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Testosterone and the dark ventral patch of male red deer: the role of the social environment

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Abstract

The expression of male sexual traits, which is stimulated by testosterone, entails significant costs for individuals. Consequently, natural selection is expected to favour the modulation of sexual trait development according to the balance between its costs and benefits. The proportion of rivals in a population may affect this balance by increasing or decreasing the reproductive benefits associated with the development of sex traits. Here, we explore the relationship between testosterone level and sex trait size under two populational conditions of mate competition: fenced (i.e. high male-male competition; all male age groups are present) and unfenced (i.e. low competition; most males present are juveniles). Our model species is the Iberian red deer (Cervus elaphus hispanicus), and the sex trait is the dark ventral patch that males exhibit during the rutting season. Our results showed that the positive relationship between testosterone levels and the size of the dark ventral patch depends on the environmental level of male-male competition. Only in populations where the operational sex ratio was high (i.e. high proportion of rival males), individuals with high levels of testosterone developed the sex trait. Conversely, when mate competition was low, there was no significant relationship between testosterone level and trait size. This result reinforces the idea that the effect of testosterone in promoting the development of sex traits may be mediated by the intensity of mate competition in the population, as well as the role of sexual selection in the evolution of the dark ventral patch in red deer.

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References

  • Ábalos J, Pérez I de Lanuza G, Carazo P, Font E (2016) The role of male colouration in the outcome of staged contests in the European common wall lizard (Podarcis muralis). Behaviour 153:607–631

    Google Scholar 

  • Adkins-Regan E (2005) Hormones and animal social behaviour. Princeton University Press, Princeton

    Google Scholar 

  • Alin A (2010) Multicollinearity. Wiley Interdiscip Rev Comput Stat 3:370–374

    Google Scholar 

  • Arteaga L, Bautista A, Martínez-Gómez M, Nicolás L, Hudson R (2008) Scent marking, dominance and serum testosterone levels in male domestic rabbits. Physiol Behav 94:510–515

    CAS  PubMed  Google Scholar 

  • Atwell J, Cardoso GC, Whittaker CJ, Price TD, Ketterson ED (2014) Hormonal, behavioral, and life-history traits exhibit correlated shifts in relation to population establishment in a novel environment. Am Nat 184:147–160

    Google Scholar 

  • Babak N (2015) Uncertainty analysis for species distribution models. R package version 1.1–15

  • Barja I, Silván G, Rosellini S, Piñeiro A, González-Gil A, Camacho L, Illera JC (2007) Stress physiological responses to tourist pressure in a wild population of European pine marten. J Steroid Biochem Mol Biol 104:136–142

    CAS  PubMed  Google Scholar 

  • Barja I, Silvá F, Rosellini S, Piñeiro A, Illera MJ, Illera JC (2008) Quantification of sexual steroid hormones in faeces of Iberian wolf (Canis lupus signatus): a non-invasive sex typing method. Reprod Domest Anim 43:701–707

    CAS  PubMed  Google Scholar 

  • Barja I, Escribano-Ávila G, Lara-Romero C, Virgós E, Benito J, Rafart E (2012) Non-invasive monitoring of adrenocortical activity in European badgers (Meles meles) and effects of sample collection and storage on faecal cortisol metabolite concentrations. Anim Biol 62:419–432

    Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Statist Softw 61:1–48

    Google Scholar 

  • Brockman DK, Whitten PL, Richard AF, Benander B (2001) Birth season testosterone levels in male Verreaux’s sifaka, Propithecus verreauxi: insights into socio-demographic factors mediating seasonal testicular function. Behav Ecol Sociobiol 49:117–127

    Google Scholar 

  • Cain KE, Pryke SR (2017) Testosterone production ability predicts breeding success and tracks breeding stage in male finches. J Evol Biol 30:430–436

    CAS  PubMed  Google Scholar 

  • Carranza J (1995) Female attraction by males versus sites in territorial rutting red deer. Anim Behav 50:445–453

    Google Scholar 

  • Carranza J, Alvarez F, Redondo T (1990) Territoriality as a mating strategy in red deer. Anim Behav 40:79–88

    Google Scholar 

  • Carranza J, Fernandez-Lario P, Gomendio M (1996) Correlates of territoriality in rutting red deer. Ethology 102:793–805

    Google Scholar 

  • Carranza J, Alarcos S, Sánchez-Prieto C, Valencia J, Mateos C (2004) Disposable-soma senescence mediated by sexual selection in an ungulate. Nature 432:215–218

    CAS  PubMed  Google Scholar 

  • Cornwallis CK, Birkhead TR (2008) Plasticity in reproductive phenotypes reveals status-specific correlations between behavioural, morphological and physiological sexual traits. Evolution 62:1149–1161

    PubMed  Google Scholar 

  • Damber JE, Janson PO (1978) The effects of LH, adrenaline and noradrenaline on testicular blood flow and plasma testosterone concentrations in anaesthetized rats. Acta Endrocrinol Buch 88:390–396

    CAS  Google Scholar 

  • de la Peña E, Martín J, Carranza J (2019) The intensity of male-male competition may affect chemical scent constituents in the dark ventral patch of male Iberian red deer. PLoS One 14(9):e0221980

    PubMed  PubMed Central  Google Scholar 

  • de la Peña E, Martín J, Barja I, Pérez-Caballero R, Acosta I, Carranza J (2020) The immune challenge of mating effort: steroid hormone profile, dark ventral patch and parasite burden in relation to intrasexual competition in male Iberian red deer. Integr Zool. https://doi.org/10.1111/1749-4877.12427

  • Dloniak SF, French JA, Holekamp KE (2006) Faecal androgen concentrations in adult male spotted hyaenas, Crocuta crocuta, reflect interactions with socially dominant females. Anim Behav 71:27–37

    Google Scholar 

  • Douglas HD, Kitaysky AS, Kitaiskaia EV, Maccomick A, Kelly A (2009) Size of ornament is negatively correlated with baseline corticosterone in males of a socially monogamous colonial seabird. J Comp Physiol B 179:297–304

    PubMed  Google Scholar 

  • Escribano-Ávila G, Pettorelli N, Virgós E, Lara-Romero C, Lozano J, Barja I, Cuadra FS, Puerta M (2013) Testing Cort-Fitness and Cort-Adaptation hypotheses in a habitat suitability gradient for roe deer. Acta Oecol 53:38–48

    Google Scholar 

  • Faivre B, Grégoire A, Préault M, Cézilly F, Sorci G (2003) Immune activation rapidly mirrored in a secondary sexual trait. Science 300:103–103

    CAS  PubMed  Google Scholar 

  • Fletcher TJ (1978) The induction of male sexual behavior in red deer (Cervus elaphus) by the administration of testosterone to hinds and estradiol-17β to stags. Horm Behav 11:74–88

    CAS  PubMed  Google Scholar 

  • Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622

    Google Scholar 

  • Gadgil M (1972) Male dimorphism as a consequence of sexual selection. Am Nat 106:574–580

    Google Scholar 

  • Galván I, Solano F, Zougagh M, Andrés F, Murtada K, Ríos A, de la Peña E, Carranza J (2019) Unprecedented high catecholamine production causing hair pigmentation after urinary excretion in red deer. Cell Mol Life Sci 76:397–404

    PubMed  Google Scholar 

  • Gatenbeck L, Eneroth P, Johansson B, Strömberg L (1987) Plasma testosterone concentrations in male rats during short and long-term stress stimulation. Scand J Urol Nephrol 21:139–142

    CAS  PubMed  Google Scholar 

  • Hartl GB, Klein F, Willing R, Apollonio M, Lang G (1995) Allozymes and the genetics of antler development in red deer (Cervus elaphus). J Zool 237:83–100

    Google Scholar 

  • Götz F, Stahl F, Rohde W, Dörner G (1983) The influence of adrenaline on plasma testosterone in adult and newborn male rats. Exp Clin Endocrinol Diabetes 81:239–244

  • Horcajada-Sánchez F, Escribano-Ávila G, Lara-Romero C, Virgós E, Barja I (2019) The effect of livestock on the physiological condition of roe deer (Capreolus capreolus) is modulated by habitat quality. Sci Rep 9:15953

  • Iglesias-Merchán C, Horcajada-Sánchez F, Diaz-Balteiro L, Escribano-Ávila G, Lara-Romero C, Virgós E, Planillo A, Barja I (2018) A new large-scale index (AcED) for assessing traffic noise disturbance on wildlife: stress response in a roe deer (Capreolus capreolus) population. Environ Monit Assess 490:185

    Google Scholar 

  • Karubian J, Lindsay WR, Schwabl H, Webster MS (2011) Bill coloration, a flexible signal in a tropical passerine bird, is regulated by social environment and androgens. Anim Behav 81:795–800

    Google Scholar 

  • Ketterson ED, Nolan V Jr, Casto JM, Buerkle CA, Clotfelter E, Grindstaff JL, Jones KJ, Lipar JL, McNabb FMA, Neudorf DL, Parker-Renga I, Schoech SJ, Snajdr E (2001) Testosterone, phenotype and fitness: a research program in evolutionary behavioral endocrinology. Avian Endocrinology. Narosa Publishing House, New Delhi, pp 19–40

    Google Scholar 

  • Lamichhaney S, Fan G, Widemo F, Gunnarsson U, Thalmann DS, Hoeppner MP, Chen W (2016) Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax). Nat Genet 48:84–88

    CAS  PubMed  Google Scholar 

  • Lemaître JF, Berger V, Bonenfant C, Douhard M, Gamelon M, Plard F, Gaillard JM (2015) Early-late life trade-offs and the evolution of ageing in the wild. Proc Biol Sci 282(1806):20150209

    PubMed  PubMed Central  Google Scholar 

  • Lendvai AZ, Giraudeau M, Németh J, Bakó V, McGraw KJ (2013) Carotenoid-based plumage colouration reflects feather corticosterone levels in male house finches (Haemorhous mexicanus). Behav Ecol Sociobiol 67:1817–1824

    Google Scholar 

  • Lincoln G, Guinness FA, Short RV (1972) The way in which testosterone controls the social and sexual behavior of the red deer stag (Cervus elaphus). Horm Behav 3:375–396

    CAS  Google Scholar 

  • Lobato E, Moreno J, Merino S, Morales J, Tomas G, Martinez J, Vasquez RA, Kuchar A, Mostl E, Osorno JL (2010) Arrival date and territorial behaviour are associated with corticosterone metabolite levels in a migratory songbird. J Ornithol 151:587–597

    Google Scholar 

  • Malo AF, Roldan ERS, Garde JJ, Soler AJ, Vicente J, Górtazar C, Gomendio M (2009) What does testosterone do for red deer males? Proc R Soc Lond B 276:971–980

    CAS  Google Scholar 

  • Martín J, Carranza J, López P, Alarcos S, Pérez-González J (2014) A new sexual signal in rutting male red deer: age related chemical scent constituents in the belly black spot. Mamm Biol 79:362–368

    Google Scholar 

  • Mateos C (2005) The subordination stress paradigm and the relation between testosterone and corticosterone in male ring-necked pheasants. Anim Behav 69:249–255

    Google Scholar 

  • Mateos C, Carranza J (1997) Signals in intrasexual competition between ring-necked pheasant males. Anim Behav 53:471–485

    Google Scholar 

  • Mayerhofer A, Steger RW, Gow G, Bartke A (1992) Catecholamines stimulate testicular testosterone release of the immature golden hamster via interaction with alpha- and beta-adrenergic receptors. Acta Endocrinol Buch 127:526–530

    CAS  Google Scholar 

  • McGraw KJ (2006) Dietary mineral content influences the expression of melanin-based ornamental colouration. Behav Ecol 18:137–142

    Google Scholar 

  • McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162:704–712

    PubMed  Google Scholar 

  • Mills SC, Grapputo A, Jokinen I, Koskela E, Mappes T, Oksanen TA, Poikonen T (2009) Testosterone-mediated effects on fitness-related phenotypic traits and fitness. Am Nat 173:475–487

    PubMed  Google Scholar 

  • Mougent F, Reader BF, Piertney SB (2005) Separating behavioural and physiological mechanisms in testosterone-mediated trade-offs. Am Nat 166:158–168

    Google Scholar 

  • Pérez-González J, Carranza J (2009) Female-biased dispersal under conditions of low male mating competition in a polygynous mammal. Mol Ecol 18:4617–4630

    PubMed  Google Scholar 

  • Pérez-González J, Carranza J (2011) Female aggregation interacts with population structure to influence the degree of polygyny in red deer. Anim Behav 82:957–970

    Google Scholar 

  • Pérez-González J, Frantz AC, Torres-Porras J, Castillo L, Carranza J (2012) Population structure, habitat features and genetic structure of managed red deer populations. Eur J Wildl Res 58:933–943

    Google Scholar 

  • Peters M, Simmons LW, Rhodes G (2008) Testosterone is associated with mating success but not attractiveness or masculinity in human males. Anim Behav 76:297–303

    Google Scholar 

  • Piñeiro A, Barja I, Silván G, Illera JC (2012) Effects of tourist pressure and reproduction on physiological stress response in wildcats: management implications for species conservation. Wildl Res 39:532–539

    Google Scholar 

  • Rajagopal T (2009) A study on the reproductive behaviour and pheromones of an endangered Indian Blackbuck (Antelope cervicapra L.) to enhance captive breeding and conservation. Ph.D. Thesis. Bharathidasan University, Tiruchirappalli, Tamil Nadu, India

  • Raouf SA, Parker PG, Ketterson ED, Nolan V, Ziegenfus C (1997) Testosterone affects reproductive success by influencing extra–pair fertilizations in male dark–eyed juncos (Aves: Junco hyemalis). Proc R Soc Lond B 264:1599–1603

    CAS  Google Scholar 

  • Roulin A, Wink A, Salamin N (2008) Selection on a eumelanic ornament is stronger in the tropics than in temperate zones in the worldwide-distributed barn owl. J Evol Biol 22:345–354

    PubMed  Google Scholar 

  • Rubenstein DR, Shen SF (2009) Reproductive conflict and the costs of social status in cooperatively breeding vertebrates. Am Nat 173:650–662

    PubMed  Google Scholar 

  • Saino N, Incagli M, Martinelli R, Møller AP (2002) Immune response of male barn swallows in relation to parental effort, corticosterone plasma levels, and sexual ornamentation. Behav Ecol 13:169–174

    Google Scholar 

  • Senar JC, Camerino M, Copete JL, Metcalfe NB (1993) Variation in black bib of the Eurasian siskin (Carduelis spinus) and its role as a reliable badge of dominance. Auk 110:924–927

    Google Scholar 

  • Shuster SM, Wade MJ (2003) Mating systems and strategies. Princeton University Press, Princeton

    Google Scholar 

  • Sinervo B, Zamudio KR (2001) The evolution of alternative reproductive strategies: fitness differential, heritability, and genetic correlation between the sexes. J Hered 92:198–205

    CAS  PubMed  Google Scholar 

  • Tibbetts EA, Dale J (2004) A socially enforced signal of quality in a paper wasp. Nature 432:218–222

    CAS  PubMed  Google Scholar 

  • Tibbetts EA, Mullen SP, Dale J (2017) Signal function drives phenotypic and genetic diversity: the effects of signaling individual identity, quality or behavioural strategy. Philos Trans R Soc B 372:20160347

    Google Scholar 

  • Torres-Porras J, Carranza J, Pérez-González J, Mateos C, Alarcos S (2014) The tragedy of the commons: unsustainable population structure of Iberian red deer in hunting estates. Eur J Wildl Res 60:351–357

    Google Scholar 

  • Vergara P, Martínez-Padilla J (2012) Social context decouples the relationship between a sexual ornament and testosterone levels in a male wild bird. Horm Behav 62:407–412

    CAS  PubMed  Google Scholar 

  • Wingfield J, Ball G, Dufty A, Hegner R, Ramenofsky M (1987) Testosterone and aggression in birds. Am Sci 75:602–608

    Google Scholar 

  • Wingfield J, Hegner RE, Dufty AM, Ball GF (1990) The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829–846

    Google Scholar 

  • Wingfield JC, Lynn S, Soma KK (2001) Avoiding the ‘costs’ of testosterone: ecological bases of hormone-behavior interactions. Brain Behav Evol 57:239–251

    CAS  PubMed  Google Scholar 

  • Wyman MJ, Agrawal AF, Rowe L (2010) Condition-dependence of the sexually dimorphic transcriptome in Drosophila melanogaster. Evolution 64:1836–1848

    PubMed  Google Scholar 

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Acknowledgements

We thank Marco Apollonio and an anonymous reviewer for helpful comments. We thank the autonomous governments of Andalucía (Junta de Andalucía) and Extremadura (Junta de Extremadura) and the owners of the hunting estates that provided permissions and facilities for fieldwork. Jose Manuel Seoane and students from the University of Córdoba helped in fieldwork and samples collection. We are indebted to P. Capilla-Lasheras for his advice on the statistical approach.

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Financial support came from projects CGL2013-48122-P and CGL2016-77052-P to JC.

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Correspondence to Eva de la Peña.

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No animal was harvested for the purpose of this study. The relevant permits were obtained for the samples and data collection after hunting actions by the government of Andalusia.

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Communicated by: Paula Roig Boixeda

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de la Peña, E., Martín, J., Barja, I. et al. Testosterone and the dark ventral patch of male red deer: the role of the social environment. Sci Nat 107, 18 (2020). https://doi.org/10.1007/s00114-020-01674-1

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