Philosophical Transactions of the Royal Society B: Biological Sciences
Restricted access

Adaptive specialization, conditional plasticity and phylogenetic history in the reproductive cue response systems of birds

and
Scott A MacDougall-Shackleton

Scott A MacDougall-Shackleton

University of Western Ontario1151 Richmond Street, Suite 2, London, Ontario, Canada N6A 5B8

Google Scholar

Find this author on PubMed

Published:https://doi.org/10.1098/rstb.2007.2139

    Appropriately timed integration of breeding into avian annual cycles is critical to both reproductive success and survival. The mechanisms by which birds regulate timing of breeding depend on environmental cue response systems that regulate both when birds do and do not breed. Despite there being multiple possible explanations for birds' abilities to time breeding appropriately in different environments, and for the distribution of different cue response system characteristics among taxa, many studies infer that adaptive specialization of cue response systems has occurred without explicitly considering the alternatives. In this paper, we make explicit three hypotheses concerning the timing of reproduction and distribution of cue response characteristics among taxa: adaptive specialization; conditional plasticity; and phylogenetic history. We emphasize in particular that although conditional plasticity built into avian cue response systems (e.g. differing rates of gonadal development and differing latencies until onset of photorefractoriness) may lead to maladaptive annual cycles in some novel circumstances, this plasticity also can lead to what appear to be adaptively specialized cue response systems if not viewed in a comparative context. We use a comparative approach to account for the distribution of one important feature of avian reproductive cue response systems, photorefractoriness. Analysis of the distribution within songbirds of one criterion for absolute photorefractoriness, the spontaneous regression of the gonads without any decline in photoperiod, reveals that a failure to display this trait probably represents an adaptive specialization to facilitate a flexible reproductive schedule. More finely resolved analysis of both criteria for absolute photorefractoriness (the second being total lack of a reproductive response even to constant light after gonadal regression has occurred) within the cardueline finches not only provides further confirmation of this interpretation, but also indicates that these two criteria for photorefractoriness can be, and have been, uncoupled in some taxa. We suggest that careful comparative studies at different phylogenetic scales will be extremely valuable for distinguishing between adaptive specialization and non-adaptive explanations, such as phylogenetic history as explanations of cue response traits in particular taxa. We also suggest that particular focus on taxa in which individuals may breed on very different photoperiods (latitudes or times of year) in different years should be particularly valuable in identifying the range of environmental conditions across which conditionally plastic cue responses can be adaptive.

    References

    • Adkisson C.S Red crossbill (Loxia curvirostra). The birds of North America , Poole A& Gill F vol. 256 1996pp. 1–24. Eds. Philadelphia, PA; Washington, DC:The Academy of Natural Sciences; The American Ornithologists'Union. Google Scholar
    • Arnaiz-Villena A, Guillen J, Ruiz-del-Valle V, Lowy E, Zamora J, Varela P, Stefani D& Allende L.M . 2001 Phylogeography of crossbills, bullfinches, grosbeaks, and rosefinches. Cell. Mol. Life Sci. 58, 1159–1166.doi:10.1007/PL00000930. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Badyaev A.V . 1997 Avian life history variation along altitudinal gradients: an example with cardueline finches. Oecologia. 111, 365–374.doi:10.1007/s004420050247. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Baker J.R The evolution of breeding seasons. Evolution: essays on aspects of evolutionary biology & DeBeer G.B . 1938pp. 161–177. Eds. Oxford, UK:Clarendon Press. Google Scholar
    • Ball G.F . 1993 The neural integration of environmental information by seasonally breeding birds. Am. Zool. 33, 185–199. CrossrefGoogle Scholar
    • Ball G.F& Hahn T.P GnRH neuronal systems in birds and their relation to the control of seasonal reproduction. GnRH Neurons: gene to behavior , Parhar I.S& Sakuma Y . 1997pp. 325–342. Eds. Tokyo, Japan:Brain Shuppan Publishers. Google Scholar
    • Beebe K, Bentley G.E& Hau M . 2005 A seasonally breeding tropical bird lacks absolute photorefractoriness in the wild, despite high photoperiodic sensitivity. Funct. Ecol. 19, 505–512.doi:10.1111/j.1365-2435.2005.00994.x. . Crossref, Web of ScienceGoogle Scholar
    • Benkman C.W . 1990 Foraging rates and the timing of crossbill reproduction. Auk. 107, 376–386. Crossref, Web of ScienceGoogle Scholar
    • Benkman C.W White-winged crossbill (Loxia leucoptera). The birds of North America , Poole A, Stettenheim P& Gill F vol. 27 1992pp. 1–20. Eds. Philadelphia, PA; Washington, DC:The Academy of Natural Sciences; The American Ornithologists'Union. Google Scholar
    • Bentley G.E, Wingfield J.C, Morton M.L& Ball G.F . 2000 Stimulatory effects on the reproductive axis in female songbirds by conspecific and heterospecific male song. Horm. Behav. 37, 179–189.doi:10.1006/hbeh.2000.1573. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Bentley G.E, Audage N.C, Hanspal E.K, Ball G.F& Hans T.P . 2003 Photoperiodic response of the hypothalamo–pituitary–gonad axis in male and female canaries, Serinus canaria. J. Exp. Zool. A. 296, 143–151.doi:10.1002/jez.a.10245. . CrossrefGoogle Scholar
    • Burger J.W . 1947 On the relation of day length to the phases of testicular involution and inactivity of the spermatogenetic cycle of the starling. J. Exp. Zool. 105, 259–268.doi:10.1002/jez.1401050207. . Crossref, PubMedGoogle Scholar
    • Chakravorty K& Chandola-Saklani A . 1985 Termination of seasonal breeding in a weaver finch, Ploceus philippinus: role of photoperiod. J. Exp. Zool. 235, 381–386.doi:10.1002/jez.1402350309. . CrossrefGoogle Scholar
    • Chandola A& Chakravorty K . 1982 Termination of seasonal breeding in the photoperiodic weaver bird. J. Exp. Zool. 222, 169–172.doi:10.1002/jez.1402220208. . CrossrefGoogle Scholar
    • Chandola-Saklani A, Thapliyal A, Negi K, Diyundi S.C& Choudhary B . 2004 Daily increments of light hours near vernal equinox synchronize circannual testicular cycle of tropical spotted munia. Chronobiol. Int. 21, 553–569.doi:10.1081/CBI-200025991. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Chaturvedi C.M& Thapliyal J.P . 1983 Thyroid photoperiod and gonadal regression in the common myna Acridotheres tristis. Gen. Comp. Endocrinol. 52, 279–282.doi:10.1016/0016-6480(83)90123-5. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Cockrem J.F . 1995 Timing of seasonal breeding in birds, with particular reference to New Zealand birds. Reprod. Fertil. Dev. 7, 1–19.doi:10.1071/RD9950001. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Coombs-Hahn, T. P. 1993 Integration of environmental cues to time reproduction in an opportunistic breeder, the red crossbill (Loxia curvirostra). PhD dissertation, University of Washington, Seattle. Google Scholar
    • Coppack T& Both C . 2002 Predicting life-cycle adaptation of migratory birds to global climate change. Ardea. 90, 369–378. Crossref, Web of ScienceGoogle Scholar
    • Coppack T& Pulido F . 2004 Photoperiodic response and the adaptability of avian life cycles to environmental change. Adv. Ecol. Res. 35, 131–150. Crossref, Web of ScienceGoogle Scholar
    • Coppack T, Pulido F& Berthold P . 2001 Photoperiodic response to early hatching in a migratory bird species. Oecologia. 128, 181–186.doi:10.1007/s004420100652. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Coppack T, Pulido F, Szisch M, Auer D.P& Berthold P . 2003 Photoperiodic response may facilitate adaptation to climatic change in long-distance migratory birds. Proc. R. Soc. B. 270, S43–S46.doi:10.1098/rsbl.2003.0005. . Link, Web of ScienceGoogle Scholar
    • Damsté P.H . 1947 Experimental modification of the sexual cycle of the greenfinch. J. Exp. Biol. 24, 20–35. Crossref, PubMed, Web of ScienceGoogle Scholar
    • Dawson A . 1991 Photoperiodic control of testicular regression and moult in male house sparrows Passer domesticus. Ibis. 133, 312–316. Crossref, Web of ScienceGoogle Scholar
    • Dawson W.R Pine siskin (Carduelis pinus). The birds of North America , Poole A& Gill F vol. 280 1997pp. 1–24. Eds. Philadelphia, PA; Washington, DC:The Academy of Natural Sciences; The American Ornithologists' Union. Google Scholar
    • Dawson A, King V.M, Bentley G.E& Ball G.F . 2001 Photoperiodic control of seasonality in birds. J. Biol. Rhythm. 16, 366–381.doi:10.1177/074873001129002079. . Crossref, Web of ScienceGoogle Scholar
    • Drent R.H& Daan S . 1980 The prudent parent: energetic adjustments in avian breeding. Ardea. 68, 225–252. Web of ScienceGoogle Scholar
    • Dolnik V.R . 1975 Fotoperiodicheskii kontrol sezonnykh tsiklov vesa tela, linki i polovoi aktivnosti u zyablikov (Fringilla coelebs). Zool. Zhur. 54, 1048–1056. Google Scholar
    • Dolnik V.R Migratsionnoe Sostioyanie Ptits. 1976a Nauka, Moscow:Izdatelstvo. Google Scholar
    • Dolnik V.R Fotoperiodizm y ptits. Fotoperiodizm Zhivotnykh I Rastenii & Zaslavskii V.A . 1976bpp. 47–81. Eds. Leningrad, Russia:Akademiya Nauk SSSR. Google Scholar
    • Donham R.S& Wilson F.E . 1970 Photorefractoriness in pinealectomized Harris' sparrows. Condor. 72, 101–102.doi:10.2307/1366482. . CrossrefGoogle Scholar
    • Engels W.L The influence of different daylengths on the tests of a transequatorial migrant, the bobolink (Dolichonyx oryzivorus). Photoperiodism and related phenomena in plants and animals & Withrow R . 1959pp. 759–766. Eds. Washington, DC:American Association for the Advancement of Science Publication No. 55. Google Scholar
    • Engels W.L . 1962 Day-length and termination of photorefractoriness in the annual testicular cycle of the transequatorial migrant Dolichonyx (the bobolink). Biol. Bull. 123, 94–104.doi:10.2307/1539506. . Crossref, Web of ScienceGoogle Scholar
    • Erpino M.J . 1969 Seasonal cycle of reproductive physiology in the black-billed magpie. Condor. 71, 267–279.doi:10.2307/1366303. . Crossref, Web of ScienceGoogle Scholar
    • Farner D.S& Follett B.K Reproductive periodicity in birds. Hormones and evolution & Barrington E.J.W . 1979pp. 829–872. Eds. New York, NY:Academic Press. Google Scholar
    • Farner D.S& Gwinner E Photoperiodicity, circannual and reproductive cycles. Avian endocrinology , Epple A& Stetson M.H . 1980pp. 331–366. Eds. New York, NY:Academic Press. Google Scholar
    • Farner D.S& Mewaldt L.R . 1955 The natural termination of the refractory period in the white-crowned sparrow. Condor. 57, 112–116.doi:10.2307/1364552. . CrossrefGoogle Scholar
    • Farner D.S& Serventy D.L . 1960 The timing of reproduction in birds in the arid regions of Australia. Anat. Rec. 137, 354. Google Scholar
    • Farner D.S& Wilson A.C . 1957 A quantitative examination of testicular growth in the white-crowned sparrow. Biol. Bull. 113, 254–267.doi:10.2307/1539083. . Crossref, Web of ScienceGoogle Scholar
    • Farner D.S, Moore R.S& Donham M.C . 1981 Induction of testicular development in house sparrows, Passer domesticus, and white-crowned sparrows, Zonotrichia leucophrys gambelii, with very long days and continuous light. Physiol. Zool. 54, 372–378. CrossrefGoogle Scholar
    • Farner D.S, Donham R.S, Matt K.S, Mattocks P.W, Moore M.C& Wingfield J.C The nature of photorefractoriness. Avian endocrinology: environmental and ecological perspectives , Mikami S.I, Homma K& Wada M . 1983pp. 149–156. Eds. Tokyo, Japan; Berlin, Germany:Japan Scientific Society Press; Springer. Google Scholar
    • Felsenstein J . 1985 Phylogenies and the comparative method. Am. Nat. 125, 1–15.doi:10.1086/284325. . Crossref, Web of ScienceGoogle Scholar
    • Follett B.K Marshall's physiology of reproduction. Birds & Lamming G.E vol. 1 1984pp. 283–350. Eds. Edinburgh, UK:Longman Green. Google Scholar
    • Follett B.K& Nicholls T.J . 1984 Photorefractoriness in Japanese quail: possible involvement of the thyroid gland. J. Exp. Zool. 232, 573–580.doi:10.1002/jez.1402320325. . Crossref, PubMedGoogle Scholar
    • Fretwell S.D Populations in a seasonal environment. 1972 Princeton, NJ:Princeton University Press. Google Scholar
    • Groth J.G . 1993 Evolutionary differentiation in morphology, vocalizations, and allozymes among nomadic sibling species in the North American red crossbill (Loxia curvirostra) complex. Univ. Calif. Publ. Zool. 127, 1–143. Google Scholar
    • Gwinner E& Dittami J Photoperiodic responses in temperate zone and equatorial stonechats: a contribution to the problem of photoperiodism in tropical organisms. The endocrine system and the environment , Gollett B.K, Ishii S& Chandola A . 1985pp. 279–294. Eds. Tokyo, Japan; Berlin, Germany:Japan Science Society Press; Springer. Google Scholar
    • 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, 66–70.doi:10.1007/BF00379321. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Gwinner E, Dittam J& Beldhuis H.J.A . 1988 The seasonal development of photoperiodic responsiveness in an equatorial migrant, the garden warbler Sylvia borin. J. Comp. Physiol. A. 162, 389–396.doi:10.1007/BF00606125. . Crossref, Web of ScienceGoogle Scholar
    • Hahn T.P . 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, 213–226.doi:10.1002/jez.1402720306. . CrossrefGoogle Scholar
    • Hahn T.P Cassin's Finch. (Carpodacus cassinii). The Birds of North America , Poole A& Gill F vol. 240 1996pp. 1–20. Eds. Philadelphia, PA; Washington, DC:The Academy of Natural Sciences; The American Ornithologists' Union. Google Scholar
    • Hahn T.P . 1998 Reproductive seasonality in an opportunistic breeder, the red crossbill, Loxia curvirostra. Ecology. 79, 2365–2375. Crossref, Web of ScienceGoogle Scholar
    • Hahn T.P& Ball G.F . 1995 Changes in brain GnRH associated with photorefractoriness in house sparrows (Passer domesticus). Gen. Comp. Endocrinol. 99, 349–363.doi:10.1006/gcen.1995.1119. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Hahn T.P, Swingle J, Wingfield J.C& Ramenofsky M . 1992 Adjustments of the prebasic molt schedule in birds. Ornis Scand. 23, 314–321.doi:10.2307/3676655. . CrossrefGoogle Scholar
    • Hahn T.P, Boswell T, Wingfield J.C& Ball G.F . 1997 Temporal flexibility in avian reproduction: patterns and mechanisms. Curr. Ornithol. 14, 39–80. CrossrefGoogle Scholar
    • Hahn T.P, Pereyra M.E, Sharbaugh S.M& Bentley G.E . 2004 Physiological responses to photoperiod in three cardueline finch species. Gen. Comp. Endocrinol. 137, 99–108.doi:10.1016/j.ygcen.2004.02.014. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Hahn T.P, Katti M, Pereyra M.E, Ward G& MacDougall-Shackleton S.A Effects of food availability on the reproductive system. Functional avian endocrinology , Dawson A& Sharp P.J . 2005pp. 167–180. Eds. New Delhi, India:Narosa Publishing House. Google Scholar
    • Hamner W.M . 1966 Photoperiodic control of the annual testicular cycle in the house finch Carpodacus mexicanus. Gen. Comp. Endocrinol. 7, 224–233.doi:10.1016/0016-6480(66)90043-8. . Crossref, Web of ScienceGoogle Scholar
    • Hamner W.M . 1968 The photorefractory period of the house finch. Ecology. 49, 211–227.doi:10.2307/1934450. . Crossref, Web of ScienceGoogle Scholar
    • Harris M.O& Turek F.W . 1982 Photoperiodic control of the timing of testicular regression in white-throated sparrows. Gen. Comp. Endocrinol. 46, 124–129.doi:10.1016/0016-6480(82)90172-1. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Harvey P.H& Pagel M.D The comparative method in evolutionary biology. 1991 Oxford, UK; New York, NY:Oxford University Press. Google Scholar
    • Hau M . 2001 Timing of breeding in variable environments: tropical birds as model systems. Horm. Behav. 40, 281–290.doi:10.1006/hbeh.2001.1673. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Hau M, Wikelski M& Wingfield J.C . 1998 A neotropical forest bird can measure the slight changes in tropical photoperiod. Proc. R. Soc. B. 265, 89–95.doi:10.1098/rspb.1998.0268. . Link, Web of ScienceGoogle Scholar
    • Hau M, Wikelski M& Wingfield J.C . 2000 Visual and nutritional food cues fine-tune timing of reproduction in a neotropical rainforest bird. J. Exp. Zool. 286, 494–504.doi:10.1002/(SICI)1097-010X(20000401)286:5<494::AID-JEZ7>3.0.CO;2-3. . Crossref, PubMedGoogle Scholar
    • Helm B& Gwinner E . 1999 Timing of postjuvenal molt in African (Saxicola torquata axillaris) and European (Saxicola torquata rubicola) stonechats: effects of genetic and environmental factors. Auk. 116, 589–603. Crossref, Web of ScienceGoogle Scholar
    • Helm B& Gwinner E . 2005 Carry-over effects of day length during spring migration. J. Ornithol. 146, 348–354.doi:10.1007/s10336-005-0009-5. . Crossref, Web of ScienceGoogle Scholar
    • Helm B, Gwinner E& Trost L . 2005 Flexible seasonal timing and migratory behavior. Ann. NY Acad. Sci. 1046, 216–227.doi:10.1196/annals.1343.019. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Hinde R.A& Steel E . 1976 The effect of male song on an estrogen-dependent behavior pattern in the female canary (Serinus canarius). Horm. Behav. 7, 293–304.doi:10.1016/0018-506X(76)90035-0. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Hinde R.A& Steel E The influence of daylength and male vocalizations on the estrogen-dependent behavior of female canaries and budgerigars, with discussion of data from other species. Advances in the study of behavior , Rosenblatt R.S, Hinde R, Beer C& Busnel M.-C vol. 8 1978pp. 39–73. Eds. New York, NY:Academic Press. Google Scholar
    • Huey R.B& Hertz P.E . 1984 Is a jack-of-all-temperatures a master of none?. Evolution. 38, 441–444.doi:10.2307/2408502. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Humphrey P& Parkes K . 1959 An approach to the study of molts and plumages. Auk. 76, 1–31. CrossrefGoogle Scholar
    • Jones P.J& Ward P . 1976 The level of reserve protein as the proximate factor controlling the timing of breeding and clutch size in the red-billed quelea, Quelea quelea. Ibis. 118, 547–574. Crossref, Web of ScienceGoogle Scholar
    • Ketterson E.D& Nolan V . 1999 Adaptation, exaptation and constraint: a hormonal perspective. Am. Nat. 154, Suppl., S4–S25.doi:10.1086/303280. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Komdeur J& Daan S . 2005 Breeding in the monsoon: semi-annual reproduction in the Seychelles warbler (Acrocephalus sechellensis). J. Ornithol. 146, 305–313.doi:10.1007/s10336-005-0008-6. . Crossref, Web of ScienceGoogle Scholar
    • Kumar B.S& Kumar V . 1993 Photoperiodic control of annual reproductive cycles in subtropical Brahminy myna, Sturnus pagodarum. Gen. Comp. Endocrinol. 89, 149–160.doi:10.1006/gcen.1993.1018. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Kumar V& Tewary P.D . 1982 Photoperiodic testicular response and photorefractoriness in common Indian rosefinch. Environ. Control Biol. 20, 39–42. CrossrefGoogle Scholar
    • Lambrechts M.M& Perret P . 2000 A long photoperiod overrides non-photoperiodic factors in blue tits' timing of reproduction. Proc. R. Soc. B. 267, 585–588.doi:10.1098/rspb.2000.1041. . Link, Web of ScienceGoogle Scholar
    • Lambrechts M.M, Perret P& Blondel J . 1996 Adaptive differences in the timing of egg laying between different populations of birds result from variation in photoresponsiveness. Proc. R. Soc. B. 263, 19–22.doi:10.1098/rspb.1996.0004. . Link, Web of ScienceGoogle Scholar
    • Lambrechts M.M, 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, 5153–5155.doi:10.1073/pnas.94.10.5153. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Leitner S, Van't Hof T.J& Gahr M . 2003 Flexible reproduction in wild canaries is independent of photoperiod. Gen. Comp. Endocrinol. 130, 102–108.doi:10.1016/S0016-6480(02)00574-9. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Lewis R.A, King J.R& Farner S . 1974 Photoperiodic responses of a subtropical population of the finch (Zonotrichia capensis hypoleuca). Condor. 76, 233–237.doi:10.2307/1366336. . Crossref, Web of ScienceGoogle Scholar
    • Ligon J.D . 1974 Green cones of the pinon pine stimulate late summer breeding in the pinon jay. Nature. 250, 80–82.doi:10.1038/250080a0. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Lofts B . 1962 Photoperiodism and the refractory period of reproduction in an equatorial bird Quelea quelea. Ibis. 104, 407–414. CrossrefGoogle Scholar
    • Lofts B . 1964 Evidence of an autonomous reproductive rhythm in an equatorial bird (Quelea quelea). Nature. 201, 523–534.doi:10.1038/201523b0. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Lofts B& Murton R.K . 1968 Photoperiodic and physiological adaptations regulating avian breeding cycles and their ecological significance. J. Zool. 155, 327–394. Crossref, Web of ScienceGoogle Scholar
    • MacDougall-Shackleton S.A, Johnson R.E& Hahn T.P Gray-crowned rosy-finch (Leucosticte tephrocotis). The birds of North America , Poole A& Gill F vol. 559 2000 Philadelphia, PA:The Birds of North America, Inc. Google Scholar
    • MacDougall-Shackleton S.A, Deviche P.J, Crain R.D, Ball G.F& Hahn T.P . 2001 Seasonal changes in brain GnRH immunoreactivity and song-control nuclei volumes in an opportunistically breeding songbird. Brain Behav. Evol. 58, 38–48.doi:10.1159/000047260. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • MacDougall-Shackleton S.A, Pereyra M.E, Katti M& Hahn T.P GnRH, photorefractoriness, and breeding schedules of cardueline finches. Functional avian endocrinology , Dawson A& Sharp P.J . 2005pp. 97–110. Eds. New Delhi, India:Narosa Publishing House. Google Scholar
    • Marsh R.H, MacDougall-Shackleton S.A& Hahn T.P . 2002 Photorefractoriness and neural response to day length in American goldfinches, Carduelis tristis. Can. J. Zool. 80, 2100–2107.doi:10.1139/z02-208. . Crossref, Web of ScienceGoogle Scholar
    • Marshall A.J . 1959 Internal and environmental control of breeding. Ibis. 101, 456–478. CrossrefGoogle Scholar
    • Marshall A.J Environmental factors other than light involved in the control of sexual cycles in birds and mammals. La photregulation de la reproduction chez les oiseaux et les mammiferes , Benoit J& Assenmacher I . 1970pp. 53–64. Eds. Paris, France:Editions du Centre National de la Recherche Scientifique. Google Scholar
    • Marshall A.J& Coombs C.J.F . 1957 The interaction of environmental, internal and behavioural factors in the rook Corvus frugilegus Linnaeus. Proc. Zool. Soc. London. 128, 545–589. CrossrefGoogle Scholar
    • Marshall A.J& Disney H.J.de.S . 1956 Photostimulation of an equatorial bird (Quelea quelea Linneaus). Nature. 177, 143–144.doi:10.1038/177143a0. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Marshall A.J& Disney H.J. de. S . 1957 Experimental induction of the breeding season in a xerophilous bird. Nature. 180, 647–649.doi:10.1038/180647a0. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Marten J.A& Johnson N.K . 1986 Genetic relationships of North American cardueline finches. Condor. 88, 409–420.doi:10.2307/1368266. . Crossref, Web of ScienceGoogle Scholar
    • McNamara J.M, Welham R.K, Houston A.I, Daan S& Tinbergen J.M . 2004 The effects of background mortality on optimal reproduction in a seasonal environment. Theor. Popul. Biol. 65, 361–372.doi:10.1016/j.tpb.2003.10.006. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Misra M, Rani S, Singh S& Kumar V . 2004 Regulation of seasonality in the migratory male blackheaded bunting (Emberiza melanocephala). Reprod. Nutr. Dev. 44, 341–352.doi:10.1051/rnd:2004039. . Crossref, PubMedGoogle Scholar
    • Monroe B.L& Sibley C.G A world checklist of birds. 1993 New Haven, CT:Yale University Press. Google Scholar
    • Moore M.C, Donham R.S& Farner D.S . 1982 Physiological preparation for autumnal migration in white-crowned sparrows. Condor. 84, 410–419.doi:10.2307/1367445. . Crossref, Web of ScienceGoogle Scholar
    • Moore I.T, Wada H, Perfito N, Busch D.S, Hahn T.P& Wingfield J.C . 2004 Territoriality and testosterone in an equatorial population of rufous-collared sparrows, Zonotrichia capensis. Anim. Behav. 67, 411–420.doi:10.1016/j.anbehav.2003.03.021. . Crossref, Web of ScienceGoogle Scholar
    • Morton M.L, Pereyra M.E& Baptista L.F . 1985 Photoperiodically induced ovarian growth in the white-crowned sparrow (Zonotrichia leucophrys gambelii) and its augmentation by song. Comp. Biochem. Physiol. A. 80, 93–97.doi:10.1016/0300-9629(85)90684-X. . Crossref, Web of ScienceGoogle Scholar
    • Newton I Finches. 1973 New York, NY:Taplinger. Google Scholar
    • Nicholls T.J, Goldsmith A.R& Dawson A . 1988 Photorefractoriness in birds and comparison with mammals. Physiol. Rev. 68, 133–176. Crossref, PubMed, Web of ScienceGoogle Scholar
    • Partecke J, Van't Hof T& Gwinner E . 2004 Differences in the timing of reproduction between urban and forest European blackbirds (Turdus merula): result of phenotypic flexibility or genetic differences?. Proc. R. Soc. B. 271, 1995–2001.doi:10.1098/rspb.2004.2821. . Link, Web of ScienceGoogle Scholar
    • Patten M.A& Fugate M . 1998 Systematic relationships among the emberizid sparrows. Auk. 115, 412–424. Crossref, Web of ScienceGoogle Scholar
    • Pereyra M.E, Sharbaugh S.M& Hahn T.P . 2005 Interspecific variation in photo-induced GnRH plasticity among nomadic cardueline finches. Brain Behav. Evol. 66, 35–49.doi:10.1159/000085046. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Perfito N, Bentley G& Hau M . 2006 Tonic activation of brain GnRH immunoreactivity despite reduction of peripheral reproductive parameters in opportunistically breeding zebra finches. Brain Behav. Evol. 67, 123–134.doi:10.1159/000090977. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Perrins C.M . 1970 The timing of birds' breeding seasons. Ibis. 112, 242–255. Crossref, Web of ScienceGoogle Scholar
    • Phillmore L.S, Hoshooley J.S, Hahn T.P& MacDougall-Shackleton S.A . 2005 A test of absolute photorefractoriness and photo-induced neural plasticity of song control regions in black-capped chickadees (Poecile atricapillus). Can. J. Zool. 83, 747–753.doi:10.1139/z05-070. . Crossref, Web of ScienceGoogle Scholar
    • Rani S, Singh S& Kumar V The pineal clock affects behavioral circadian rhythms but not photoperiodic induction in the Indian weaver bird (Ploceus philippinus). J. Ornithol. 146, 2005a 355–364.doi:10.1007/s10336-005-0005-9. . Crossref, Web of ScienceGoogle Scholar
    • Rani S, Singh S, Misra M, Malik S, Singh B.P& Kumar V Daily light regulates seasonal responses in the migratory male redheaded bunting (Emberiza bruniceps). J. Exp. Zool. A. 303, 2005b 541–550.doi:10.1002/jez.a.187. . CrossrefGoogle Scholar
    • Robinson J.E& Follett B.K . 1982 Photoperiodism in Japanese quail: the termination of seasonal breeding by photorefractoriness. Proc. R. Soc. B. 215, 95–116.doi:10.1098/rspb.1982.0030. . Link, Web of ScienceGoogle Scholar
    • Rowan W . 1925 Relation of light to bird migration and developmental changes. Nature. 115, 494–495. CrossrefGoogle Scholar
    • Rowan W . 1926 On photoperiodism, reproductive periodicity and the annual migrations of birds and certain fishes. Proc. Boston Soc. Nat. Hist. 38, 147–189. Google Scholar
    • Runfeldt S& Wingfield J.C . 1985 Experimentally prolonged sexual activity in female song sparrows delays termination of reproductive activity in their untreated mates. Anim. Behav. 33, 403–410.doi:10.1016/S0003-3472(85)80064-6. . Crossref, Web of ScienceGoogle Scholar
    • Schoech, S. J. & Hahn, T. P. Submitted. Latitude affects degree of advancement in laying by birds in response to food supplementation: a meta-analysis. Google Scholar
    • Schwab R.G& Lott D.F . 1969 Testis growth and regression in starlings (Sturnus vulgaris) as a function of the presence of females. J. Exp. Zool. 171, 39–42.doi:10.1002/jez.1401710106. . CrossrefGoogle Scholar
    • Sharp P.J . 1996 Strategies in avian breeding cycles. Anim. Reprod. Sci. 42, 505–513.doi:10.1016/0378-4320(96)01556-4. . Crossref, Web of ScienceGoogle Scholar
    • Sibley C.G& Ahlquist J.E Phylogeny and classification of birds: a study in molecular evolution. 1990 New Haven, CT:Yale University Press. Google Scholar
    • Sibley C.G& Monroe B.L Distribution and taxonomy of birds of the world. 1990 New Haven, CT; London, UK:Yale University Press. Google Scholar
    • Silverin B . 1995 Reproductive adaptations to breeding in the North. Am. Zool. 35, 191–202. CrossrefGoogle Scholar
    • Silverin G& Viebke P.A . 1994 Low temperatures affect the photoperiodically induced LH and testicular cycles differently in closely related species of tits (Parus spp.). Horm. Behav. 28, 199–206.doi:10.1006/hbeh.1994.1017. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Silverin B, Viebke P.A& Westin J . 1989 An artificial simulation of the vernal increase in day length and its effects on the reproductive system in three species of tits (Parus spp.), and modifying effects of environmental factors. Condor. 91, 598–608.doi:10.2307/1368110. . Crossref, Web of ScienceGoogle Scholar
    • Silverin B, Massa R& Stokkan K.A . 1993 Photoperiodic adaptation to breeding at different latitudes in great tits. Gen. Comp. Endocrinol. 90, 14–22.doi:10.1006/gcen.1993.1055. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Sossinka R . 1974 Der Einfluss von Dursteperioden auf die Schilddrusse- und Gonaden-aktvitat und ihre Bedeuten fur die Brutperiodik des Zebrafinken (Taeniopygia castanotis Gould). J. Ornithol. 115, 128–141.doi:10.1007/BF01643286. . CrossrefGoogle Scholar
    • Stearns S.C The evolution of life histories. 1992 Oxford, UK:Oxford University Press. Google Scholar
    • Storey C.R& Nicholls T.J . 1976 Some effects of manipulation of daily photoperiod on rate of onset of a photorefractory state in canaries (Serinus canarius). Gen. Comp. Endocrinol. 30, 204–208.doi:10.1016/0016-6480(76)90101-5. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Storey C.R& Nicholls T.J . 1982 A photoperiodically induced cycle of gonadotropin secretion in intact, hemi castrated and fully castrated male bullfinches Pyrrhula pyrhhula. Ibis. 124, 55–60. Crossref, Web of ScienceGoogle Scholar
    • Styrsky J.D, Berthold P& Robinson W.D . 2004 Endogenous control of migration and calendar effects in an intratropical migrant, the yellow–green vireo. Anim. Behav. 67, 1141–1149.doi:10.1016/j.anbehav.2003.07.012. . Crossref, Web of ScienceGoogle Scholar
    • Svensson E . 1997 Natural selection on avian breeding time: causality, fecundity-dependent, and fecundity-independent selection. Evolution. 51, 1276–1283.doi:10.2307/2411056. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Tewary P.D& Dixit A.S . 1983 Photoperiodic control of the ovarian cycle in the rosefinch, Carpodacus erythrinus. J. Exp. Zool. 228, 537–542.doi:10.1002/jez.1402280313. . CrossrefGoogle Scholar
    • Tewary P.D& Kumar V . 1982 VPhotoperiodic responses of a subtropical migratory finch, the black-headed bunting (Emberiza melanocephala). Condor. 84, 168–171.doi:10.2307/1367661. . Crossref, Web of ScienceGoogle Scholar
    • Tewary P.D& Tripathi P.M . 1985 Circadian photoperiodicity in termination of photorefractoriness in the yellow-throated sparrow. Experientia. 41, 135–1351.doi:10.1007/BF01952090. . CrossrefGoogle Scholar
    • Tewary P.D, Kumar V& Prasad B.N . 1983 Influence of photoperiod in a subtropical migratory finch, the common Indian rosefinch Carpodacus erythrinus. Ibis. 125, 115–120. Crossref, Web of ScienceGoogle Scholar
    • Thapliyal J.P& Saxena R.N . 1964 Absence of a refractory period in the common weaver bird. Condor. 66, 199–208.doi:10.2307/1365644. . CrossrefGoogle Scholar
    • Tordoff H.B& Dawson W.R . 1965 The influence of daylength on reproductive timing in the red crossbill. Condor. 67, 416–422.doi:10.2307/1365634. . CrossrefGoogle Scholar
    • van Noordwijk A.J The methods of genetical ecology applied to the study of evolutionary change. Population biology: ecological and evolutionary viewpoints , Wohrmann K& Jain S.K . 1990pp. 291–319. Eds. Berlin, Germany:Springer. CrossrefGoogle Scholar
    • Vaugien L . 1952 Sur le comportement sexual singulaier de la Peruch ondulee, maintenue a l'obscurite. Comp. Acad. Sci. 234, 1489. Google Scholar
    • Vaugien L . 1953 Sur l'apparition de la maturite sexuelle des jeunes perruches ondulees males soumises a diverses conditions d'eclairement: Le developpement testiculaire est plus rapide dans l'obscurite complete. Bull. Biol. 87, 274–286. Google Scholar
    • Verhulst S& Nilsson J.-Å . 2008 The timing of birds' breeding seasons: a review of experiments that manipulated timing of breeding. Phil. Trans. R. Soc. B. 363, 399–410.doi:10.1098/rstb.2007.2146. . Link, Web of ScienceGoogle Scholar
    • Visser M.E& Lambrechts M.M . 1999 Information constraints in the timing of reproduction in temperate zone birds: great and blue tits. Proc. Int. Ornithol. Cong. 22, 249–264. Google Scholar
    • Visser M.E, van Noordwijk A.J, Tinbergen J.M& Lessells C.M . 1998 Warmer springs lead to mis-timed reproduction in great tits (Parus major). Proc. R. Soc. B. 265, 1867–1870.doi:10.1098/rspb.1998.0514. . Link, Web of ScienceGoogle Scholar
    • Visser M.E, Both C& Lambrechts M.M . 2004 Global climate change leads to mistimed avian reproduction. Adv. Ecol. Res. 35, 89–110. Crossref, Web of ScienceGoogle Scholar
    • Wilson F.E& Donham R.S Daylength and control of seasonal reproduction in male birds. Processing of environmental information in vertebrates & Stetson M.H . 1988pp. 101–120. Eds. Berlin, Germany:Springer. CrossrefGoogle Scholar
    • Wilson F.E& Follett B.K . 1974 Plasma and pituitary luteinizing hormone in intact and castrated tree sparrows (Spizella arborea) during a photoinduced gonadal cycle. Gen. Comp. Endocrinol. 23, 82–93.doi:10.1016/0016-6480(74)90056-2. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Wingfield J.C Fine temporal adjustments of reproductive function. Avian endocrinology , Epple A& Stetson M.H . 1980pp. 367–389. Eds. New York, NY:Academic Press. Google Scholar
    • Wingfield J.C Environmental and endocrine control of reproduction: an ecological approach. Avian endocrinology: environmental and ecological perspectives , Mikami S.I, Homma K& Wada M . 1983pp. 265–288. Eds. Tokyo, Japan; Berlin, Germany:Japan Scientific Society Press; Springer. Google Scholar
    • Wingfield J.C . 1993 Control of testicular cycles in the song sparrow, Melospiza melodia melodia: interaction of photoperiod and an endogenous program?. Gen. Comp. Endocrinol. 92, 388–401.doi:10.1006/gcen.1993.1176. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Wingfield J.C& Farner D.S . 1993 Endocrinology of reproduction in wild species. Avian Biol. 9, 163–327. Google Scholar
    • Wingfield J.C, Hahn T.P, Levin R.N& Honey P . 1992 Environmental predictability and control of gonadal cycles in birds. J. Exp. Zool. 261, 214–231.doi:10.1002/jez.1402610212. . CrossrefGoogle Scholar
    • Wingfield J.C, Hahn T.P& Doak D Integration of environmental factors regulating transitions of physiological state, morphology and behaviour. Avian endocrinology & Sharp P . 1993pp. 111–122. Eds. Bristol, UK:Journal of Endocrinology Ltd. Google Scholar
    • Wingfield J.C, Hahn T.P, Wada M, Astheimer L.B& Schoech S . 1996 Interrelationship of daylength and temperature in the control of gonadal development, body mass and fat depots in white-crowned sparrows, Zonotrichia leucophrys gambelii. Gen. Comp. Endocrinol. 101, 242–255.doi:10.1006/gcen.1996.0027. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Wingfield J.C, Hahn T.P, Wada M& Schoech S . 1997 Effects of day length and temperature on gonadal development, body mass and fat depots in white-crowned sparrows, Zonotrichia leucophrys pugetensis. Gen. Comp. Endocrinol. 107, 44–62.doi:10.1006/gcen.1997.6894. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Wingfield J.C, Hahn T.P, Maney D.L, Schoech S, Wada M& Morton M.L . 2003 Effects of temperature on photoperiodically-induced reproductive development, circulating plasma luteinizing hormone and thyroid hormones, body mass, fat deposition and molt in mountain white-crowned sparrows, Zonotrichia leucophrys oriantha. Gen. Comp. Endocrinol. 131, 143–158.doi:10.1016/S0016-6480(02)00648-2. . Crossref, PubMed, Web of ScienceGoogle Scholar
    • Wolfson A . 1952 The occurrence and regulation of the refractory period in the gonadal and fat cycles of the junco. J. Exp. Zool. 121, 311–326.doi:10.1002/jez.1401210204. . CrossrefGoogle Scholar
    • Wolfson A The role of light and darkness in the regulation of spring migration and reproductive cycles in birds. Photoperiodism & Withrow R.B . 1959pp. 679–716. Eds. Washington, DC:American Association for the Advancement of Science Publication 55. Google Scholar
    • Zink R.M . 1982 Patterns of genic and morphologic variation among sparrows in the genera Zonotrichia, Melospiza, Junco and Passerella. Auk. 99, 632–649. Web of ScienceGoogle Scholar
    • Zink R.M& Blackwell R.C . 1996 Patterns of allozyme, mitochondrial DNA, and morphometric variation in four sparrow genera. Auk. 113, 59–67. Crossref, Web of ScienceGoogle Scholar
    • Zink R.M, Dittman D.L& Rootes W.L . 1991 Mitochondrial DNA variation and the phylogeny of Zonotrichia. Auk. 108, 578–584. Crossref, Web of ScienceGoogle Scholar