Volume 13 Issue 1
Mar.  2022
Turn off MathJax
Article Contents
Xudong Li, Wenyu Xu, Jiangping Yu, Wutong Zhang, Haitao Wang. 2022: Plasma levels of luteinizing hormone and prolactin in relation to double brooding in Great Tit (Parus major). Avian Research, 13(1): 100017. doi: 10.1016/j.avrs.2022.100017
Citation: Xudong Li, Wenyu Xu, Jiangping Yu, Wutong Zhang, Haitao Wang. 2022: Plasma levels of luteinizing hormone and prolactin in relation to double brooding in Great Tit (Parus major). Avian Research, 13(1): 100017. doi: 10.1016/j.avrs.2022.100017

Plasma levels of luteinizing hormone and prolactin in relation to double brooding in Great Tit (Parus major)

doi: 10.1016/j.avrs.2022.100017
More Information
  • The reproductive behaviors of birds are mainly controlled by the hypothalamus-pituitary-gonad axis. Many studies have shown that reproductive hormones are tightly linked to the breeding sub-stages. However, only a few studies have examined the temporal trend of hormone levels among different reproductive stages in multiple brooded species. We investigated the changes in plasma luteinizing hormone (LH) and prolactin (PRL) concentrations during different reproductive stages of the facultative double-brooded Great Tit (Parus major). We found that the concentrations of LH and PRL in females were significantly higher than those in males. Females had significantly higher LH and lower PRL concentrations in the pre-breeding period than in the first/second brooding periods, and there were no significant changes between the first and second brooding periods. The concentrations of LH and PRL in males had no significant difference between the pre-breeding period and the first brooding periods, while LH and PRL concentrations in the second brooding period were significantly higher than those in the first brooding period. We conclude that there are sex-based differences between LH and PRL at different stages of reproduction. The changes in LH and PRL in both males and females should be related to their physiological functions. Especially for males, individuals with higher levels of LH and PRL are more likely to maintain second clutches.

     

  • loading
  • Ahola, M.P., Laaksonen, T., Eeva, T., Lehikoinen, E., 2007. Climate change can alter competitive relationships between resident and migratory birds. J. Anim. Ecol. 76, 1045-1052 doi: 10.1111/j.1365-2656.2007.01294.x
    Angelier, F., Chastel, O., 2009. Stress, prolactin and parental investment in birds: A review. Gen. Comp. Endocrinol. 163, 142-148 doi: 10.1016/j.ygcen.2009.03.028
    Angelier, F., Shaffer, S.A., Weimerskirch, H., Chastel, O., 2006. Effect of age, breeding experience and senescence on corticosterone and prolactin levels in a long-lived seabird: The wandering albatross. Gen. Comp. Endocrinol. 149, 1-9 doi: 10.1016/j.ygcen.2006.04.006
    Angelier, F., Weimerskirch, H., Dano, S., Chastel, O., 2007. Age, experience and reproductive performance in a long-lived bird: A hormonal perspective. Behav. Ecol. Sociobiol. 61, 611-621 doi: 10.1007/s00265-006-0290-1
    Ball, G.F., Ketterson, E.D., 2008. Sex differences in the response to environmental cues regulating seasonal reproduction in birds. Philos. T. R. Soc. B. 363, 231-246 doi: 10.1098/rstb.2007.2137
    Basso, A., Richner, H., 2015. Effects of nest predation risk on female incubation behavior and offspring growth in great tits. Behav Ecol Sociobiol. 69, 977-989 doi: 10.1007/s00265-015-1910-4
    Buntin, J.D., Hnasko, R.M., Zuzick, P.H., Valentine, D.L., Scammell, J.G., 1996. Changes in bioactive prolactin-like activity in the plasma and its relationship to incubation behavior in breeding ring doves. Gen. Comp. Endocrinol. 102, 221-232 doi: 10.1006/gcen.1996.0063
    Caro, S.P., Lambrechts, M.M., Chastel, O., Sharp, P.J., Thomas, D.W., Balthazart, J., 2006. Simultaneous pituitary-gonadal recrudescence in two Corsican populations of male blue tits with asynchronous breeding dates. Horm. Behav. 50, 347-360 doi: 10.1016/j.yhbeh.2006.03.001
    Carro, M.E., Mermoz, M.E., Fernandez, G.J., 2015. Factors affecting the probability of double brooding by Southern House Wrens. J. Field Ornithol. 85, 227-236
    Cate, C.T., Lea, R.W., Ballintijn, M.R., Sharp, P.J., 1993. Brood size affects behavior, interclutch interval, LH levels, and weight in ring dove (Streptopelia risoria) breeding pairs. Horm. Behav. 27, 539-550 doi: 10.1006/hbeh.1993.1039
    Chastel, O., Barbraud, C., Weimerskirch, H., Lormee, H., Lacroix, A., Tostain, O., 2005. High levels of LH and testosterone in a tropical seabird with an elaborate courtship display. Gen. Comp. Endocrinol. 140, 33-40 doi: 10.1016/j.ygcen.2004.10.012
    Christensen, D., Vleck, C.M., 2008. Prolactin release and response to vasoactive intestinal peptide in an opportunistic breeder, the zebra finch (Taeniopygia guttata). Gen. Comp. Endocrinol. 157, 91-98 doi: 10.1016/j.ygcen.2008.04.013
    Dawson, A., 2008. Control of the annual cycle in birds: Endocrine constraints and plasticity in response to ecological variability. Philos. T. R. Soc. B. 363, 1621-1633 doi: 10.1098/rstb.2007.0004
    Dawson, A., Goldsmith, A.R., 1984. Effects of gonadectomy on seasonal changes in plasma LH and prolactin concentrations in male and female starlings (Sturnus vulgaris). J. Endocrinol. 100, 213-218 doi: 10.1677/joe.0.1000213
    Dawson, A., Goldsmith, A.R., 1985. Modulation of gonadotropin and prolactin secretion by daylength and breeding behavior in free-living starlings, Sturnus vulgaris. Zoology 206, 241-252 doi: 10.1111/j.1469-7998.1985.tb05648.x
    Dawson, A., Sharp, P.J., 2010. Seasonal changes in concentrations of plasma LH and prolactin associated with the advance in the development of photo refractoriness and molt by high temperature in the starling. Gen. Comp. Endocrinol. 167, 122-127 doi: 10.1016/j.ygcen.2010.02.004
    Dittami, J.P., 1981. Seasonal changes in the behavior and plasma titres of various hormones in barheaded geese, (Anser indicus). Z. Tierpsychol. 55, 289-324
    El Halawani, M.E., Fehrer, S., Hargis, B.M., Porter, T.E., 1988. Incubation behavior in the domestic turkey: physiological correlates. CRC Crit. Rev. Poult. Biol. 1, 285-314
    Fan, Q., Mingju, E., Wei, Y., Sun, W., Wang, H., 2021. Mate choice in double-breeding female great tits (Parus major): Good males or compatible males. Animals 11, 1-17
    Gao, L., Gao, J., Zhang, S. 2018. Temperature effect on luteinizing hormone secretion of Eurasian Skylark (Alauda arvensis) and Great Tit (Parus major) in China. Avian Res.; 9, 3 doi: 10.1186/s40657-018-0095-8
    Goldsmith, A.R., Burke, S., Prosser, J.M., 1984. Inverse changes in plasma prolactin and LH concentrations in female canaries after disruption and reinitiation of incubation. J. Endocrinol. 103, 251-256 doi: 10.1677/joe.0.1030251
    Goldsmith, A.R., Williams, D.M., 1980. Incubation in mallards (Anas platyrhynchos): changes in plasma levels of prolactin and luteinizing hormone. J. Endocrinol. 86:371-379 doi: 10.1677/joe.0.0860371
    Goldsmith, A.R., 1982. Plasma concentrations of prolactin during incubation and parental feeding throughout repeated breeding cycles in canaries (Serinus canarius). J. Endocrinol. 94, 51-59 doi: 10.1677/joe.0.0940051
    Gratto-Trevor, C.L., Oring, L.W., Fivizzani, A.J., El Halawani, M.E., Cooke, F., 1990. The role of prolactin in parental care in a monogamous and a polyandrous shorebird. Auk 107, 718-729 doi: 10.2307/4088002
    Greives, T.J., Fudickar, A.M., Atwell, J.W., Meddle, S.L., Ketterson, E.D., 2016. Early spring sex differences in luteinizing hormone response to gonadotropin releasing hormone in co-occurring resident and migrant dark-eyed juncos (Junco hyemalis). Gen. Comp. Endocrinol. 236, 17-23 doi: 10.1016/j.ygcen.2016.06.031
    Griffiths, R., Double, M.C., Orr, K., Dawson, R.J., 1998. A DNA test to sex most birds. Mol. Ecol. 7, 1071-1075 doi: 10.1046/j.1365-294x.1998.00389.x
    Hiatt, E.S., Goldsmith, A.R., Farner, D.S., 1987. Plasma levels of prolactin and gonadotropins during the reproductive cycle of White-Crowned Sparrows (Zonotrichia leucophrys). Auk 104, 208-217 doi: 10.1093/auk/104.2.208
    Hissa, R., Saarela, S., Balthazart, J., Etches, R.J., 1983. Annual variation in the concentrations of circulating hormones in Capercaillie (Tetrao urogallus). Gen. Comp. Endocrinol. 51, 183-190 doi: 10.1016/0016-6480(83)90071-0
    Hoffmann, J., Postma, E., Schaub, M., 2015. Factors influencing double brooding in Eurasian Hoopoes Upupa epops. Ibis 157, 17-30 doi: 10.1111/ibi.12188
    Husby, A., Kruuk, L.E.B., Visser, M.E., 2009. Decline in the frequency and benefits of multiple brooding in great tits as a consequence of a changing environment. Proc. R. Soc. B. 276, 1845-1854 doi: 10.1098/rspb.2008.1937
    Krause, J.S., Meddle, S.L., Wingfield, J.C., 2015. The effects of acute restraint stress on plasma levels of prolactin and corticosterone across life-history stages in a short-lived bird: Gambel’s white-crowned sparrow (Zonotrichia leucophrys gambelii). Physiol. Biochem. Zool. 88, 589-598 doi: 10.1086/683321
    Li, D., Hao, Y., Liu, X., Yao, Y., Du, C., Zhang, X., et al., 2015. Changes in phytohaemagglutinin skin-swelling responses during the breeding season in a multi-brooded species, the eurasian tree sparrow: do males with higher testosterone levels show stronger immune responses? J Ornithol. 156, 133-141 doi: 10.1007/s10336-014-1104-2
    Li, M., Sun, Y., Wu, J., Zhang, X., Li, J., Yao, Y., et al. 2016. Variation in corticosterone response and corticosteroid binding-globulin during different breeding sub-stages in Eurasian tree sparrow (Passer montanus). J. Exp. Zool. Part A. 325, 75-83 doi: 10.1002/jez.1998
    Lormee, H., Jouventin, P., Lacroix, A., Lallemand, J., Chastel, O., 2000. Reproductive endocrinology of tropical seabirds: Sex-specific patterns in LH, steroids, and prolactin secretion in relation to parental care. Gen. Comp. Endocrinol. 117, 413-426 doi: 10.1006/gcen.1999.7434
    Matysiokova, B., Remes, V., 2010. Incubation feeding and nest attentiveness in a socially monogamous songbird: Role of feather colouration, territory quality and ambient environment. Ethology 116, 596-607
    Monroe, A.P., Hallinger, K.K., Brasso, R.L., Cristol, D.A., 2008. Occurrence and implications of double brooding in a southern population of tree swallows. Condor 110, 382-386 doi: 10.1525/cond.2008.8341
    Nagy, L.R., Holmes, R.T., 2005b. To double-brood or not? individual variation in the reproductive effort in black-throated blue warblers (Dendroica caerulescens). Auk 122, 902-914 doi: 10.1093/auk/122.3.902
    Oring, L.W., Fivizzani, A.J., Colwell, M.A., El Halawani, M.E., 1988. Hormonal changes associated with natural and manipulated incubation in the sex-role reversed Wilson’s phalarope. Gen. Comp. Endocrinol. 72, 247-256 doi: 10.1016/0016-6480(88)90207-9
    Ouyang, J.Q., Sharp, P., Quetting, M., Hau, M., 2013. Endocrine phenotype, reproductive success and survival in the great tit, Parus major. J. Evolution. Biol. 26, 1988-1998 doi: 10.1111/jeb.12202
    Ouyang, J.Q., Sharp, P.J., Dawson, A., Quetting, M., Hau, M., 2011. Hormone levels predict individual differences in reproductive success in a passerine bird. Proc. Royal Soc. B. 278, 2537-2545 doi: 10.1098/rspb.2010.2490
    Pawson, A.J., McNeilly, A.S., 2005. The pituitary effects of GnRH. Anim Reprod Sci. 88, 75-94 doi: 10.1016/j.anireprosci.2005.05.010
    Riechert, J., Chastel, O., Becker, P.H., 2012. Why do experienced birds reproduce better? Possible endocrine mechanisms in a long-lived seabird, the common tern. Gen. Comp. Endocrinol. 178, 391-399 doi: 10.1016/j.ygcen.2012.06.022
    Riechert, J., Becker, P.H., Chastel, O., 2014. Predicting reproductive success from hormone concentrations in the common tern (Sterna hirundo) while considering food abundance. Oecologia 176, 715-727 doi: 10.1007/s00442-014-3040-5
    Ryan, C.P., Dawson, A., Sharp, P.J., Meddle, S.L., Williams, T.D., 2014. Circulating breeding and pre-breeding prolactin and LH are not associated with clutch size in the zebra finch (Taeniopygia guttata). Gen. Comp. Endocrinol. 202, 26-34 doi: 10.1016/j.ygcen.2014.04.006
    Schaper, S.V., Dawson, A., Sharp, P.J., Caro, S.P., Visser, M.E., 2012. Individual variation in avian reproductive physiology does not reliably predict variation in laying date. Gen. Comp. Endocrinol. 179, 53-62 doi: 10.1016/j.ygcen.2012.07.021
    Schaper, S.V., Rueda, C., Sharp, P.J., Dawson, A., Visser, M.E., 2011. Spring phenology does not affect timing of reproduction in the great tit (Parus major). J. Exp. Biol. 214, 3664-3671 doi: 10.1242/jeb.059543
    Sharp, P.J., Dawson, A., Lea, R.W., 1998. Control of luteinizing hormone and prolactin secretion in birds. Comp. Biochem. Phys. C. 119, 275-282
    Sharp, P.J., Macnamee, M.C., Sterling, R.J., Lea, R.W., Pedersen, H.C., 1988. Relationships between prolactin, LH and broody behavior in bantam hens. J. Endocrinol. 118, 279-286 doi: 10.1677/joe.0.1180279
    Sharp, P.J., Massa, R., Bottoni, L., Lucini, V., Lea, R.W., Dunn, I.C., Trocchi, V., 1986. Photoperiodic and endocrine control of seasonal breeding in Grey Partridge (Perdix perdix). Zool. London. 209, 187-200 doi: 10.1111/j.1469-7998.1986.tb03575.x
    Silver, R., Goldsmith, A.R., Follett, B.K., 1980. Plasma luteinizing hormone in male ring doves during the breeding cycle. Gen. Comp. Endocrinol. 42, 19-24 doi: 10.1016/0016-6480(80)90252-X
    Silverin, B., Kikuchi, M., Ishii, S., 1999. Effect of season and photoperiod on FSH in male great tits. Gen. Comp. Endocrinol. 113, 457-463 doi: 10.1006/gcen.1998.7223
    Silverin, B., Wingfield, J., Stokkan, K.A., Massa, R., Jarvinen, A., Andersson, N.A., Lambrechts, M., Sorace, A., Blomqvist, D., 2008. Ambient temperature effects on photo induced gonadal cycles and hormonal secretion patterns in Great Tits from three different breeding latitudes. Horm. Behav. 54, 60-68 doi: 10.1016/j.yhbeh.2008.01.015
    Silverin, B., 1991. Annual changes in plasma levels of LH, and prolactin in free-living female great tits (Parus major). Gen. Comp. Endocrinol. 83, 425-431 doi: 10.1016/0016-6480(91)90148-Y
    Silverin, B., 1994. Photoperiodism in male Great Tits (Parus major). Ethol. Ecol. Evol. 6, 131-157 doi: 10.1080/08927014.1994.9522990
    Smiley, K.O., Adkins-Regan, E., 2016. Prolactin is related to individual differences in parental behavior and reproductive success in a biparental passerine, the zebra finch (Taeniopygia guttata). Gen. Comp. Endocrinol. 234, 88-94 doi: 10.1016/j.ygcen.2016.03.006
    Smiley, K.O., Adkins-Regan, E., 2016. Relationship between prolactin, reproductive experience, and parental care in a biparental songbird, the zebra finch (Taeniopygia guttata). Gen. Comp. Endocrinol. 232, 17-24 doi: 10.1016/j.ygcen.2015.11.012
    Smiley, K.O., 2019. Prolactin and avian parental care: New insights and unanswered questions. Horm Behav. 111, 114-130 doi: 10.1016/j.yhbeh.2019.02.012
    Sockman, K.W., Schwabl, H., Sharp, P.J., 2000. The role of prolactin in the regulation of clutch size and onset of incubation behavior in the American kestrel. Horm. Behav. 38, 168-176 doi: 10.1006/hbeh.2000.1616
    Sockman, K.W., Sharp, P.J., Schwabl, H., 2010. Orchestration of avian reproductive effort: an integration of the ultimate and proximate bases for flexibility in clutch size, incubation behaviour, and yolk androgen deposition. Biol. Rev. Camb. Philos. Soc. 81, 629-666
    Stodola, K.W., Linder, E.T., Buehler, D.A., Franzreb, K.E., Cooper, R.J., 2009. Parental care in the multi-brooded black-throated blue warbler. Condor 111, 497-502 doi: 10.1525/cond.2009.080072
    Stokkan, K.A., Sharp, P.J., Dunn, I.C., Lea, R.W., 1988. Endocrine changes in photo stimulated Willow Ptarmigan (Lagopus lagopus lagopus) and Svalbard Ptarmigan (Lagopus mutus hyperboreus). Gen. Comp. Endocrinol. 70, 169-177 doi: 10.1016/0016-6480(88)90107-4
    Tolla, E., Stevenson, T.J., 2020. Sex differences and the neuroendocrine regulation of seasonal reproduction by supplementary environmental cues. Integr. Comp. Biol. 60, 1506-1516 doi: 10.1093/icb/icaa096
    Valle, S., Carpentier, E., Vu, B., Tsutsui, K., Deviche, P., 2015. Food restriction negatively affects multiple levels of the reproductive axis in male house finches, Haemorhous mexicanus. J. Exp. Biol. 218, 2694-2704
    Vatka, E., Orell, M., Rytkonen, S., Merila, J., 2021. Effects of ambient temperatures on evolutionary potential of reproductive timing in boreal passerines. J Anim Ecol. 90, 367-375 doi: 10.1111/1365-2656.13370
    Verboven, N., Tinbergen, J.M., Verhulst, S. 2001. Food, reproductive success and multiple breeding in the Great Tit Parus major. Ardea 89, 387-406
    Verhulst, S., Tinbergen, J.M., Daan, S., 1997. Multiple breeding in the great tit. A trade-off between successive reproductive attempts? Funct Ecol. 11, 714-722 doi: 10.1046/j.1365-2435.1997.00145.x
    Vleck, C.M., 1998. Hormonal control of incubation/brooding behavior: lessons from Wild birds. In: Proceedings of the WSPA 10 European Poultry Conference, Israel, pp. 163–169.
    Wingfield, J.C., Farner, D.S., 1993. Endocrinology of reproduction in wild species. In: Farner, D.S., King, J.R., Parkes, K.C. (Eds.), Avian Biology, IX. Academic Press, London, pp. 163–327.
    Wojczulanis-Jakubas, K., Jakubas, D., Kulpinska-Chamera, M., Chastel, O., 2018. Sex- and breeding stage-specific hormonal stress response of seabird parents. Horm. Behav. 103, 71-79 doi: 10.1016/j.yhbeh.2018.06.005
    Yu, J., E, M., Sun, W., Liang, W., Wang, H., Moeller, A.P., 2020. Differently sized cuckoos pose different threats to hosts. Curr. Zool. 66, 247-253 doi: 10.1093/cz/zoz049
    Yu, J., Lv, W., Xu, H., Bibi, N., Yu, Y., Jiang Y, et al., 2017. Function of note strings in Japanese Tit alarm calls to the Common Cuckoo: A playback experiment. Avian Res. 8: 22 doi: 10.1186/s40657-017-0080-7
    Zhang, S., Chen, X., Zhang, J., Li, H., 2014. Differences in the reproductive hormone rhythm of tree sparrows (Passer montanus) from urban and rural sites in Beijing: The effect of anthropogenic light sources. Gen. Comp. Endocrinol. 206, 24-29 doi: 10.5510/OGP20150100184
    Zhang, S., Xu, X., Wang, W., Yang, W., Liang, W., 2017a. Clock gene is associated with individual variation in the activation of reproductive endocrine and behavior of Asian short toed lark. Sci. Rep. 7, 1-8 doi: 10.1038/s41598-016-0028-x
    Zhang, S., Xu, X., Wang, W., Zhao, L., Gao, L., Yang, W., 2017b. Annual variation in the reproductive hormone and behavior rhythm in a population of the Asian short-toed lark: Can spring temperature influence activation of the HPG axis of wild birds? Horm. Behav. 95, 76-84 doi: 10.1016/j.yhbeh.2017.08.002
    Zhang, X., Yang, W., Liang, W., Wang, Y., Zhang, S., 2019. Intensity dependent disruptive effects of light at night on activation of the HPG axis of tree sparrows (Passer montanus). Environ. Pollut. 249, 904-909 doi: 10.1016/j.envpol.2019.03.008
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(1)  / Tables(4)

    Article Metrics

    Article views (91) PDF downloads(0) Cited by()
    Proportional views

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return