Environmental and genetic control of brain and song structure in the zebra finch

Evolution

Volumn 68, Issue 1, 2014, Pages 230-240

  Woodgate, Joseph L ^a,b,c   Buchanan, Katherine L ^a,b   Bennett, Andrew T D ^a   Catchpole, Clive K ^d   Brighton, Roswitha ^e   Leitner, Stefan ^e  

^a DEAKIN UNIVERSITY   (Australia)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF SUSSEX   (United Kingdom)

^d UNIVERSITY OF LONDON   (United Kingdom)

^e MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

Author keywords

Birdsong; Genotype by environment interaction; Heritability; HVC; Song system; Taeniopygia guttata

Indexed keywords

BRAIN; CONTROL SYSTEM; CULTURAL HERITAGE; GENETIC VARIATION; GENOTYPE-ENVIRONMENT INTERACTION; HERITABILITY; LEARNING; LIFE HISTORY TRAIT; PASSERINE; SEXUAL SELECTION; SONG;

PASSERI; TAENIOPYGIA GUTTATA;

ANIMAL; ARTICLE; BIRDSONG; BRAIN; FINCH; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; GENOTYPE-BY-ENVIRONMENT INTERACTION; HERITABILITY; HISTOLOGY; HVC; PHYSIOLOGY; SONG SYSTEM; TAENIOPYGIA GUTTATA; VOCALIZATION;

BIRDSONG; GENOTYPE-BY-ENVIRONMENT INTERACTION; HERITABILITY; HVC; SONG SYSTEM; TAENIOPYGIA GUTTATA;

ANIMALS; BRAIN; FINCHES; GENE-ENVIRONMENT INTERACTION; VOCALIZATION, ANIMAL;

EID: 84890891519     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12261     Document Type: Article

References (73)

1. Airey, D. C., H. Castillo-Juarez, G. Casella, E. J. Pollak, and T. J. DeVoogd 2000a. Variation in the volume of zebra finch song control nuclei is heritable: developmental and evolutionary implications. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 267:2099-2104.
2. Airey, D. C., D. E. Kroodsma, and T. J. DeVoogd 2000b. Differences in the complexity of song tutoring cause differences in the amount learned and in dendritic spine density in a songbird telencephalic song control nucleus. Neurobiol. Learn. Memory 73:274-281.
3. Andersson, M. 1994. Sexual selection. Princeton Univ. Press, Princeton, NJ.
4. Arnold, K. E., J. D. Blount, N. B. Metcalfe, K. J. Orr, A. Adam, D. Houston, and P. Monaghan 2007. Sex-specific differences in compensation for poor neonatal nutrition in the zebra finch, Taeniopygia guttata. J. Avian Biol. 38:356-366.
5. Birkhead, T. R., F. Fletcher, and E. J. Pellatt 1999. Nestling diet, secondary sexual traits and fitness in the zebra finch. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 266:385-390.
6. Blount, J. D., N. B. Metcalfe, K. E. Arnold, P. F. Surai, G. L. Devevey, and P. Monaghan 2003. Neonatal nutrition, adult antioxidant defences and sexual attractiveness in the zebra finch. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 270:1691-1696.
7. Boogert, N. J., L. A. Giraldeau, and L. Lefebvre 2008. Song complexity correlates with learning ability in zebra finch males. Anim. Behav. 76:1735-1741.
8. Brainard, M. S., and A. J. Doupe 2002. What songbirds teach us about learning. Nature 417:351-358.
9. Brenowitz, E. A., and M. D. Beecher 2005. Song learning in birds: diversity and plasticity, opportunities and challenges. Trends Neurosci. 28:127-132.
10. Buchanan, K. L., K. A. Spencer, A. R. Goldsmith, and C. K. Catchpole 2003. Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris). Proc. R. Soc. Lond. Ser. B-Biol. Sci. 270:1149-1156.
11. Buchanan, K. L., S. Leitner, K. A. Spencer, A. R. Goldsmith, and C. K. Catchpole 2004. Developmental stress selectively affects the song control nucleus HVC in the zebra finch. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 271:2381-2386.
12. Buchanan, K. L., J. Grindstaff, and V. V. Pravosudov 2013. Condition-dependence, developmental plasticity and cognition: implications for ecology and evolution. Trends Ecol. Evol. 28:290-296.
13. Catchpole, C. K., and P. J. B. Slater 2008. Bird song: biological themes and variations. Cambridge Univ. Press, New York.
14. Charlesworth, B. 1984. The evolutionary genetics of life histories. Pp. 117-133 in B. Shorrocks, ed. Evolutionary ecology. Blackwell Scientific Publications, Oxford, U.K.
15. Christe, P., A. P. Møller, N. Saino, and F. De Lope 2000. Genetic and environmental components of variation in immune response and body size of a colonial bird, Delichon urbica (the house martin). Heredity 85:75-83.
16. Clayton, N. S. 1987. Song learning in cross-fostered zebra finches-a reexamination of the sensitive phase. Behaviour 102:67-81.
17. Cotton, S., K. Fowler, and A. Pomiankowski 2004. Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc. R. Soc. Lond. Ser. B-Biol. Sci. 271:771-783.
18. Danielson-Francois, A. M., J. K. Kelly, and M. D. Greenfield 2006. Genotype x environment interaction for male attractiveness in an acoustic moth: evidence for plasticity and canalization. J. Evol. Biol. 19:532-542.
19. de Kogel, C. H. 1997. Long-term effects of brood size manipulation on morphological development and sex-specific mortality of offspring. J. Anim. Ecol. 66:167-178.
20. DeVoogd, T. J., J. R. Krebs, S. D. Healy, and A. Purvis 1993. Relations between song repertoire size and the volume of brain nuclei related to song-comparative evolutionary analyses amongst oscine birds. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 254:75-82.
21. Farrell, T. M., K. Weaver, Y. S. An, and S. A. MacDougall-Shackleton 2012. Song bout length is indicative of spatial learning in European starlings. Behav. Ecol. 23:101-111.
22. Forstmeier, W., G. Segelbacher, J. C. Mueller, and B. Kempenaers 2007. Genetic variation and differentiation in captive and wild zebra finches (Taeniopygia guttata). Mol. Ecol. 16:4039-4050.
23. Forstmeier, W., C. Burger, K. Temnow, and S. Deregnaucourt 2009. The genetic basis of zebra finch vocalizations. Evolution 63:2114-2130.
24. Gil, D., M. Naguib, K. Riebel, A. Rutstein, and M. Gahr 2006. Early condition, song learning, and the volume of song brain nuclei in the zebra finch (Taeniopygia guttata). J. Neurobiol. 66:1602-1612.
25. Goymann, W., M. Trappschuh, W. Jensen, and I. Schwabl 2006. Low ambient temperature increases food intake and dropping production, leading to incorrect estimates of hormone metabolite concentrations in European stonechats. Horm. Behav. 49:644-653.
26. Greenfield, M. D., and R. L. Rodriguez 2004. Genotype-environment interaction and the reliability of mating signals. Anim. Behav. 68:1461-1468.
27. Hardouin, L. A., D. Reby, C. Bavoux, G. Burneleau, and V. Bretagnolle 2007. Communication of male quality in owl hoots. Am. Nat. 169:552-562.
28. Healy, S. D., and C. Rowe 2007. A critique of comparative studies of brain size. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 274:453-464.
29. Higginson, A. D., and T. Reader 2009. Environmental heterogeneity, genotype-by-environment interactions and the reliability of sexual traits as indicators of mate quality. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 276:1153-1159.
30. Hoffmann, A. A., and J. Merila 1999. Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol. Evol. 14:96-101.
31. Houle, D. 1992. Comparing evolvability and variability of quantitative traits. Genetics 130:195-204.
32. Hurley, P., C. Pytte, and J. R. Kirn 2008. Nest of origin predicts adult neuron addition rates in the vocal control system of the zebra finch. Brain Behav. Evol. 71:263-270.
33. Jia, F. Y., M. D. Greenfield, and R. D. Collins 2000. Genetic variance of sexually selected traits in waxmoths: maintenance by genotype x environment interaction. Evolution 54:953-967.
34. Kilner, R. 1998. Primary and secondary sex ratio manipulation by zebra finches. Anim. Behav. 56:155-164.
35. Kirn, J. R. 2010. The relationship of neurogenesis and growth of brain regions to song learning. Brain Lang. 115:29-44.
36. Kokko, H., and K. Heubel 2008. Condition-dependence, genotype-by-environment interactions and the lek paradox. Genetica 134:55-62.
37. Kotrschal, A., B. Rogell, A. Bundsen, B. Svensson, S. Zajitschek, I. Brannstrom, S. Immler, A. A. Maklakov, and N. Kolm 2013. Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain. Curr. Biol. 23:168-171.
38. Kremen, W. S., E. Prom-Wormley, M. S. Panizzon, L. T. Eyler, B. Fischl, M. C. Neale, C. E. Franz, M. J. Lyons, J. Pacheco, M. E. Perry, et al. 2010. Genetic and environmental influences on the size of specific brain regions in midlife: The VETSA MRI study. Neuroimage 49:1213-1223.
39. Leitner, S., and C. K. Catchpole 2002. Female canaries that respond and discriminate more between male songs of different quality have a larger song control nucleus (HVC) in the brain. J. Neurobiol. 52:294-301.
40. Lovell, P. V., D. F. Clayton, K. L. Replogle, and C. V. Mello 2008. Birdsong "transcriptomics": neurochemical specializations of the oscine song system. PLoS ONE 3:e3440.
41. MacDonald, I. F., B. Kempster, L. Zanette, and S. A. MacDougall-Shackleton 2006. Early nutritional stress impairs development of a song-control brain region in both male and female juvenile song sparrows (Melospiza melodia) at the onset of song learning. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 273:2559-2564.
42. MacDougall-Shackleton, S., and K. Spencer 2012. Developmental stress and birdsong: current evidence and future directions. J. Ornithol. 153:S105-S117.
43. Mager, J. N., C. Walcott, and W. H. Piper 2007. Male common loons, Gavia immer, communicate body mass and condition through dominant frequencies of territorial yodels. Anim. Behav. 73:683-690.
44. Marler, P. 1990. Song learning-the interface between behavior and neuroethology. Philos. Trans. R. Soc. Lond. Ser. B-Biol. Sci. 329:109-114.
45. Martins, T. L. F. 2004. Sex-specific growth rates in zebra finch nestlings: a possible mechanism for sex ratio adjustment. Behav. Ecol. 15:174-180.
46. Merila, J. 1996. Genetic variation in offspring condition: an experiment. Funct. Ecol. 10:465-474.
47. Metcalfe, N. B., and P. Monaghan 2001. Compensation for a bad start: grow now, pay later? Trends Ecol. Evol. 16:254-260.
48. Metcalfe, N. B., and P. Monaghan 2003. Growth versus lifespan: perspectives from evolutionary ecology. Exp. Gerontol. 38:935-940.
49. Miller, D. B. 1979. Long-term recognition of father's song by female zebra finches. Nature 280:389-391.
50. Nowicki, S., S. Peters, and J. Podos 1998. Song learning, early nutrition and sexual selection in songbirds. Am. Zool. 38:179-190.
51. Nowicki, S., W. A. Searcy, and S. Peters 2002. Brain development, song learning and mate choice in birds: a review and experimental test of the "nutritional stress hypothesis". J. Comp. Physiol. A-Neuroethol. Sens. Neural Behav. Physiol. 188:1003-1014.
52. Peper, J. S., R. M. Brouwer, D. I. Boomsma, R. S. Kahn, and H. E. H. Poll 2007. Genetic influences on human brain structure: a review of brain imaging studies in twins. Hum. Brain Mapp. 28:464-473.
53. Pomiankowski, A., and A. P. Møller 1995. A resolution of the lek paradox. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 260:21-29.
54. Qvarnström, A., T. Part, and B. C. Sheldon 2000. Adaptive plasticity in mate preference linked to differences in reproductive effort. Nature 405:344-347.
55. Reiner, A., D. J. Perkel, L. L. Bruce, A. B. Butler, A. Csillag, W. Kuenzel, L. Medina, G. Paxinos, T. Shimizu, G. Striedter, et al. 2004. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J. Comp. Neurol. 475:288-288.
56. Riebel, K. 2009. Song and female mate choice in zebra finches: a review. Adv. Study Behav. 40:197-238.
57. Ruploh, T., H. J. Bischof, and N. von Engelhardt 2013. Adolescent social environment shapes sexual and aggressive behaviour of adult male zebra finches (Taeniopygia guttata). Behav. Ecol. Sociobiol. 67:175-184.
58. Sartor, J. J., and G. F. Ball 2005. Social suppression of song is associated with a reduction in volume of a song-control nucleus in European starlings (Sturnus vulgaris). Behav. Neurosci. 119:233-244.
59. Schmidt, K. L., E. A. MacDougall-Shackleton, and S. A. MacDougall-Shackleton 2012. Developmental stress has sex-specific effects on nestling growth and adult metabolic rates but no effect on adult body size or body composition in song sparrows. J. Exp. Biol. 215:3207-3217.
60. Sockman, K. W., K. G. Salvante, D. M. Racke, C. R. Campbell, and B. A. Whitman 2009. Song competition changes the brain and behavior of a male songbird. J. Exp. Biol. 212:2411-2418.
61. Soma, M., M. Takahasi, M. Ikebuchi, H. Yamada, M. Suzuki, T. Hasegawa, and K. Okanoya 2006. Early rearing conditions affect the development of body size and song in Bengalese finches. Ethology 112:1071-1078.
62. Spencer, K. A., and S. A. MacDougall-Shackleton 2011. Indicators of development as sexually selected traits: the developmental stress hypothesis in context. Behav. Ecol. 22:1-9.
63. Swaddle, J. P. 2011. Assessing the developmental stress hypothesis in the context of a reaction norm. Behav. Ecol. 22:13-14.
64. Tchernichovski, O., and F. Nottebohm 1998. Social inhibition of song imitation among sibling male zebra finches. Proc. Natl. Acad. Sci. U. S. A. 95:8951-8956.
65. Turelli, M., and N. H. Barton 2004. Polygenic variation maintained by balancing selection: pleiotropy, sex-dependent allelic effects and GxE interactions. Genetics 166:1053-1079.
66. Visscher, P. M., W. G. Hill, and N. R. Wray 2008. Heritability in the genomics era-concepts and misconceptions. Nat. Rev. Genet. 9:255-266.
67. Ward, B. C., E. J. Nordeen, and K. W. Nordeen 2001. Anatomical and ontogenetic factors producing variation in HVC neuron number in zebra finches. Brain Res. 904:318-326.
68. Wilkinson, G. S. 1987. Equilibrium analysis of sexual selection in Drosophila melanogaster. Evolution 41:11-21.
69. Woodgate, J. L., A. T. D. Bennett, S. Leitner, C. K. Catchpole, and K. L. Buchanan 2010. Developmental stress and female mate choice behaviour in the zebra finch. Anim. Behav. 79:1381-1390.
70. Woodgate, J. L., M. M. Mariette, A. T. D. Bennett, S. C. Griffith, and K. L. Buchanan 2012. Male song structure predicts reproductive success in a wild zebra finch population. Anim. Behav. 83:773-781.
71. Yu, A. C., and D. Margoliash 1996. Temporal hierarchical control of singing in birds. Science 273:1871-1875.
72. Zann, R. A. 1996. The zebra finch: a synthesis of field and laboratory studies. Oxford Univ. Press, Oxford, U.K.
73. Zollinger, S. A., J. Podos, E. Nemeth, F. Goller, and H. Brumm 2012. On the relationship between, and measurement of, amplitude and frequency in birdsong. Anim. Behav. 84:E1-E9.