[en] Seasonal timing of reproduction is a key life-history trait, but we know little about the mechanisms underlying individual variation in female endocrine profiles associated with reproduction. In birds, 17b-oestradiol is a key repro- ductive hormone that links brain neuroendocrine mechanisms, involved in information processing and decision-making, to downstream mechanisms in the liver, where egg-yolk is produced. Here, we test, using a simulated induction of the reproductive system through a GnRH challenge, whether the ovary of pre-breeding female great tits responds to a brain stimulation by increasing oestradiol. We also assess how this response is modified by individual-specific traits like age, ovarian follicle size and personality, using females from lines artificially selected for divergent levels of explora- tory behaviour. We show that a GnRH injection leads to a rapid increase in circulating concentrations of oestradiol, but responses varied among individ- uals. Females with more developed ovarian follicles showed stronger responses and females from lines selected for fast exploratory behaviour showed stronger increases compared to females from the slow line, indicat- ing a heritable component. This study shows that the response of the ovary to a reproductive stimulation from the brain greatly varies among individ- uals and that this variation can be attributed to several commonly measured individual traits, which sheds light on the mechanisms shaping heritable endocrine phenotypes.
Research Center/Unit :
Giga-Neurosciences - ULiège
Disciplines :
Neurosciences & behavior
Author, co-author :
Caro, Samuel
Cornil, Charlotte ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
van Oers, Kees
Visser, Marcel
Language :
English
Title :
Personality and gonadal development as sources of individual variation in response to GnRH challenge in female great tits
Publication date :
2019
Journal title :
Proceedings of the Royal Society of London. Series B, Biological Sciences
ISSN :
0080-4649
Publisher :
Royal Society
Volume :
286
Issue :
1902
Pages :
20190142
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
Centre National de la recherche scientifique = French National Centre for Scientific Research - CNRS Fédération Wallonie Bruxelles. Fonds de la Recherche Scientifique - F.R.S.-FNRS
Lack D. 1968 Ecological adaptations for breeding in birds. London, UK: Methuen.
Baker JR. 1938 The evolution of breeding seasons. In Evolution: essays on aspects of evolutionary biology (ed. GR. de Beer), pp. 161-177. London, UK: Oxford University Press.
Gow EA et al. 2019 A range-wide domino effect and resetting of the annual cycle in a migratory songbird. Proc. R. Soc. B 286, 20181916. (doi:10. 1098/rspb.2018.1916)
Dawson A. 2008 Control of the annual cycle in birds: endocrine constraints and plasticity in response to ecological variability. Phil. Trans. R. Soc. B 363, 1621-1633. (doi:10.1098/ rstb.2007.0004)
Dawson A, King VM, Bentley GE, Ball GF. 2001 Photoperiodic control of seasonality in birds. J. Biol. Rhythms 16, 365-380. (doi:10.1177/ 074873001129002079)
Goldman BD. 2001 Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement. J. Biol. Rhythms 16, 283-301. (doi:10.1177/ 074873001129001980)
Burger WJ. 1949 A review of experimental investigations on seasonal reproduction in birds. Wilson Bull. 61, 211-230.
Caro SP. 2012 Avian ecologists and physiologists have different sexual preferences. Gen. Comp. Endocrinol. 176, 1-8. (doi:10.1016/j.ygcen.2011. 12.021)
Ball GF, Ketterson ED. 2008 Sex differences in the response to environmental cues regulating seasonal reproduction in birds. Phil. Trans. R. Soc. B 363, 231-246. (doi:10.1098/rstb.2007.2137)
van Noordwijk AJ, van Balen JH, Scharloo W. 1981 Genetic variation in the timing of reproduction in the great tit. Oecologia 49, 158-166. (doi:10.1007/ BF00349183)
Caro SP, Charmantier A, Lambrechts MM, Blondel J, Balthazart J, Williams TD. 2009 Local adaptation of timing of reproduction: females are in the driver's seat. Funct. Ecol. 23, 172-179. (doi:10.1111/j.1365-2435.2008.01486.x)
Sheldon BC, Kruuk L.EB, Merila J. 2003 Natural selection and inheritance of breeding time and clutch size in the collared flycatcher. Evolution 57, 406-420. (doi:10.1111/j.0014-3820.2003.tb00274.x)
van de Pol M, Heg D, Bruinzeel LW, Kuijper B, Verhulst S. 2006 Experimental evidence for a causal effect of pair-bond duration on reproductive performance in oystercatchers (Haematopus ostralegus). Behav. Ecol. 17, 982-991. (doi:10. 1093/beheco/arl036)
Williams TD. 2012 Physiological adaptation for breeding in birds. Princeton, NJ: Princeton University Press.
Williams TD. 2008 Individual variation in endocrine systems: moving beyond the 'tyranny of the Golden Mean'. Phil. Trans. R. Soc. B 363, 1687-1698. (doi:10.1098/rstb.2007.0003)
Williams TD, Kitaysky AS, Vezina F. 2004 Individual variation in plasma estradiol-17ß and androgen levels during egg formation in the European starling Sturnus vulgaris: implications for regulation of yolk steroids. Gen. Comp. Endocrinol. 136, 346-352. (doi:10.1016/j.ygcen.2004.01.010)
Kempenaers B, Peters A, Foerster K. 2008 Sources of individual variation in plasma testosterone levels. Phil. Trans. R. Soc. B 363, 1711-1723. (doi:10. 1098/rstb.2007.0001)
Zera AJ, Harshman LG, Williams TD. 2007 Evolutionary endocrinology: the developing synthesis between endocrinology and evolutionary genetics. Annu. Rev. Ecol. Evol. Syst. 38, 793-817. (doi:10.1146/annurev.ecolsys.38.091206.095615)
McGlothlin JW, Whittaker DJ, Schrock SE, Gerlach NM, Jawor JM, Snajdr EA, Ketterson ED. 2010 Natural selection on testosterone production in a wild songbird population. Am. Nat. 175, 687-701. (doi:10.1086/652469)
Rosvall KA. 2013 Proximate perspectives on the evolution of female aggression: good for the gander, good for the goose? Phil. Trans. R. Soc. B 368, 20130083. (doi:10.1098/rstb.2013.0083)
Visser ME, Caro SP, van Oers K, Schaper SV, Helm B. 2010 Phenology, seasonal timing and circannual rhythms: towards a unified framework. Phil. Trans. R. Soc. B 365, 3113-3127. (doi:10.1098/rstb. 2010.0111)
King JR, Follett BK, Farner DS, Morton ML. 1966 Annual gonadal cycles and pituitary gonadotropins in Zonotrichia leucophrys gambelli. Condor 68, 476-487. (doi:10.2307/1365320)
Dawson A, Goldsmith AR. 1983 Plasma prolactin and gonadotropins during gonadal development and the onset of photorefractoriness in male and female starlings (Sturnus vulgaris) on artificial photoperiods. J. Endocrinol. 97, 253-260. (doi:10. 1677/joe.0.0970253)
Farner DS, Follett BK, King JR, Morton ML. 1966 A quantitative examination of ovarian growth in the white-crowned sparrow. Biol. Bull. 130, 67-75. (doi:10.2307/1539953)
Schmidt KL, MacDougall-Shackleton EA, Soma KK, MacDougall-Shackleton SA. 2014 Developmental programming of the HPA and HPG axes by early-life stress in male and female song sparrows. Gen. Comp. Endocrinol. 196, 72-80. (doi:10.1016/j. ygcen.2013.11.014)
Crino OL, Jensen SM, Buchanan KL, Griffith SC. 2018 Evidence for condition mediated trade-offs between the HPA- and HPG-axes in the wild zebra finch. Gen. Comp. Endocrinol. 259, 189-198. (doi:10. 1016/j.ygcen.2017.11.025)
Rosvall KA, Bergeon Burns CM, Hahn TP, Ketterson ED. 2013 Sources of variation in HPG axis reactivity and individually consistent elevation of sex steroids in a female songbird. Gen. Comp. Endocrinol. 194, 230-239. (doi:10.1016/j.ygcen. 2013.09.015)
Ball GF. 2007 The ovary knows more than you think! New views on clock genes and the positive feedback control of luteinizing hormone. Endocrinology 148, 3029-3030. (doi:10.1210/en.2007-0570)
Nakao N et al. 2007 Circadian clock gene regulation of steroidogenic acute regulatory protein gene expression in preovulatory ovarian follicles. Endocrinology 148, 3031-3038. (doi:10.1210/en. 2007-0044)
Kriegsfeld LJ, Ubuka T, Bentley GE, Tsutsui K. 2015 Seasonal control of gonadotropin-inhibitory hormone (GnIH) in birds and mammals. Front Neuroendocrinol. 37, 65-75. (doi:10.1016/j.yfrne. 2014.12.001)
Drent PJ, van Oers K, van Noordwijk AJ. 2003 Realized heritability of personalities in the great tit (Parus major). Proc. R. Soc. B 270, 45-51. (doi:10. 1098/rspb.2002.2168)
van Oers K, Naguib M. 2013 Avian personality. In Animal personalities: behavior, physiology and evolution (eds C Carere, D Maestripieri), pp. 66-95. Chicago, IL, and London, UK: University of Chicago Press.
van Oers K, de Jong G, Drent PJ, van Noordwijk AJ. 2004 A genetic analysis of avian personality traits: correlated, response to artificial selection. Behav. Genet. 34, 611-619. (doi:10.1007/s10519-004-5588-z)
van Oers K, Drent PJ, de Goede P, van Noordwijk AJ. 2004 Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proc. R. Soc. B 271, 65-73. (doi:10.1098/rspb.2003. 2518)
Baugh AT, Witonsky KR, Davidson SC, Hyder L, Hau M, van Oers K. 2017 Novelty induces behavioural and glucocorticoid responses in a songbird artificially selected for divergent personalities. Anim. Behav. 130, 221-231. (doi:10.1016/j.anbehav. 2017.06.028)
Reparaz LB, van Oers K, Naguib M, Doutrelant C, Visser ME, Caro SP. 2014 Mate preference of female blue tits varies with experimental photoperiod. PLos One 9, e92527. (doi:10.1371/journal.pone.0092527)
Jawor JM, McGlothlin JW, Casto JM, Greives TJ, Snajdr EA, Bentley GE, Ketterson ED. 2006 Seasonal and individual variation in response to GnRH challenge in male dark-eyed juncos (Junco hyemalis). Gen. Comp. Endocrinol. 149, 182-189. (doi:10.1016/j.ygcen.2006.05.013)
Apfelbeck B, Goymann W. 2011 Ignoring the challenge? Male black redstarts (Phoenicurus ochruros) do not increase testosterone levels during territorial conflicts but they do so in response to gonadotropin-releasing hormone. Proc. R. Soc. B 278, 3233-3242. (doi:10.1098/rspb.2011.0098)
Newman AEM, Chin EH, Schmidt KL, Bond L, Wynne-Edwards KE, Soma KK. 2008 Analysis of steroids in songbird plasma and brain by coupling solid phase extraction to radioimmunoassay. Gen. Comp. Endocrinol. 155, 503-510. (doi:10.1016/j. ygcen.2007.08.007)
Wingfield JC, Farner DS. 1975 The determination of five steroids in avian plasma by radioimmunoassay and competitive protein-binding. Steroids 26, 311-327. (doi:10.1016/0039-128X(75)90077-X)
Charlier TD, Po KWL, Newman AEM, Shah AH, Saldanha CJ, Soma KK. 2010 17b-Estradiol levels in male zebra finch brain: combining Palkovits punch and an ultrasensitive radioimmunoassay. Gen. Comp. Endocrinol. 167, 18-26. (doi:10.1016/j.ygcen.2010. 02.002)
Bates D, Machler M, Bolker BM, Walker SC. 2015 Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1-48. (doi:10.18637/jss.v067.i01)
R-Core-Team. 2015 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. See http://www.R-project.org/.
Crawley MJ. 2007 The R book. Chichester, UK: John Wiley & Sons, Ltd.
Korner-Nievergelt F, Roth T, von Felten S, Guélat J, Almasi B, Korner-Nievergelt P. 2015 Bayesian data analysis in ecology using linear models with R, BUGS, and stan. New York, NY: Academic Press.
Gelman A, Sue Y-S. 2016 arm: Data analysis using regression and multilevel/hierarchical models. R package version 1.9-1. http://CRAN.R-project.org/ package=arm.
Needham KB, Burns CB, Graham JL, Bauer CM, Kittilson JD, Ketterson ED, Hahn T, Greives TJ. 2019 Changes in processes downstream of the hypothalamus are associated with seasonal follicle development in a songbird, the dark-eyed junco (Junco hyemalis). Gen. Comp. Endocrinol. 270, 103-112. (doi:10.1016/j.ygcen.2018.10.012)
Williams TD. 2012 Hormones, life-history, and phenotypic variation: opportunities in evolutionary avian endocrinology. Gen. Comp. Endocrinol. 176, 1145-1154. (doi:10.1016/j. ygcen.2011.11.028)
Vezina F, Salvante KG, Williams TD. 2003 The metabolic cost of avian egg formation: possible impact of yolk precursor production? J. Exp. Biol. 206, 4443-4451. (doi:10.1242/jeb.00702)
Williams TD, Martyniuk CJ. 2000 Tissue mass dynamics during egg-production in female Zebra Finches Taeniopygia guttata: dietary and hormonal manipulations. J. Avian Biol. 31, 87-95. (doi:10. 1034/j.1600-048X.2000.310112.x)
Edinger RS, Mambo E, Evans MI. 1997 Estrogen-dependent transcriptional activation and vitellogenin gene memory. Mol. Endocrinol. 11, 1985-1993. (doi:10.1210/mend.11.13.0037)
Ball GF, Balthazart J. 2002 Neuroendocrine mechanisms regulating reproductive cycles and reproductive behavior in birds. In Hormones, brain and behavior (eds DW Pfaff, AP Arnold, AM Etgen, SE Fahrbach, RT Rubin), pp. 649-798. San Diego, CA: Academic Press.
Wang C, Hsueh AJW, Erickson GF. 1981 LH stimulation of estrogen secretion by cultured rat granulosa cells. Mol. Cell. Endocrinol. 24, 17-28. (doi:10.1016/0303-7207(81)90075-7)
Johnson AL, Woods DC. 2007 Ovarian dynamics and follicle development. In Reproductive biology and phylogeny of birds (ed. BGM Jamieson), pp. 243-277. Enfield, NH: Science Publishers.
Caldwell JD, Gebhart VM, Jirikowski GF. 2016 Estradiol's interesting life at the cell's plasma membrane. Steroids 111, 4-11. (doi:10.1016/j. steroids.2016.03.012)
Kawaguchi R et al. 2011 Receptor-mediated cellular uptake mechanism that couples to intracellular storage. ACS Chem. Biol. 6, 1041-1051. (doi:10. 1021/cb200178w)
Selva DM, Hogeveen KN, Seguchi K, Tekpetey F, Hammond GL. 2002 A human sex hormone-binding globulin isoform accumulates in the acrosome during spermatogenesis. J. Biol. Chem. 277, 45 291 - 45 298. (doi:10.1074/jbc.M205903200)
Hammond GL. 2011 Diverse roles for sex hormone-binding globulin in reproduction. Biol. Reprod. 85, 431-441. (doi:10.1095/biolreprod.111.092593)
Deviche P, Hurley LL, Fokidis HB, Lerbour B, Silverin B, Silverin B, Sabo J, Sharp PJ. 2010 Acute stress rapidly decreases plasma testosterone in a free-ranging male songbird: potential site of action and mechanism. Gen. Comp. Endocrinol. 169, 82-90. (doi:10.1016/j.ygcen.2010.07.009)
Greives TJ, Fudickar AM, Atwell JW, Meddle SL, Ketterson ED. 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)
Groothuis T.GG, Carere C. 2005 Avian personalities: characterization and epigenesis. Neurosci. Biobehav. Rev. 29, 137-150. (doi:10.1016/j.neubiorev.2004. 06.010)
Cockrem JF. 2013 Individual variation in glucocorticoid stress responses in animals. Gen. Comp. Endocrinol. 181, 45-58. (doi:10.1016/j. ygcen.2012.11.025)
Overli O, Sorensen C, Pulman KG, Pottinger TG, Korzan W, Summers CH, Nilsson GE. 2007 Evolutionary background for stress-coping styles: relationships between physiological, behavioral, and cognitive traits in non-mammalian vertebrates. Neurosci. Biobehav. Rev. 31, 396-412. (doi:10. 1016/j.neubiorev.2006.10.006)
Koolhaas JM, de Boer SF, Coppens CM, Buwalda B. 2010 Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Front. Neuroendocrinol. 31, 307-321. (doi:10.1016/ j.yfrne.2010.04.001)
Carere C, Groothuis TGG, Mostl E, Daan S, Koolhaas JM. 2003 Fecal corticosteroids in a territorial bird selected for different personalities: daily rhythm and the response to social stress. Horm. Behav. 43, 540-548. (doi:10.1016/S0018-506X(03)00065-5)
Cockrem JF. 2007 Stress, corticosterone responses and avian personalities. J. Ornithol. 148, S169-S178. (doi:10.1007/s10336-007-0175-8)
Baugh AT, Schaper SV, Hau M, Cockrem JF, de Goede P, van Oers K. 2012 Corticosterone responses differ between lines of great tits (Parus major) selected for divergent personalities. Gen. Comp. Endocrinol. 175, 488-494. (doi:10.1016/j.ygcen.2011.12.012)
van Oers K, Buchanan KL, Thomas TE, Drent PJ. 2011 Correlated response to selection of testosterone levels and immunocompetence in lines selected for avian personality. Anim. Behav. 81, 1055-1061. (doi:10.1016/j.anbehav.2011. 02.014)
Ruuskanen S, Groothuis Ton GG, Baugh Alexander T, Schaper Sonja V, Vries B, Oers K. 2017 Maternal egg hormones in the mating context: the effect of pair personality. Funct. Ecol. 32, 439-449. (doi:10.1111/ 1365-2435.12987)
Langmore NE, Cockrem JF, Candy EJ. 2002 Competition for male reproductive investment elevates testosterone levels in female dunnocks, Prunella modularis. Proc. R. Soc. B 269, 2473-2478. (doi:10.1098/rspb.2002.2167)
Merritt JR, Davis MT, Jalabert C, Libecap TJ, Williams DR, Soma KK, Maney DL. 2018 Rapid effects of estradiol on aggression depend on genotype in a species with an estrogen receptor polymorphism. Horm. Behav. 98, 210-218. (doi:10.1016/j.yhbeh. 2017.11.014)
Laredo SA, Landeros RV, Trainor BC. 2014 Rapid effects of estrogens on behavior: environmental modulation and molecular mechanisms. Front. Neuroendocrinol. 35, 447-458. (doi:10.1016/j.yfrne. 2014.03.005)
Hegner RE, Wingfield JC. 1986 Behavioral and endocrine correlates of multiple brooding in the semicolonial house sparrow Passer domesticus. II. Females. Horm. Behav. 20, 313-326. (doi:10.1016/ 0018-506X(86)90040-1)
Reale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ. 2007 Integrating animal temperament within ecology and evolution. Biol. Rev. 82, 291-318. (doi:10.1111/j.1469-185X.2007. 00010.x)
Dubuc-Messier G, Caro SP, Perrier C, van Oers K, Réale D, Charmantier A. 2018 Gene flow does not prevent personality and morphological differentiation between two blue tit populations. J. Evol. Biol. 31, 1127-1137. (doi:10.1111/jeb.13291)
Verbeek MEM, Boon A, Drent PJ. 1996 Exploration, aggressive behavior and dominance in pair-wise confrontations of juvenile male great tits. Behaviour 133, 945-963. (doi:10.1163/156853996X00314)
Mutzel A, Kempenaers B, Laucht S, Dingemanse NJ, Dale J. 2011 Circulating testosterone levels do not affect exploration in house sparrows: observational and experimental tests. Anim. Behav. 81, 731-739. (doi:10.1016/j.anbehav.2011.01.001)
Evans MR, Roberts ML, Buchanan KL, Goldsmith AR. 2006 Heritability of corticosterone response and changes in life history traits during selection in the zebra finch. J. Evol. Biol. 19, 343-352. (doi:10. 1111/j.1420-9101.2005.01034.x)
Caro SP, Schaper SV, Dawson A, Sharp PJ, Gienapp P, Visser ME. 2013 Is microevolution the only emergency exit in a warming world? Temperature influences egg laying but not its underlying mechanisms in great tits. Gen. Comp. Endocrinol. 190, 164-169. (doi:10.1016/j.ygcen.2013.02.025)
Visser ME. 2008 Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc. R. Soc. B 275, 649-679. (doi:10.1098/rspb. 2007.0997)
Nussey DH, Froy H, Lemaitre J-F, Gaillard J-M, Austad SN. 2013 Senescence in natural populations of animals: widespread evidence and its implications for bio-gerontology. Ageing Res. Rev. 12, 214-225. (doi:10.1016/j.arr.2012.07.004)
Bouwhuis S, Sheldon BC, Verhulst S, Charmantier A. 2009 Great tits growing old: selective disappearance and the partitioning of senescence to stages within the breeding cycle. Proc. R. Soc. B 276, 2769-2777. (doi:10.1098/rspb.2009.0457)
Charmantier A, Perrins C, McCleery RH, Sheldon BC. 2006 Quantitative genetics of age at reproduction in wild swans: support for antagonistic pleiotropy models of senescence. Proc. Natl Acad. Sci. USA 103, 6587-6592. (doi:10.1073/pnas.0511123103)
Grunst AS, Grunst ML, Formica VA, Korody ML, Betuel AM, Barcelo-Serra M, Ford S, Gonser RA, Tuttle EM. 2018 Morph-specific patterns of reproductive senescence: connections to discrete reproductive strategies. Am. Nat. 191, 744-755. (doi:10.1086/697377)
Ottinger MA. 2007 Neuroendocrine aging in birds: comparing lifespan differences and conserved mechanisms. Ageing Res. Rev. 6, 46-53. (doi:10. 1016/j.arr.2007.02.006)
Nisbet ICT, Finch CE, Thompson N, Russek-Cohen E, Proudman JA, Ottinger MA. 1999 Endocrine patterns during aging in the common tern (Sterna hirundo). Gen. Comp. Endocrinol. 114, 279-286. (doi:10. 1006/gcen.1999.7255)
Wilcoxen TE, Bridge ES, Boughton RK, Hahn TP, Schoech SJ. 2013 Physiology of reproductive senescence in Florida scrub-jays: results from a long-term study and GnRH challenge. Gen. Comp. Endocrinol. 194, 168-174. (doi:10.1016/j.ygcen. 2013.09.016)
Caro SP, Cornil CA, van Oers K, Visser ME. 2019 Data from: Personality and gonadal development as sources of individual variation in response to GnRH challenge in female great tits. Dryad Digital Repository. (doi:10.5061/dryad.t6r3mq1)
