Postnatal nutrition influences male attractiveness and promotes plasticity in male mating preferences

Abstract

Poor early-life nutrition could reduce adult reproductive success by negatively affecting traits linked to sexual attractiveness such as song complexity. If so, this might favor strategic mate choice, allowing males with less complex songs to tailor their mating tactics to maximize the reproductive benefits. However, this possibility has been ignored in theoretical and empirical studies. By manipulating the micronutrient content of the diet (e.g., low or high) during the postnatal period of male zebra finches, we show for the first time (1) that males reared on a poor (low) micronutrient diet had less complex songs as adults; (2) that these males, in contrast to the high micronutrient diet group, were more selective in their mating strategies, discriminating against those females most likely to reduce their clutch size when paired with males having less complex songs; and (3) that by following different mating strategies, males reared on the contrasting diets obtained similar reproductive benefits. These results suggest that early-life dietary conditions can induce multiple and long-lasting effects on male and female reproductive traits. Moreover, the results seem to reflect a previously unreported case of adaptive plasticity in mate choice in response to a nutritionally mediated reduction in sexual attractiveness.

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References

  1. Adar E, Lotem A et al (2008) The effect of social environment on singing behavior in the zebra finch (Taeniopygia guttata) and its implication for neuronal recruitment. Behav Brain Res 187:178–184

    Article  PubMed  Google Scholar 

  2. Alonso-Alvarez C, Bertrand S et al (2006) An experimental manipulation of life-history trajectories and resistance to oxidative stress. Evolution 60:1913–1924

    Article  PubMed  Google Scholar 

  3. Amundsen T (2000) Why are female birds ornamented? Trends Ecol Evol 15:149–155

    CAS  Article  PubMed  Google Scholar 

  4. Amundsen T, Forsgren E (2003) Male preference for colourful females affected by male size in a marine fish. Behav Ecol Sociobiol 54:55–64

    Article  Google Scholar 

  5. Amundsen T, Forsgren E et al (1997) On the function of female ornaments: male bluethroats prefer colourful females. Proc R Soc B 264:1579–1586

    Article  PubMed Central  Google Scholar 

  6. Andersen SL (2003) Trajectories of brain development: point of vulnerability or window of opportunity? Neurosci Biobehav Rev 27:3–18

    Article  PubMed  Google Scholar 

  7. Andersson MB (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  8. Ashworth CJ, Antipatis C (2001) Micronutrient programming of development throughout gestation. Reproduction 122:527–535

    CAS  Article  PubMed  Google Scholar 

  9. Badás E, Martínez J et al (2015) Ageing and reproduction: antioxidant supplementation alleviates telomere loss in wild birds. J Evol Biol 28:896–905

    Article  PubMed  Google Scholar 

  10. Balzer AL, Williams TD (1998) Do female zebra finches vary primary reproductive effort in relation to mate attractiveness? Behaviour 135:297–309

    Article  Google Scholar 

  11. Bennett AT, Cuthill IC et al (1996) Ultraviolet vision and mate choice in zebra finches. Nature 380:433–435

    CAS  Article  Google Scholar 

  12. Blount JD, Metcalfe NB et al (2003) Neonatal nutrition, adult antioxidant defences and sexual attractiveness in the zebra finch. Proc R Soc B 270:1691–1696

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. Bolund E, Schielzeth H et al (2009) Compensatory investment in zebra finches: females lay larger eggs when paired to sexually unattractive males. Proc R Soc B 276:707–715

    Article  PubMed  Google Scholar 

  14. Bonaparte KM, Riffle-Yokoi C et al (2011) Getting a head start: diet, sub-adult growth, and associative learning in a seed-eating passerine. PLoS One 6:e23775

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. Boogert NJ, Giraldeau L-A et al (2008) Song complexity correlates with learning ability in zebra finch males. Anim Behav 76:1735–1741

    Article  Google Scholar 

  16. Buchanan KL, Leitner S et al (2004) Developmental stress selectively affects the song control nucleus HVC in the zebra finch. Proc R Soc B 271:2381–2386

    Article  PubMed  PubMed Central  Google Scholar 

  17. Buchanan KL, Spencer K et al (2003) Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris). Proc R Soc B 270:1149–1156

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Burley N (1986) Sexual selection for aesthetic traits in species with biparental care. Am Nat 127:415–445

    Article  Google Scholar 

  19. Burley N (1988) The differential-allocation hypothesis: an experimental test. Am Nat 132:611–628

    Article  Google Scholar 

  20. Burley N, Coopersmith CB (1987) Bill color preferences of zebra finches. Ethology 76:133–151

    Article  Google Scholar 

  21. Candolin U, Salesto T (2009) Does competition allow male mate choosiness in threespine sticklebacks? Am Nat 173:273–277

    Article  PubMed  Google Scholar 

  22. Cate CT, Mug G (1984) The development of mate choice in zebra finch females. Behaviour 90:125–150

    Article  Google Scholar 

  23. Christians JK (2002) Avian egg size: variation within species and inflexibility within individuals. Biol Rev 77:1–26

    Article  PubMed  Google Scholar 

  24. Clayton NS (1990) Assortative mating in zebra finch subspecies, Taeniopygia guttata guttata and T. g. castanotis. Philos Trans R Soc B 330:351–370

    Article  Google Scholar 

  25. Clutton-Brock TH (1984) Reproductive effort and terminal investment in iteroparous animals. Am Nat 123:212–229

    Article  Google Scholar 

  26. Collins SA, Hubbard C, Houtman, AM (1994) Female mate choice in the zebra finch ? the effect of male beak colour and male song. Behav Ecol Sociobiol 35:21-25

  27. Crino OL, Prather CT et al (2014) Developmental stress increases reproductive success in male zebra finches. Proc R Soc B 281:20141266

    Article  PubMed  PubMed Central  Google Scholar 

  28. Edward DA, Chapman T (2011) The evolution and significance of male mate choice. Trends Ecol Evol 26:647–654

    Article  PubMed  Google Scholar 

  29. Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223

    CAS  Article  PubMed  Google Scholar 

  30. Gil D, Naguib M et al (2006) Early condition, song learning, and the volume of song brain nuclei in the zebra finch (Taeniopygia guttata). J Neurobiol 66:1602–1612

    Article  PubMed  Google Scholar 

  31. Gowaty PA (2008) Reproductive compensation. J Evol Biol 21:1189–1200

    Article  PubMed  Google Scholar 

  32. Gowaty PA, Anderson WW et al (2007) The hypothesis of reproductive compensation and its assumptions about mate preferences and offspring viability. Proc Natl Acad Sci U S A 104:15023–15027

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. Griggio M, Hoi H (2010) Only females in poor condition display a clear preference and prefer males with an average badge. BMC Evol Biol 10:261

    PubMed  PubMed Central  Google Scholar 

  34. Harris WE, Uller T (2009) Reproductive investment when mate quality varies: differential allocation versus reproductive compensation. Phil Trans R Soc B 364:1039–1048

    Article  PubMed  PubMed Central  Google Scholar 

  35. Heidinger BJ, Blount JD et al (2012) Telomere length in early life predicts lifespan. Proc Natl Acad Sci U S A 109:1743–1748

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Hill GE (1993) Male mate choice and the evolution of female plumage coloration in the house finch. Evolution 47:1515–1525

    Article  PubMed  Google Scholar 

  37. Holveck M-J, de Castro ACV et al (2008) Accuracy of song syntax learning and singing consistency signal early condition in zebra finches. Behav Ecol 19:1267–1281

    Article  Google Scholar 

  38. Holveck M-J, Geberzahn N et al (2011) An experimental test of condition-dependent male and female mate choice in zebra finches. PLoS One 6:e23974

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. Holveck M-J, Riebel K (2010) Low-quality females prefer low-quality males when choosing a mate. Proc R Soc B 277:153–160

    Article  PubMed  Google Scholar 

  40. Jennions MD, Petrie M (1997) Variation in mate choice and mating preferences: a review of causes and consequences. Biol Rev 72:283–327

    CAS  Article  PubMed  Google Scholar 

  41. Kokko H, Härdling R (2005) The evolution of prudent choice. Evol Ecol Res 7:697–715

    Google Scholar 

  42. Lande R (1980) Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34:292–305

    Article  PubMed  Google Scholar 

  43. Laubu C, Schweitzer C et al (2017) Mate choice based on behavioural type: do convict cichlids prefer similar partners? Anim Behav 126:281–291

    Article  Google Scholar 

  44. Liu R, Liu IY et al (2003) Reversal of age-related learning deficits and brain oxidative stress in mice with superoxide dismutase/catalase mimetics. Proc Natl Acad Sci U S A 100:8526–8531

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. Lucas A, Morley R et al (2001) Nutrition and mental development. Nutrition Rev 59:S24–S33

    CAS  Article  Google Scholar 

  46. Magurran AE, Seghers BH (1990) Risk sensitive courtship in the guppy (Poecilia reticulata). Behaviour 112:194–201

    Article  Google Scholar 

  47. Mahmoud KZ, Edens F et al (2004) Ascorbic acid decreases heat shock protein 70 and plasma corticosterone response in broilers (Gallus gallus domesticus) subjected to cyclic heat stress. Comp Biochem Phys B 137:35–42

    Article  Google Scholar 

  48. Mautz BS, Jennions MD (2011) The effect of competitor presence and relative competitive ability on male mate choice. Behav Ecol 22:769–775

    Article  Google Scholar 

  49. Metcalfe NB, Alonso-Alvarez C (2010) Oxidative stress as a life-history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Funct Ecol 24:984–996

    Article  Google Scholar 

  50. Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260

    Article  PubMed  Google Scholar 

  51. Monaghan P, Metcalfe NB et al (1996) Male finches selectively pair with fecund females. Proc R Soc B 263:1183–1186

    Article  Google Scholar 

  52. Mougeot F, Martinez-Padilla J et al (2007) Carotenoid-based colouration and ultraviolet reflectance of the sexual ornaments of grouse. Behav Ecol Sociobiol 61:741–751

    Article  Google Scholar 

  53. Noguera JC, Kim SY et al (2012) Pre-fledgling oxidative damage predicts recruitment in a long-lived bird. Biol Lett 8:61–63

    CAS  Article  PubMed  Google Scholar 

  54. Noguera JC, Metcalfe NB et al (2015a) Sex-dependent effects of nutrition on telomere dynamics in zebra finches (Taeniopygia guttata). Biol Lett 11:20140938

    Article  PubMed  PubMed Central  Google Scholar 

  55. Noguera JC (2017) Interacting effects of early dietary conditions and reproductive effort on the oxidative costs of reproduction. PeerJ 5:e3094

    Article  PubMed  PubMed Central  Google Scholar 

  56. Noguera JC, Metcalfe NB et al (2015b) Are you what you eat? Micronutritional deficiencies during development influence adult personality-related traits. Anim Behav 101:129–140

    Article  Google Scholar 

  57. Nordeen KW, Nordeen EJ (1992) Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches. Behav Neural Biol 57:58–66

    CAS  Article  PubMed  Google Scholar 

  58. Nowicki S, Searcy W et al (2002) Brain development, song learning and mate choice in birds: a review and experimental test of the “nutritional stress hypothesis”. J Comp Phys A 188:1003–1014

    CAS  Article  Google Scholar 

  59. Parker G (1983) Mate quality and mating decisions. In: Bateson P (ed) Mate choice. Cambridge University Press, Cambridge, pp 141–166

    Google Scholar 

  60. Pianka ER, Parker WS (1975) Age-specific reproductive tactics. Am Nat:453–464

  61. Reichert S, Stier A et al (2014) Increased brood size leads to persistent eroded telomeres. Front Ecol Evol 22:2–9

    Google Scholar 

  62. Riebel K (2009) Song and female mate choice in zebra finches: a review. Adv Study Behav 40:197–238

    Article  Google Scholar 

  63. Rutstein AN, Brazill-Boast J et al (2007) Evaluating mate choice in the zebra finch. Anim Behav 74:1277–1284

    Article  Google Scholar 

  64. Saino N, Caprioli M et al (2011) Antioxidant defenses predict long-term survival in a passerine bird. PLoS One 6:e19593

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  65. Sheldon BC (2000) Differential allocation: tests, mechanisms and implications. Trends Ecol Evol 15:397–402

    CAS  Article  PubMed  Google Scholar 

  66. Spencer K, Buchanan K et al (2003) Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata). Horm Behav 44:132–139

    CAS  Article  PubMed  Google Scholar 

  67. Spencer K, Buchanan K et al (2004) Developmental stress, social rank and song complexity in the European starling (Sturnus vulgaris). Proc R Soc B 271:S121–S123

    Article  PubMed  PubMed Central  Google Scholar 

  68. Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  69. Surai PF (2002) Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, Nottingham

    Google Scholar 

  70. Surai PF (2006) Selenium in nutrition and health. Nottingham University Press, Nottingham

    Google Scholar 

  71. Tchernichovski O, Nottebohm F et al (2000) A procedure for an automated measurement of song similarity. Anim Behav 59:1167–1176

    CAS  Article  PubMed  Google Scholar 

  72. Trivers R (1972) Parental investment and sexual selection. In: Campbell BG (ed) Sexual selection & the descent of man. Aldine de Gruyter, New York, pp 136–179

    Google Scholar 

  73. Whittingham MJ, Stephens PA et al (2006) Why do we still use stepwise modelling in ecology and behaviour? J Anim Ecol 75:1182–1189

    Article  PubMed  Google Scholar 

  74. Williams TD (2012) Physiological adaptations for breeding in birds. Princeton University Press, Princeton

    Google Scholar 

  75. Zann RA, Bamford M (1996) The zebra finch: a synthesis of field and laboratory studies. Oxford University Press, Oxford

    Google Scholar 

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Acknowledgements

We thank the animal care staff for their support and P. Surai for his advice with the micronutrient treatment. We also thank S. Cowan and L. Glen for their help during the experiment, R. Bassar and S. Auer for the constructive comments on the statistical analyses, and K. Buchanan and D. Gil for their advice with the song recordings. We also thank three anonymous referees for their comments which greatly improved the manuscript.

Funding

JCN was supported by AXA Research fellowship (PDOC-2013-W1) and later on by a Juan de la Cierva Fellowship (IJCI-2014-20246), NBM by ERC Advanced Grant (322784), and PM by ERC Advanced Grant (268926).

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JCN, NBM, and PM conceived and designed the experiments. JCN performed the experiments and analyzed the data. JCN, NBM, and PM wrote the manuscript.

Corresponding author

Correspondence to José C. Noguera.

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The study was carried out with the permission of UK Home Office and all tests were subjected to local ethical review (Project License No. 60/4109).

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The authors declare that they have no competing interests.

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Communicated by: Sven Thatje

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Noguera, J.C., Metcalfe, N.B. & Monaghan, P. Postnatal nutrition influences male attractiveness and promotes plasticity in male mating preferences. Sci Nat 104, 102 (2017). https://doi.org/10.1007/s00114-017-1524-y

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Keywords

  • Differential allocation
  • Fertility
  • Mate choice
  • Song
  • Taeniopygia guttata