Evolutionary significance of phenotypic accommodation in novel environments: An empirical test of the Baldwin effect

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 364, Issue 1520, 2009, Pages 1125-1141

  Badyaev, Alexander V ^a  

^a University of Arizona   (United States)

Author keywords

Baldwin effect; Developmental plasticity; Evolution; Hormones; Inheritance; Maternal effects

Indexed keywords

ADAPTATION; COLONIZATION; ENVIRONMENTAL CONDITIONS; EVOLUTIONARY BIOLOGY; EVOLUTIONARY THEORY; FITNESS; GENETIC VARIATION; HORMONE; MATERNAL EFFECT; NATURAL SELECTION; PHENOTYPIC PLASTICITY; SURVIVAL;

CARPODACUS MEXICANUS;

ACCLIMATIZATION; ADAPTATION; ANIMAL; ARTICLE; BIOLOGICAL MODEL; BODY SIZE; CLIMATE; ENVIRONMENT; FEMALE; FINCH; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; MALE; MATERNAL BEHAVIOR; MOLECULAR EVOLUTION; PHENOTYPE; PHYSIOLOGY; SEXUAL DEVELOPMENT; UNITED STATES;

ACCLIMATIZATION; ADAPTATION, PHYSIOLOGICAL; ANIMALS; BODY SIZE; CLIMATE; ENVIRONMENT; EVOLUTION, MOLECULAR; FEMALE; FINCHES; GENETIC VARIATION; MALE; MATERNAL BEHAVIOR; MODELS, GENETIC; PHENOTYPE; SELECTION (GENETICS); SEX CHARACTERISTICS; UNITED STATES;

EID: 65649086418     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2008.0285     Document Type: Article

References (104)

1. Alonso-Alvarez, C. 2006 Manipulation of primary sex-ratio: an updated review. Avian Poult. Biol. Rev. 17, 1-20. (doi:10.3184/ 147020606783437930)
2. Ancel, L. W. 1999 A quantitative model of the Simpson-Baldwin effect. J. Theor. Biol. 196, 197-209. (doi:10.1006/jtbi.1998.0833)
3. Andersson, M., Wallander, J., Oring, L., Akst, E., Reed, J. M. & Fleischer, R. C. 2003 Adaptive seasonal trend in brood sex ratio: test in two sister species with contrasting breeding systems. J. Evol. Biol. 16, 510-515. (doi: 10.1046/j. 1420-9101.2003.00533.x)
4. Badyaev, A. V. 2005a Maternal inheritance and rapid evolution of sexual size dimorphism: passive effects or active strategies? Am. Nat. 166, S17-S30. (doi:10.1086/444601)
5. Badyaev, A. V. 2005b Stress-induced variation in evolution: from behavioral plasticity to genetic assimilation. Proc. R. Soc. B 272, 877-886. (doi:10.1098/rspb.2004.3045)
6. Badyaev, A. V. 2007 Evolvability and robustness in color displays: bridging the gap between theory and data. Evol. Biol. 34, 61-71. (doi:10.1007/sll692-007-9004-5)
7. Badyaev, A. V. 2008 Maternal effects as generators of evolutionary change: a reassessment. In The year in evolutionary biology 2008 (eds C. D. Schlichting & T. A. Mousseau), pp. 151-161. New York, NY: Wiley-Blackwell.
8. Badyaev, A. V. & Hill, G. E. 2000 The evolution of sexual dimorphism in the house finch. I. Population divergence in morphological covariance structure. Evolution 54, 1784-1794. (doi:10.1111/j0014-3820.2000. tb00722.x)
9. Badyaev, A. V. & Martin, T. E. 2000a Individual variation in growth trajectories: phenotypic and genetic correlations in ontogeny of the house finch (Carpodacus mexicanus). J. Evol. Biol. 13, 290-301. (doi: 10.1046/j.1420-9101. 2000.00172.x)
10. Badyaev, A. V. & Martin, T. E. 2000b Sexual dimorphism in relation to current selection in the house finch. Evolution 54, 987-997. (doi:10.1111/j.0014-3820.2000.tb0098.x)
11. Badyaev, A. V. & Oh, K. P. 2008 Environmental induction and phenotypic retention of adaptive maternal effects. BMC Evol. Biol. 8, 3. (doi:10.1186/1471-2148-8-3)
12. Badyaev, A. V., Hill, G. E., Stoehr, A. M., Nolan, P. M. & McGraw, K. J. 2000 The evolution of sexual dimorphism in the house finch: II. Population divergence in relation to local selection. Evolution 54, 2134-2144. (doi:10.1111/j.0014-3820.2000.tb01255.x)
13. Badyaev, A. V., Hill, G. E. & Whittingham, L. A. 2001a The evolution of sexual size dimorphism in the house finch: IV. Population divergence in ontogeny of dimorphism. Evolution 55, 2534-2549. (doi:10.1111/j.0014-3820. 2001.tb00767.x)
14. Badyaev, A. V., Whittingham, L. A. & Hill, G. E. 2001b The evolution of sexual size dimorphism in the house finch: III. Developmental basis. Evolution 55, 176-189. (doi:10. 1111/j.0014-3820.200 l.tbO 1282.x)
15. Badyaev, A. V., Hill, G. E., Beck, M. L., Dervan, A. A., Duckworth, R. A., McGraw, K. J., Nolan, P. M. & Whittingham, L. A. 2002a Sex-biased hatching order and adaptive population divergence in a passerine bird. Science 295, 316-318. (doi:10.1126/science.1066651)
16. Badyaev, A. V., Hill, G. E. & Whittingham, L. A. 2002b Population consequences of maternal effects: sex-biased hatching order produces divergence in sexual dimorphism between newly established bird populations. J. Evol. Biol. 15, 997-1003. (doi:10.1046/j.1420-9101.2002.00462.x)
17. Badyaev, A. V., Beck, M. L., Hill, G. E. & Whittingham, L. A. 2003a The evolution of sexual size dimorphism in the house finch: V. Maternal effects. Evolution 57, 384-396. (doi:10.1111/j.0014-3820.2003.tb00272.x)
18. Badyaev, A. V., Hill, G. E. & Beck, M. L. 2003b Interaction between maternal effects: onset of incubation is related to offspring sex in a passerine bird. Oecologia 135, 386-390.
19. Badyaev, A. V., Schwabl, H., Young, R. L., Duckworth, R. A., Navara, K. & Parlow, A. F. 2005 Adaptive sex differences in growth of pre-ovulation oocytes in a passerine bird. Proc. R. Soc. B 272, 2165-2172. (doi:10. 1098/rspb.2005.3194)
20. Badyaev, A. V., Acevedo Seaman, D., Navara, K. J., Hill, G. E. & Mendonça, M. T. 2006a Evolution of sex-biased maternal effects in birds: III. Adjustment of ovulation order can enable sex-specific allocation of hormones, carotenoids, and vitamins. J. Evol. Biol. 19, 1044-1057. (doi:10.1111/j.1420-9101.2006.01106.x)
21. Badyaev, A. V., Hamstra, T. L., Oh, K. P. & Acevedo Seaman, D. 2006b Sex-biased maternal effects reduce ectoparasite-induced mortality in a passerine bird. Proc. Natl Acad. Sci. USA 103, 14 406-14 411. (doi:10.1073/pnas.0602452103)
22. Badyaev, A. V., Oh, K. P. & Mui, R. 2006c Evolution of sex-biased maternal effects in birds: II. Contrasting sex-specific oocyte competition in native and recently established populations. J. Evol. Biol. 19, 909-921. (doi: 10.1111/j. 1420-9101.2005.01041.x)
23. Badyaev, A. V., Young, R. L., Hill, G. E. & Duckworth, R. A. 2008 Evolution of sex-biased maternal effects in birds: IV. Intra-ovarian growth dynamics can link sex-determination and sex-specific acquisition of resources. J. Evol. Biol. 21, 449-460. (doi:10.1111/j.1420-9101.2007.01498.x)
24. Baldwin, J. M. 1896 A new factor in evolution. Am. Nat. 30, 441-451. (doi: 10.1086/276408)
25. Baldwin, J. M. 1902 Development and evolution. New York, NY: Macmillan.
26. Ball, G. F. & Balthazart, J. 2008 Individual variation and the endocrine regulation of behavior and physiology in birds: a cellular/molecular perspective. Phil. Trans. R. Soc. B 363, 1699-1710. (doi:10.1098/rstb.2007.0010)
27. Blanco, G., Dávila, J. A., López Septiem, J. A., Rodríguez, R. & Martínez, F. 2002 Sex-biased initial eggs favour sons in the slightly size-dimorphic scops owl (Otus scops). Biol. J. Linn. Soc. 76, 1-7. (doi:10.1111/j.1095-8312. 2002.tb01709.x)
28. Bortolotti, G. R. 1986 Influence of sibling competition on nestling sex ratios of sexually dimorphic birds. Am. Nat. 127, 495-507. (doi: 10.1086/284498)
29. Carere, C. & Balthazart, J. 2007 Sexual versus individual differentiation: the controversial role of avian maternal hormones. Trends Endocrinol. Metab. 18, 73-80. (doi: 10. 1016/j.tem.2007.01.003)
30. Carroll, S. B. 2005 Evolution at two levels: on genes and form. PLoS Biol. 3, e245. (doi:10.1371/journal.pbio.0030245)
31. Cheng, M.-F. 1986 Female cooing promotes ovarian development in ring doves. Physiol. Behav. 37 371-374. (doi:10.1016/0031-9384(86) 90248-9)
32. Chetverikov, S. S. 1926 On certain aspects of the evolutionary process from the standpoint of modern genetics. J. Exp. Biol. Ser. A 2, 1-40.
33. Clark, A. B. & Wilson, D. S. 1981 Avian breeding adaptations: hatching asynchrony, brood reduction, and nest failure. Q. Rev. Biol. 56, 253-277. (doi:10.1086/412316)
34. Conway, C. J. & Martin, T. E. 2000 Evolution of passerine incubation behavior: influence of food, temperature, and nest prédation. Evolution 54, 670-685. (doi:10.1111/j.0014-3820.2000.tb00068.x)
35. Cope, E. D. 1887 The origin of the fittest: essays on evolution. New York, NY: Appleton.
36. Cordero, P. J., Vinuela, J., Aparicio, J. M. & Veiga, J. P. 2001 Seasonal variation in sex ratio and sexual egg dimorphism favouring daughters in first clutches of the spotless starling. J. Evol. Biol. 14, 829-834. (doi:10.1046/j.1420-9101.2001.00320.x)
37. Davidson, E. H. 2006 The regulatory genome: gene regulatory networks in development and evolution. San Diego, CA: Academic Press.
38. Dijkstra, C., Daan, S. & Buker, J. B. 1990 Adaptive seasonal variation in the sex ratio of kestrel broods. Fund. Ecol. 4, 143-147. (doi:10.2307/2389333)
39. Dobzhansky, T. 1937 Genetics and the origin of species. New York: Columbia University Press.
40. Duckworth, R. A. In press. The role of behavior in evolution: a search for mechanism. Evol. Ecol. 22.(doi:10.1007/S10682-008-9252-6)
41. Duckworth, R. A. 2009 Maternal effects and range expansion: a key factor in a dynamic process? Phil. Trans. R. Soc. B 364, 1075-1086. (doi:10.1098/rstb.2008.0294)
42. Duckworth, R. A., Badyaev, A. V., Farmer, K. L., Hill, G. E. & Roberts, S. R. 2003 First case of mycoplasmosis in the native range of the house finch (Carpodacus mexicanus). Auk 120, 528-530. (doi: 10.1642/0004-8038 (2003) 120[0528: FCO MGI]2.0.CO;2)
43. Eising, C. M., Muller, W., Dijkstra, C. & Groothuis, G. G. 2003 Maternal androgens in egg yolks: relation with sex, incubation time and embryonic growth. Gen. Comp. Endocrinol. 132, 241-247. (doi:10.1016/S0016-6480(03) 00090-X)
44. Elliott, J. J. & Arbib, R. S. 1953 Origin and status of the house finch in the eastern United States. Auk 70, 31-37.
45. Etches, R. J., Gargbutt, A. & Middleton, A. L. 1979 Plasma concentrations of prolactin during egg laying and incubation in the ruffed grouse (Bonasa umbellus). Can. J. Zool. 57, 1624-1627. (doi:10.1139/z79-213)
46. Gerhart, J. & Kirschner, M. 2007 The theory of facilitated variation. Proc. Natl Acad. Sci. USA 104, 8582-8589. (doi:10.1073/pnas. 0701035104)
47. Gould, S. J. 2002 The structure of evolutionary theory. Cambridge, MA: Belknap Press, Harvard University Press.
48. Grinnell, J. 1911 The linnet of the Hawaiian Islands: a problem in speciation. Univ. Calif. Publ. Zool. 7, 79-95.
49. Hébert, P. N. 2002 Ecological factors affecting initiation of incubation behaviour. In Avian incubation: behaviour, environment, and evolution (ed. D. C. Deeming), pp. 271-279. New York, NY: Oxford University Press.
50. Hill, G. E. 2002 A red bird in a brown bag: the function and evolution of colorful plumage in the house finch. New York, NY: Oxford University Press.
51. Jablonka, E. 2001 The systems of inheritance. In Cycles of contingency: developmental systems and evolution (eds S. Oyama, P. E. Griffiths & R. D. Gray), pp. 99-116. Cambridge, MA: MIT Press.
52. Jablonka, E. & Lamb, M. J. 1995 Epigenetic inheritance and evolution: the Lamarckian dimension. Oxford, UK: Oxford University Press.
53. Jablonka, E., Oborny, B., Molnar, I., Kisdi, E., Hofbauer, J. & Czaran, T. 1995 The adaptive advantage of phenotypic memory in changing environments. Phil. Trans. R. Soc. B 350, 133-141. (doi:10.1098/rstb.1995.0147)
54. Johnson, A. L. 2000 Reproduction in the female. In Sturkie's avian physiology (éd. G. C. Whittow), pp. 569-596. San Diego, CA: Academic Press.
55. King, M. C. & Wilson, A. C. 1975 Evolution at two levels in humans and chimnanzees. Science 188, 107-116. (doi:10. 1126/science.1090005)
56. Kirschner, M. & Gerhart, J. C. 2005 The plausibility of life: resolving Darwin's Dilemma. New Haven, CT: Yale University Press.
57. Kopp, M. & Hermisson, J. 2006 The evolution of genetic architecture under frequency-dependent disruptive selection. Evolution 60, 1537-1550. (doi: 10.1554/06-220.1)
58. Lande, R. 1976 Natural selection and random genetic drift in phenotypic evolution. Evolution 30, 314-334. (doi: 10. 2307/2407703)
59. Lewontin, R. C. 1970 The units of evolution. Annu. Rev. Ecol. 1, 1-23. (doi:10.1146/annurev.es.01.110170.000245)
60. Lewontin, R. C. 1974 The genetic basis of evolutionary change. New York, NY: Columbia University Press.
61. Losos, J. B. & Queiroz, K. D. 1997 Evolutionary consequences of ecological release in Caribbean Anolis lizards. Biol. J. Linn. Soc. 61, 459-483. (doi:10.1111/j.1095-8312. 1997.tb01802.x)
62. Martin, T. E., Auer, S. K., Bassar, R. D., Niklison, A. M. & Lloyd, P. 2007 Geographic variation in avian incubation periods and parental influences on embryonic temperature. Evolution 61, 2558-2569. (doi: 10.1111/j.1558-5646. 2007.00204.x)
63. Mayr, E. 1960 The emergence of evolutionary novelties. In Evolution after Darwin, vol. 1 (ed. S. Tax), pp. 349-380. Chicago, IL: The University of Chicago
64. Mayr, E. 1982 The growth of biological thought. Cambridge, MA: Belknap Press, Harvard University Press.
65. Mead, P. S. & Morton, M. L. 1985 Hatching asynchrony in the mountain white-crowned sparrow (Zonotrichia leucophyris oriantha): a selected or incidental trait? Auk 102, 781-792.
66. Morgan, C. L. 1896 Habit and instinct. London, UK: Arnold.
67. Mousseau, T. A. & Dingle, H. 1991 Maternal effects in insects: examples, constraints, and geographical variation. In The unity of evolutionary biology (ed. E. C. Dudley), pp. 745-761. Portland, OR: Dioscorides Press.
68. Mousseau, T. A. & Fox, C. W (eds) 1998 Maternal effects as adaptations. Oxford, UK: Oxford University Press.
69. Müller, G. B. & Newman, S. 2003 Origination of organismal form: beyond the gene in developmental and evolutionary biology. Cambridge, MA: MIT Press.
70. Müller, G. B. & Newman, S. A. 2005 The innovation triad: an EvoDevo agenda. J. Exp. Zool. B (Mol. Dev. Evol.) 304, 487-503. (doi:10.1002/jez.b.21081)
71. Müller, G. B. & Wagner, G. P. 1991 Novelty in evolution: restructuring the concept. Annu. Rev. Ecol. Syst. 22, 229-256. (doi:10.1146/annurev.es.22.110191.001305)
72. Mundinger, P. C. & Hope, S. 1982 Expansion of the winter range of the house finch: 1947-1979. Am. Birds 36, 347-353.
73. Newman, S. A. & Müller, G. B. 2000 Epigenetic mechanisms of character origination. J. Exp. Zool. 288, 304-314. (doi:10. 1002/1097-010X(20001215)288:4<304::AID-JEZ3>3.0. CO; 2-G)
74. Osborn, H. F. 1896 A mode of evolution requiring neither natural selection nor the inheritance of acquired characteristics. Trans. NY Acad. Sci. 15, 141-142.
75. Oyama, S. 2000 The ontogeny of information: developmental systems and evolution. Science and cultural theory. Durham, NC: Duke University Press.
76. Pfaff, D. W., Phillips, M. I. & Rubun, R. T. 2004 Principles of hormone/behavior relations. Amsterdam, The Netherlands: Elsevier.
77. Pigliucci, M. & Murren, C. J. 2003 Perspective: genetic assimilation and a possible evolutionary paradox: can macroevolution sometimes be so fast as to pass us by? Evolution 57, 1455-1464. (doi:10.1111/j.0014-3820. 2003.tb00354.x)
78. Pike, T. W. & Pétrie, M. 2006 Experimental evidence that corticosterone affects offspring sex ratios in quail. Proc. R. Soc. B 273, 1093-1098. (doi:10.1098/rspb.2005.3422)
79. Reid, R. G. B. 1985 Evolutionary theory: the unfinished synthesis. Beckenham, UK: Crom Helm.
80. Reid, R. G. B. 2007 Biological emergences: evolution by natural experiment. Vienna Series in Theoretical Biology. Cambridge, MA: MIT Press.
81. Ricklefs, R. E. 1993 Sibling competition, hatching asyn-chrony, incubation period, and lifespan in altricial birds. Curr. Ornithol. 11, 199-276.
82. Rutkowska, J. & Badyaev, A. V. 2008 Meiotic drive and sex determination: molecular mechanisms of sex ratio adjustment in birds. Phil. Trans. R. Soc. B 363, 1675-1686. (doi:10.1098/rstb.2007.0006)
83. Schmalhausen, I. I. 1938 Organism as a whole in individual development and history. Leningrad, Russia: Academy of Sciences, USSR.
84. Severtsov, A. H. 1934 Principal directions of the evolutionary process. Leningrad, Russia: Biomedgiz.
85. Simpson, G. G. 1953 The Baldwin effect. Evolution 7, 110-117. (doi:10.2307/2405746)
86. Simpson, G. G. 1984 Tempo and mode in evolution. A Columbia classic in evolution. New York, NY: Columbia University Press.
87. Sockman, K. W. & Schwabl, H. 1999 Daily estradiol and progesterone levels relative to laying and onset of incubation in canaries. Gen. Comp. Endocrinol. 114, 257-268. (doi:10.1006/gcen.1999.7252)
88. Sockman, K. W., Schwabl, H. & Sharp, P. J. 2001 Regulation of yolk-androgen concentrations by plasma prolactin in the American Kestrel. Horm. Behav. 40, 462-471. (doi:10. 1006/hbeh.2001.1715)
89. Sockman, K. W., Gentner, T. Q. & Ball, G. F. 2002 Recent experience modulates forebrain gene-expression in response to mate choice cues in European starlings. Proc. R. Soc. B 269, 2479-2485. (doi:10.1098/rspb. 2002.2180)
90. Sockman, K. W., Sharp, P. J. & Schwabl, H. 2006 Orchestration of avian reproductive effort: an integration of the ultimate and proximate bases for flexibility of clutch size, incubation behavior, and yolk-androgen deposition. Biol. Rev. 81, 629-666. (doi:10.1017/S146479310 6007147)
91. Stern, D. L. 2000 Evolutionary developmental biology and the problem of variation. Evolution 54, 1079-1091. (doi:10.1111/j.0014-3820.2000. tb00544.x)
92. Stoleson, S. H. & Beissinger, S. R. 1995 Hatching asynchrony and the onset of incubation in birds, revisited: when is the crucial period? Curr. Ornithol. 12, 191-270.
93. Tabibzadeh, C., Rozenboim, I., Silsby, J. L., Pitts, G. R., Foster, D. N. & El Halawani, M. E. 1995 Modulation of ovarian cytochrome P 450 17a-hydroxylase and cyto-chrome aromatase messenger ribonucleic acid by prolacin in the domestic turkey. Biol. Reprod. 52, 600-608. (doi:10. 1095/biolreprod52.3.600)
94. Ulier, T. 2008 Developmental plasticity and the evolution of parental effects. Trends Ecol. Evol. 23, 432-438. (doi: 10. 1016/j.tree.2008.04.005)
95. Van Valen, L. 1965 Morphological variation and width of the ecological niche. Am. Nat. 94, 377-390. (doi:10.1086/282379)
96. Vleck, C. M. 2002 Hormonal control of incubation behaviour. In Avian incubation: behaviour, environment, and evolution (éd. D. C. Deeming), pp. 54-62. New York, NY: Oxford University Press.
97. Waddington, C. H. 1953 Genetic assimilation of an acquired character. Evolution 7, 119-127. (doi: 10.2307/2405747)
98. Webb, D. R. 1987 Thermal tolerance of avian embryos; a review. Condor 89, 874-898. (doi:10.2307/1368537)
99. Weismann, A. 1896 Uber Germinal Selektion: Eine Quelle bestimmt gerichterer Variation. Jena, Germany: Gustav Fischer.
100. West-Eberhard, M. J. 2003 Developmental plasticity and evolution. Oxford, UK: Oxford University Press.
101. West-Eberhard, M. J. 2005 Phenotypic accommodation: adaptive innovation due to developmental plasticity. J. Exp. Zool. B (Mol. Dev. Evol.) 304, 610-618. (doi: 10. 1002/jez.b.21071)
102. Whyte, L. L. 1965 Internal factors in evolution. New York, NY: George Braziller.
103. Williams, T. D., Ames, C. E., Kiparissis, Y & Wynne-Edwards, K. E. 2005 Laying-sequence-specific variation in yolk oestrogen levels, and relationship to plasma oestrogen in female zebra finches (Taeniopygia guttatd). Proc. R. Soc. B 272, 173-177. (doi:10.1098/rspb.2004.2935)
104. Yoo, B. H., Sheldon, B. L. & Podger, R. N. 1986 Analyses of oviposition times and intervals in a wide range of layer flocks under normal and continuous lighting regimes. Br. Poult. Sci. 27, 267-288. (doi:10.1080/0007166860 8416880)