Natural selection acts in opposite ways on correlated hormonal mediators of prenatal maternal effects in a wild bird population

Ecology Letters

Volumn 17, Issue 10, 2014, Pages 1310-1315

  Tschirren, Barbara ^a   Postma, Erik ^a   Gustafsson, Lars ^b   Groothuis, Ton G G ^c   Doligez, Blandine ^d  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UPPSALA UNIVERSITY   (Sweden)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

^d UNIVERSITÉ LYON 1   (France)

Author keywords

Adaptation; Adaptive phenotypic plasticity; Maintenance of variation; Maternal effects; Natural selection; Prenatal effects; Trade off; Transgenerational effects; Yolk androgens; Yolk hormones

Indexed keywords

BIRD; CORRELATION; HORMONE; MATERNAL EFFECT; NATURAL SELECTION; PHENOTYPE; WILD POPULATION;

AVES;

ANDROSTENEDIONE; TESTOSTERONE;

ANIMAL; CHEMISTRY; EGG YOLK; FEMALE; FERTILITY; GENETIC SELECTION; GENETICS; LONGEVITY; PHYSIOLOGY; REPRODUCTIVE FITNESS; SONGBIRD; SWEDEN;

ANDROSTENEDIONE; ANIMALS; EGG YOLK; FEMALE; FERTILITY; GENETIC FITNESS; LONGEVITY; SELECTION, GENETIC; SONGBIRDS; SWEDEN; TESTOSTERONE;

EID: 84908291666     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/ele.12339     Document Type: Article

References (44)

1. Balthazart, J. & Adkins-Regan, E. (2002). Sexual differentiation of brain and behavior in birds. In: Hormones, Brain and Behavior (eds Pfaff, D.W., Arnold, A.P., Fahrbach, S.E., Etgen, A.M. & Rubin, R.T.). Academic Press, London, pp. 223-301.
2. Blows, M.W. & Brooks, R. (2003). Measuring nonlinear selection. Am. Nat., 162, 815-820.
3. Buchanan, K.L., Evans, M.R., Goldsmith, A.R., Bryant, D.M. & Rowe, L.V. (2001). Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signalling? Proc. R. Soc. Lond. B, 268, 1337-1344.
4. DeWitt, T.J., Sih, A. & Wilson, D.S. (1998). Costs and limits of phenotypic plasticity. Trends Ecol. Evol., 13, 77-81.
5. Doligez, B., Gustafsson, L. & Pärt, T. (2009). 'Heritability' of dispersal propensity in a patchy population. Proc. R. Soc. Lond. B, 276, 2829-2836.
6. Eising, C.M., Visser, G.H., Müller, W. & Groothuis, T.G.G. (2003). Steroids for free? No metabolic costs of elevated maternal androgen levels in the black-headed gull. J. Exp. Biol., 206, 3211-3218.
7. Gil, D. (2008). Hormones in avian eggs: physiology, ecology and behavior. Adv. Stud. Behav., 38, 337-398.
8. Gil, D., Leboucher, G., Lacroix, A., Cue, R. & Kreutzer, M. (2004). Female canaries produce eggs with greater amount of testosterone when exposed to preferred male song. Horm. Behav., 45, 64-70.
9. Groothuis, T.G. & Schwabl, H. (2002). Determinants of within- and among-clutch variation in levels of maternal hormones in black-headed gull eggs. Funct. Ecol., 16, 281-289.
10. Groothuis, T.G.G. & Schwabl, H. (2008). Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Philos. Trans. R. Soc. Lond. B, 363, 1647-1661.
11. Groothuis, T.G.G., Eising, C.M., Dijkstra, C. & Müller, W. (2005a). Balancing between costs and benefits of maternal hormone deposition in avian eggs. Biol. Lett., 1, 78-81.
12. Groothuis, T.G.G., Müller, W., von Engelhardt, N., Carere, C. & Eising, C. (2005b). Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci. Biobehav. Rev., 29, 329-352.
13. Gustafsson, L. (1989). Collared flycatcher. In Lifetime Reproduction in Birds. (ed Newton, I.). Academic Press, London, pp. 75-88.
14. Hegyi, G., Herényi, M., Szöllosi, E., Rosivall, B., Török, J. & Groothuis, T.G.G. (2011). Yolk androstenedione, but not testosterone, predicts offspring fate and reflects parental quality. Behav. Ecol., 22, 29-38.
15. Kyo, S., Takakura, M., Kanaya, T., Zhuo, W., Fujimoto, K., Nishio, Y. et al. (1999). Estrogen activates telomerase. Cancer Res., 59, 5917-5921.
16. Lande, R. & Arnold, S.J. (1983). The measurement of selection on correlated characters. Evolution, 37, 1210-1226.
17. Lindén, M., Gustafsson, L. & Pärt, T. (1992). Selection on fledging mass in the collared flycatcher and the great tit. Ecology, 73, 336-343.
18. Michl, G., Török, J., Péczely, P., Garamszegi, L.Z. & Schwabl, H. (2005). Female collared flycatchers adjust yolk testosterone to male age, but not to attractiveness. Behav. Ecol., 16, 383-388.
19. Morgane, P.J., Austinlafrance, R., Bronzino, J., Tonkiss, J., Diazcintra, S., Cintra, L. et al. (1993). Prenatal malnutrition and development of the brain. Neurosci. Biobehav. Rev., 17, 91-128.
20. Mousseau, T.A. & Fox, C.W. (1998). Maternal Effects as Adaptations. Oxford University Press, New York.
21. Muriel, J., Perez-Rodriguez, L., Puerta, M. & Gil, D. (2013). Differential effects of yolk testosterone and androstenedione in embryo development and nestling growth in the spotless starling (Sturnus unicolor). Gen. Comp. Endocrinol., 194, 175-182.
22. Navara, K.J., Hill, G.E. & Mendonca, M.T. (2006). Yolk testosterone stimulates growth and immunity in house finch chicks. Physiol. Biochem. Zool., 79, 550-555.
23. Okuliarova, M., Groothuis, T.G.G., Skrobanek, P. & Zeman, M. (2011). Experimental evidence for genetic heritability of maternal hormone transfer to offspring. Am. Nat., 177, 824-834.
24. Pärt, T. & Gustafsson, L. (1989). Breeding dispersal in the Collared flycatcher (Ficedula albicollis) - possible causes and reproductive consequences. J. Anim. Ecol., 58, 305-320.
25. Pigliucci, M. (2001). Phenotypic Plasticity: Beyond Nature and Nurture. John Hopkins University Press, Baltimore.
26. Pitala, N., Ruuskanen, S., Laaksonen, T., Doligez, B., Tschirren, B. & Gustafsson, L. (2009). The effects of experimentally manipulated yolk androgens on growth and immune function of male and female nestling collared flycatchers Ficedula albicollis. J. Avian Biol., 40, 225-230.
27. Postma, E., Siitari, H., Schwabl, H., Richner, H. & Tschirren, B. (2014). The multivariate egg: quantifying within- and among-clutch correlations between maternally derived yolk immunoglobulins and yolk androgens using multivariate mixed models. Oecologia, 174, 631-638.
28. Roberts, M.L., Buchanan, K.L. & Evans, M.R. (2004). Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim. Behav., 68, 227-239.
29. Rossiter, M.C. (1996). Incidence and consequences of inherited environmental effects. Annu. Rev. Ecol. Syst., 27, 451-476.
30. Schwabl, H. (1993). Yolk is a source of maternal testosterone for developing birds. Proc. Natl Acad. Sci. USA, 90, 11446-11450.
31. Schwabl, H., Mock, D.W. & Gieg, J.A. (1997). A hormonal mechanism for parental favouritism. Nature, 386, 231-231.
32. Skaug, H., Fournier, D., Nielsen, A., Magnusson, A. & Bolker, B. (2013). Generalized Linear Mixed Models using AD Model Builder. R package version 0.7.5. Available at: https://www.google.ch/url?sa=t&rct=j& q=&esrc=s&source=web&cd=1&ved=0CCEQFjAA&url=https%3A %2F%2Fr-forge.r-project.org%2Fscm%2Fviewvc.php%2F*checkout*% 2Fpkg%2Finst%2Fdoc%2FglmmADMB.pdf%3Froot%3Dglmmadmb& ei=EBPSU5TFGbCT0QWOnIBo&usg=AFQjCNHmM09fDt7VswAzv VTCmWvbaoskbA&bvm=bv.71667212,d.d2k.
33. Sockman, K.W. & Schwabl, H. (2000). Yolk androgens reduce offspring survival. Proc. R. Soc. Lond. B, 267, 1451-1456.
34. Stinchcombe, J.R., Agrawal, A.F., Hohenlohe, P.A., Arnold, S.J. & Blows, M.W. (2008). Estimating nonlinear selection gradients using quadratic regression coefficients: double or nothing? Evolution, 62, 2435-2440.
35. Svensson, L. (1992). Identification Guide to European Passerines. Heraclio Fournier SA, Vitoria.
36. Tinbergen, J.M. & Boerlijst, M.C. (1990). Nestling weight and survival in individual great tits (Parus major). J. Anim. Ecol., 59, 1113-1127.
37. Tobler, M., Nilsson, J.A. & Nilsson, J.F. (2007). Costly steroids: egg testosterone modulates nestling metabolic rate in the zebra finch. Biol. Lett., 3, 408-410.
38. Tschirren, B., Saladin, V., Fitze, P.S., Schwabl, H. & Richner, H. (2005). Maternal yolk testosterone does not modulate parasite susceptibility or immune function in great tit nestlings. J. Anim. Ecol., 74, 675-682.
39. Tschirren, B., Fitze, P.S. & Richner, H. (2007). Maternal modulation of natal dispersal in a passerine bird: an adaptive strategy to cope with parasitism? Am. Nat., 169, 87-93.
40. Tschirren, B., Sendecka, J., Groothuis, T.G.G., Gustafsson, L. & Doligez, B. (2009). Heritable variation in maternal yolk hormone transfer in a wild bird population. Am. Nat., 174, 557-564.
41. Venables, W.N. & Ripley, B.D. (2002). Modern Applied Statistics with S, 4th edn. Springer, New York.
42. Weinstock, M. (2008). The long-term behavioural consequences of prenatal stress. Neurosci. Biobehav. Rev., 32, 1073-1086.
43. Wolf, J.B. & Wade, M.J. (2001). On the assignment of fitness to parents and offspring: whose fitness is it and when does it matter? J. Evol. Biol., 14, 347-356.
44. Yee, T.W. (2013). VGAM: Vector Generalized Linear and Additive Models. R package version 0.9-3. Available at: http://cran.r-project.org/web/packages/VGAM/citation.html.