Press, New York, 1997), pp. 251-278)] estimated an interspecific distance correction of 350,000 years, which would have the maximum effect of shifting values in Fig. 1 one column to the left.
42. Those 13 pairs are as follows: Mexican and Chestnut-backed chickadees (Parus sclateri versus P. rufescens, 4.75%), Black-capped and Mountain chickadees (Parus atricapillus versus P. gambeli, 4.1%) (16); Rusty and Brewer's blackbirds (Euphagus carolinus versus E. cyanocephalus, 5.4%), Hooded and Orchard orioles (Icterus cucullatus versus I. spurius, 4.6%), Bronzed and Shiny cowbirds (Molothrus aeneus versus M. bonariensis, 2.0%) (19), Baird's and Henslow's sparrows (Ammodramus bairdii versus A. henslowii, 4.9%), Seaside and Sharp-tailed sparrows (Ammodramus maritimus versus A. caudacutus, 2.15%) [R. M. Zink and J. C. Avise, Syst. Zool. 39, 148 (1990)], Bell's and White-eyed vireos (Vireo bellii versus V. griseus, 5.7%), Philadelphia and Warbling vireos (Vireo philadelphicus versus V. gilvus, 7.85%), Black-capped and Solitary vireos (Vireo atricapillus versus V. solitarius, 10.8%), Red-eyed and Black-whiskered vireos (Vireo olivaceus versus V. altiloquus, 4.5%) [B. W. Murray, W. B. McGillivray, J. C. Barlow, R. N. Beech, C. Strobeck, Condor 96, 1037 (1994)], Swamp and Lincoln's sparrows (Melosp/za georgiana versus M. Iincolnii, 3.6%), and Black-chinned and Field sparrows (Spizella atrogularis versus S. pusilla, 6.5%) (R. M. Zink, unpublished data).
43. Those 13 pairs are as follows: Mexican and Chestnut-backed chickadees (Parus sclateri versus P. rufescens, 4.75%), Black-capped and Mountain chickadees (Parus atricapillus versus P. gambeli, 4.1%) (16); Rusty and Brewer's blackbirds (Euphagus carolinus versus E. cyanocephalus, 5.4%), Hooded and Orchard orioles (Icterus cucullatus versus I. spurius, 4.6%), Bronzed and Shiny cowbirds (Molothrus aeneus versus M. bonariensis, 2.0%) (19), Baird's and Henslow's sparrows (Ammodramus bairdii versus A. henslowii, 4.9%), Seaside and Sharp-tailed sparrows (Ammodramus maritimus versus A. caudacutus, 2.15%) [R. M. Zink and J. C. Avise, Syst. Zool. 39, 148 (1990)], Bell's and White-eyed vireos (Vireo bellii versus V. griseus, 5.7%), Philadelphia and Warbling vireos (Vireo philadelphicus versus V. gilvus, 7.85%), Black-capped and Solitary vireos (Vireo atricapillus versus V. solitarius, 10.8%), Red-eyed and Black-whiskered vireos (Vireo olivaceus versus V. altiloquus, 4.5%) [B. W. Murray, W. B. McGillivray, J. C. Barlow, R. N. Beech, C. Strobeck, Condor 96, 1037 (1994)], Swamp and Lincoln's sparrows (Melosp/za georgiana versus M. Iincolnii, 3.6%), and Black-chinned and Field sparrows (Spizella atrogularis versus S. pusilla, 6.5%) (R. M. Zink, unpublished data).
44. J. D. Rising, in Current Ornithology, R. F. Johnston, Ed. (Plenum, New York, 1983), vol. 1, pp. 131-157.
45. The AOU [see (13)] Committee on Classification and Nomenclature considers the Timberline Sparrow to be a subspecies of Brewer's Sparrow, although we consider it a species (J. Klicka et al., unpublished data). This taxon pair is characterized by differences in morphology, ecology, and vocalizations [T. J. Doyle, Western Birds 28, 1 (1997)].
46. The AOU [see (13)] Committee on Classification and Nomenclature considers the Timberline Sparrow to be a subspecies of Brewer's Sparrow, although we consider it a species (J. Klicka et al., unpublished data). This taxon pair is characterized by differences in morphology, ecology, and vocalizations [T. J. Doyle, Western Birds 28, 1 (1997)].
47. DNA methods followed standard protocols (15). Primers for polymerase chain reaction included L14841 [T. D. Kocher et al., Proc. Natl. Acad. Sci. U.S.A. 86, 6196 (1989)]
48. and H4A [J. Harshman, thesis, University of Chicago (1996)] for cytochrome b (1050 bp),
49. and LGL2 and H417 [C. L. Tarr, Mol. Ecol. 4, 527 (1995)] for control region I (400 bp).
50. J. C. Avise, Evolution 43, 1192 (1989).
51. A. Wetmore, Smithson. Misc. Collect. 138 (no. 4), 1 (1959).
52. P. Brodkorb, In Avian Biology, D. S. Farner and J. R. King, Eds. (Academic Press, New York, 1971), vol. 1, pp. 19-55.
53. T. Webb and P. J. Bartlein, Annu. Rev. Ecol. Syst. 23, 141 (1992).
54. R. M. Zink and J. B. Slowinski, Proc. Natl. Acad. Sci. U.S.A. 92, 5832 (1995).
55. We thank D. Alstad, J. Curtsinger, R. Shaw, G. Hewitt, J. Avise, F. McKinney, S. Lanyon, S. Weller, C. Tarr, R. Fleischer, R. Sikes, and A. Kessen for comments. K. Omland and S. Lanyon provided unpublished data. We thank Louisiana State University (F. Sheldon) and the University of Washington (S. Edwards) for tissue samples. This work was funded in part by the Dayton and Wilkie Natural History Funds and NSF.