Advertisement

Journal of Ornithology

, 148:219 | Cite as

Adaptation and evolution of photoperiod response systems in birds

  • Scott A. MacDougall-ShackletonEmail author
  • Thomas P. Hahn
Review

Abstract

The reproductive cycle of most birds is driven by the annual change in photoperiod, with birds cycling between the physiological states of photosensitivity, photostimulation and photorefractoriness. Comparative studies show that variation in breeding schedules is often correlated with variation in photoperiod response systems. We caution, however, that before adaptive specialization of photoperiod response systems can be concluded, the effects of conditional plasticity and phylogenetic history need to be considered. Conditional plasticity can result in birds with identical response systems displaying different breeding schedules at different latitudes. Consideration of phylogeny can reveal whether parameters of response systems are derived adaptations or ancestral traits. Comparative data on photorefractoriness suggests that one criterion for absolute photorefractoriness—spontaneous regression of the gonads on constant long days—is ancestral in the songbirds. Only four species lack this form of photorefractoriness and all of them are opportunistic breeders. A second criterion for absolute photorefractoriness is insensitivity to even 24 h light when birds are refractory. In contrast to spontaneous regression of the gonads, the distribution of this second criterion across species does not support an adaptive hypothesis. In cardueline finches, a lack of photorefractoriness by this second criterion is widespread and is present even among strictly seasonal breeders. Further exploration of the evolution and adaptation of photoperiod responses will require measuring the response of each species to a range of photoperiods and interpreting results within a phylogenetic context.

Keywords

Photoperiodism Reproduction Seasonality 

Notes

Acknowledgments

Our research programs have been supported by NSF (USA) and NSERC (Canada).

References

  1. Ball GF, Balthazart J (2003) Birds return every spring like clockwork, but where is the clock? Endocrinol 144:3739–3741CrossRefGoogle Scholar
  2. Both C, Visser ME (2001) Adjustment to climate change is constrained by arrival date in a long-distance migrant bird. Nature 411:296–298PubMedCrossRefGoogle Scholar
  3. Chakravorty K, Chandola-Saklani A (1985) Termination of seasonal breeding in a weaver finch, Ploceus philippinus: role of photoperiod. J Exp Zool 235:381–386CrossRefGoogle Scholar
  4. Chandola A, Chakravorty K (1982) Termination of seasonal breeding in the photoperiodic weaver bird. J Exp Zool 222:169–172CrossRefGoogle Scholar
  5. Coppack T, Pulido F, Czisch M, Auer DP, Berthold P (2003) Photoperiodic response may facilitate adaptation to climatic change in long-distance migratory birds. Proc R Soc Lond B 270 (Suppl 1):S43–S46CrossRefGoogle Scholar
  6. Coppack T (2007) Experimental determination of the photoperiodic basis for geographic variation in avian seasonality. J Ornith (this issue)Google Scholar
  7. Dawson A (1991) Photoperiodic control of testicular regression and moult in male house sparrows Passer domesticus. Ibis 133:312–316CrossRefGoogle Scholar
  8. Dawson A (2007) Seasonality in a temperate zone bird can be entrained by near equatorial photoperiods. Proc R Soc Lond B 274:721–725CrossRefGoogle Scholar
  9. Dawson A, Goldsmith AR (1983) Plasma prolactin and gonadotrophins during gonadal development and the onset of photorefractoriness in male and female starlings (Sturnus vulgaris) on artificial photoperiods. J Endocrinol 97:253–260PubMedGoogle Scholar
  10. Dawson A, King VM, Bentley GE, Ball GF (2001) Photoperiodic control of seasonality in birds. J Biol Rhythms 16:366–381CrossRefGoogle Scholar
  11. Farner DS, Donham RS, Matt KS, Mattocks PW Jr, Moore MC, Wingfield JC (1983) The nature of photorefractoriness. In: Mikami SI, Homma K, Wada M (eds) Avian Endocrinology: environmental and ecological perspectives. Japan Scientific Society/Springer Tokyo Berlin Heidelberg, pp 149–156Google Scholar
  12. Goodson JL, Saldanha CJ, Hahn TP, Soma KK (2005) Recent advances in behavioral neuroendocrinology: insights from studies on birds. Horm Behav 48:461–473PubMedCrossRefGoogle Scholar
  13. Gwinner E, Dittami J, Gwinner H (1983) Postjuvenile molt in East African and Central European stonechats (Saxicola torquata axillaris, S. t. rubicola) and its modification by photoperiod. Oecologia 60:66–70CrossRefGoogle Scholar
  14. Hahn TP (1995) Integration of photoperiodic and food cues to time changes in reproductive physiology by an opportunistic breeder, the red crossbill, Loxia curvirostra (Aves: Carduelinae). J Exp Zool 272:213–226CrossRefGoogle Scholar
  15. Hahn TP (1998) Reproductive seasonality in an opportunistic breeder, the Red Crossbill, Loxia curvirostra. Ecology 79:2365–2375Google Scholar
  16. Hahn TP, MacDougall-Shackleton SA (2007) Adaptive specialization, conditional plasticity, and phylogenetic history in the reproductive cue response systems of birds. Phil Trans R Soc Lond B (in press)Google Scholar
  17. Hahn TP, Boswell T, Wingfield JC, Ball GF (1997) Temporal flexibility in avian reproduction: patterns and mechanisms. Curr Ornithol 14:39–80Google Scholar
  18. Hamner WM (1968) The photorefractory period of the house finch. Ecology 49:211–227CrossRefGoogle Scholar
  19. Hau M (2001) Timing of breeding in variable environments: tropical birds as model systems. Horm Behav 40:281–290PubMedCrossRefGoogle Scholar
  20. Hau M, Wikelski M, Wingfield JC (1998) A neotropical forest bird can measure the slight changes in tropical photoperiod. Proc R Soc Lond B 265:89–95CrossRefGoogle Scholar
  21. Hau M, Wikelski M, Wingfield JC (2000) Visual and nutritional food cues fine-tune timing of reproduction in a neotropical rainforest bird. J Exp Zool 286:494–504PubMedCrossRefGoogle Scholar
  22. Lambrects MM, Blondel J, Maistre M, Perret P (1997) A single response mechanism is responsible for evolutionary adaptive variation in a bird’s laying date. Proc Natl Acad Sci USA 94:5153–5155CrossRefGoogle Scholar
  23. Lofts B, Murton RK (1968) Photoperiodic and physiological adaptations regulating avian breeding cycles and their ecological significance. J Zool 155:327–394CrossRefGoogle Scholar
  24. MacDougall-Shackleton SA, Pereyra ME, Katti M, Hahn TP (2005) GnRH, photorefractoriness, and breeding schedules of cardueline finches. In: Dawson A, Sharp PJ (eds) Functional avian endocrinology. Narosa, New Delhi, pp 97–110Google Scholar
  25. MacDougall-Shackleton S, Katti M, Hahn TP (2006) Tests of absolute photorefractoriness in four species of carduelines finch that differ in reproductive schedule. J Exp Biol 209:3786–3794PubMedCrossRefGoogle Scholar
  26. Meddle SL, Follett BK (1997) Photoperiodically driven changes in Fos expression within the basal tuberal hypothalamus and median eminence of Japanese quail. J Neurosci 17:8909–8919PubMedGoogle Scholar
  27. Nicholls TJ, Goldsmith AR, Dawson A (1988) Photorefractoriness in birds and comparison with mammals. Phys Rev 68:133–176Google Scholar
  28. Robinson JE, Follett BK (1982) Photoperiodism in Japanese quail: the termination of seasonal breeding by photorefractoriness. Proc R Soc Lond B 215:95–116PubMedCrossRefGoogle Scholar
  29. Rowan W (1925) Relation of light to bird migration and developmental changes. Nature 115:494–495CrossRefGoogle Scholar
  30. Rowan W (1926) On photoperiodism, reproductive periodicity and the annual migrations of birds and certain fishes. Proc Boston Soc Nat Hist 38:147–189Google Scholar
  31. Rowan W (1929) Experiments in bird migration. I. Manipulation of the reproductive cycle: seasonal histological changes in the gonads. Proc Boston Soc Nat Hist 39:115–208Google Scholar
  32. Saldanha CJ, Leak RK, Silver R (1994) Detection and transduction of daylength in birds. Psychoneuroendocrinol 19:641–656CrossRefGoogle Scholar
  33. Schoech SJ, Hahn TP (2007) Food supplementation and timing of reproduction: does the responsiveness to supplementary information vary with latitude? J Ornith (this issue).  doi:10.1007/s10336-007-0177-6
  34. Sharp PJ, Follett BK (1969) The effect of hypothalamic lesions on gonadotrophin release in Japanese quail (Coturnix coturnix japonica). Neuroendocrinol 5:205–218CrossRefGoogle Scholar
  35. Silverin B, Massa R, Stokkan KA (1993) Photoperiodic adaptation to breeding at different latitudes in great tits. Gen Comp Endocrinol 90:14–22PubMedCrossRefGoogle Scholar
  36. Visser ME, van Noordwijk AJ, Tinbergen JM, Lessells CM (1998) Warmer springs lead to mis-timed reproduction in great tits (Parus major). Proc R Soc Lond B 265:1867–1870CrossRefGoogle Scholar
  37. Visser ME, Both C, Lambrechts MM (2004) Global climate change leads to mistimed avian reproduction. Adv Ecol Res 35:89–110CrossRefGoogle Scholar
  38. Wingfield JC (1983) Environmental and endocrine control of reproduction: an ecological approach. In: Mikami SI, Homma K, Wada M (eds) Avian endocrinology: environmental and ecological perspectives. Japan Scientific Society/Springer, Tokyo Berlin Heidelberg, pp 265–288Google Scholar
  39. Wolfson A (1959) The role of light and darkness in the regulation of spring migration and reproductive cycles in birds. In: Withrow RB (ed) Photoperiodism. American Association for the Advancement of Science Publication 55, Washington pp 679–716Google Scholar
  40. Yasuo S, Watanabe M, Okabayashi N, Ebihara S, Yoshimura T (2003) Circadian clock genes and photoperiodism: comprehensive analysis of clock gene expression in the medial basal hypothalamus, the suprachiasmatic nucleus, and the pineal gland of Japanes quail under various light schedules. Endocrinol 144:3742–3748CrossRefGoogle Scholar
  41. Yoshimura T, Yasuo S, Watanabe M, Iigo M, Yamamura T, Hirunagi K, Ebihara S (2003) Light-induced hormone conversion of T4 to T3 regulates photoperiod response of gonads in birds. Nature 426:178–181Google Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2007

Authors and Affiliations

  • Scott A. MacDougall-Shackleton
    • 1
    Email author
  • Thomas P. Hahn
    • 2
  1. 1.Department of PsychologyUniversity of Western OntarioLondonCanada
  2. 2.Section of Neurobiology, Physiology and BehaviorUniversity of California-DavisDavisUSA

Personalised recommendations