Oecologia

, Volume 160, Issue 4, pp 657–665

Hormonally mediated maternal effects shape offspring survival potential in stressful environments

Physiological Ecology - Original Paper

Abstract

In most egg-laying vertebrates, maternal responses to stressful conditions are translated into the release of glucocorticoid hormones such as cortisol, which are then transmitted to their developing embryos. Although such maternally transmitted hormonal resources have been shown to influence or even interfere with the optimal developmental trajectories of offspring in many taxa, their influence on the dynamics of wild fish populations remains largely unexplored. Here, we examined the extent to which simulated hormonally mediated maternal effects influence the development and early survival of the coral reef damselfish, Pomacentrus amboinensis. Concentrations of cortisol in the eggs were manipulated within naturally occurring limits by immersion. We found that the proportion of embryos that delayed hatching when exposed to high levels of cortisol was considerably lower than in the other two treatments (low cortisol dose and control). High cortisol levels in P. amboinensis eggs resulted in increased egg mortality and greater asymmetry in hatchlings. For embryos that successfully hatched, individuals from the elevated cortisol treatments (especially low dose) survived longer after hatching. Although individuals that originated from eggs with elevated cortisol levels survived longer after hatching, they may not gain an overall survival advantage. Our results suggest that subtle increases in the allocation of maternally derived hormones, such as cortisol, to offspring are a direct way for stressed mothers to endow their young with an immediate survival advantage. We propose that this immediate benefit outweighs the developmental costs which may be expressed as reduced fitness at later life stages.

Keywords

Coral reef fish Cortisol Fluctuating asymmetry Phenotypic plasticity Selective mortality 

Supplementary material

442_2009_1335_MOESM1_ESM.eps (10.3 mb)
Supplementary material (EPS 10.3 MB)

References

  1. Barry TP, Malison JA, Held JA, Parrish JJ (1995) Ontogeny of the cortisol stress response in larval rainbow trout. Gen Comp Endocrinol 97:57–65PubMedCrossRefGoogle Scholar
  2. Braastad BO (1998) Effects of prenatal stress on behaviour of offspring of laboratory and farmed mammals. Appl Anim Behav Sci 61:159–180CrossRefGoogle Scholar
  3. Bowden RM, Ewert MA, Nelson CE (2002) Hormone levels in yolk decline throughout development in the red-eared slider turtle (Trachemys scripta elegans). Gen Comp Endocrinol 129:171–177PubMedCrossRefGoogle Scholar
  4. Crespi EJ, Denver RJ (2005) Ancient origins of human developmental plasticity. Am J Hum Biol 17:44–54PubMedCrossRefGoogle Scholar
  5. de Fraipont M, Clobert J, John-Alder H, Meylan S (2000) Increased prenatal maternal corticosterone promotes philanthropy of offspring in common lizard (Lacerta vivipara). J Anim Ecol 69:404–413CrossRefGoogle Scholar
  6. De Jesus EG, Hirano T (1992) Changes in whole body concentrations of cortisol, thyroid hormones and sex steroids during early development of the chum salmon, Oncorhynchus keta. Gen Comp Endocrinol 85:55–61PubMedCrossRefGoogle Scholar
  7. Debat V, David P (2001) Mapping phenotypes: canalization, plasticity and developmental stability. Trends Ecol Evol 16:555–561CrossRefGoogle Scholar
  8. Denver RJ (1997) Environmental stress as a developmental cue: corticotrophin-releasing hormone is a proximate mediator of adaptive phenotypic plasticity in amphibian metamorphosis. Horm Behav 31:169–179PubMedCrossRefGoogle Scholar
  9. Dillon TM, Lynch MP (1981) Physiological responses as determinants of stress in marine and estuarine organisms. In: Barrett GW, Rosenberg R (eds) Stress effects on natural ecosystems. Wiley, New York, pp 227–241Google Scholar
  10. Dufty AM Jr, Clobert J, Møller AP (2002) Hormones, developmental plasticity and adaptation. Trends Ecol Evol 17:190–196CrossRefGoogle Scholar
  11. Eising CM, Muller W, Dijkstra C, Groothuis TGG (2003) Maternal androgens in egg yolks: relation with sex, incubation time and embryonic growth. Gen Comp Endocrinol 132:241–247PubMedCrossRefGoogle Scholar
  12. Elf PK, Fivizzani AJ (2002) Changes in sex steroid levels in yolks of the leghorn chicken, Gallus domesticus, during embryonic development. J Exp Zool 293:594–600PubMedCrossRefGoogle Scholar
  13. Elf PK, Lang JW, Fivizzani AJ (2002) Dynamics of yolk steroid hormones during development in a reptile with temperature-dependent sex determination. Gen Comp Endocrinol 127:34–39PubMedCrossRefGoogle Scholar
  14. Emslie MJ, Jones GP (2001) Patterns of embryo mortality in a demersally spawning coral reef fish and the role of predatory fishes. Environ Biol Fish 60:363–373CrossRefGoogle Scholar
  15. Eriksen MS, Haug A, Torjesen PA, Bakken M (2003) Prenatal exposure to corticosterone impairs embryonic development and increases fluctuating asymmetry in chickens (Gallus domesticus). Br Poult Sci 44:690–697PubMedCrossRefGoogle Scholar
  16. Eriksen MS, Bakken M, Espmark Å, Braadstad BO, Salte R (2006) Prespawning stress in farmed Atlantic salmon Salmo salar: maternal cortisol exposure and hyperthermia during embryonic development affect offspring survival, growth and incidence of malformations. J Fish Biol 69:114–129CrossRefGoogle Scholar
  17. Gagliano M, McCormick MI (2007) Maternal condition influences phenotypic selection on offspring. J Anim Ecol 76:174–182PubMedCrossRefGoogle Scholar
  18. Gagliano M, Depczynski M, Simpson SD, Moore JAY (2008) Dispersal without errors: symmetrical ears tune into the right frequency for survival. Proc R Soc B 275:527–534PubMedCrossRefGoogle Scholar
  19. Gibson G, Wagner G (2000) Canalization in evolutionary genetics: a stabilizing theory? Bioessays 22:372–380PubMedCrossRefGoogle Scholar
  20. Groothuis TGG, Müller W, von Engelhardt N, Carere C, Eising C (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev 29:329–352PubMedCrossRefGoogle Scholar
  21. Hayward LS, Wingfield JC (2004) Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. Gen Comp Endocrinol 135:365–371PubMedCrossRefGoogle Scholar
  22. Kerrigan BA (1996) Temporal patterns in the size and condition of settlement in two tropical reef fishes (Pomacentridae: Pomacentrus amboinensis and P. nagasakiensis). Mar Ecol Prog Ser 135:27–41CrossRefGoogle Scholar
  23. Kitaysky AS, Kitaiskaia EV, Piatt JF, Wingfield JC (2003) Benefits and costs of increased levels of corticosterone in seabird chicks. Horm Behav 43:140–149PubMedCrossRefGoogle Scholar
  24. Lacey EP (1998) What is an adaptive environmentally induced parental effect? In: Mousseau TA, Fox CW (eds) Maternal effects as adaptations. Oxford University Press, New York, pp 54–66Google Scholar
  25. Leis JM, McCormick MI (2002) The biology, behavior and ecology of the pelagic, larval stage of coral reef fishes. In Sale PF (ed) Coral reef fishes—dynamics and diversity in a complex ecosystem. Academic Press, London, pp 171—199 Google Scholar
  26. Lemberget T, McCormick MI (2009) Replenishment success linked to fluctuating asymmetry in larval fish. Oecologia 159:8–93CrossRefGoogle Scholar
  27. Lychakov DV, Rebane YT, Lombarte A, Fuiman LA, Takabayashi A (2006) Fish otolith asymmetry: morphometry and modeling. Hear Res 219:1–11PubMedCrossRefGoogle Scholar
  28. McCormick MI (1998) Behaviourally induced maternal stress in a fish influences progeny quality by a hormonal mechanism. Ecology 79:1873–1883CrossRefGoogle Scholar
  29. McCormick MI (1999) Experimental test of the effect of maternal hormones on larval quality of a coral reef fish. Oecologia 118:412–422CrossRefGoogle Scholar
  30. McCormick MI (2006) Mothers matter: crowding leads to stressed mothers and smaller offspring in marine fish. Ecology 87:1104–1109PubMedCrossRefGoogle Scholar
  31. McCormick MI (in press) Indirect effects of heterospecific interactions on progeny quality through maternal stress. Oecologia doi:10.1111/j.1600-0706.2008.17410.x
  32. McCormick Mi, Gagliano M (in press) Carry-over effects: the importance of a good start. Eleventh International Coral Reef SymposiumGoogle Scholar
  33. McCormick MI, Nechaev I (2002) Influence of cortisol on developmental rhythms during embryogenesis in a tropical damselfish. J Exp Zool 293:456–466PubMedCrossRefGoogle Scholar
  34. McCormick MI, Smith SA (2004) Efficacy of passive integrated transponder tags to determine spawning site visitations by a tropical fish. Coral Reefs 23:570–577Google Scholar
  35. Møller AP, Swaddle JP (1997) Asymmetry, developmental stability and evolution. Oxford University Press, OxfordGoogle Scholar
  36. Palmer AR, Strobeck C (1986) Fluctuating asymmetry: measurement, analysis, patterns. Annu Rev Ecol Syst 17:391–421CrossRefGoogle Scholar
  37. Palmer AR, Strobeck C (2003) Fluctuating asymmetry analyses revisited. In: Polak M (ed) Developmental instability (DI): causes and consequences. Oxford University Press, Oxford, pp 279–319Google Scholar
  38. Räsänen K, Kruuk EB (2007) Maternal effects and evolution at ecological time-scales. Funct Ecol 21:408–421CrossRefGoogle Scholar
  39. Rombough PJ (1994) Energy partitioning during fish development: additive or compensatory allocation of energy to support growth? Funct Ecol 8:178–186CrossRefGoogle Scholar
  40. Santos M, Iriarte PF, Cespedes W (2005) Genetics and geometry of canalization and developmental stability in Drosophila subobscura. Evol Biol 5:7–7CrossRefGoogle Scholar
  41. Sokal RR, Rohlf FJ (2001) Biometry. Freeman, New YorkGoogle Scholar
  42. Szisch V, Papandroulakis N, Fanouraki E, Pavlidis M (2005) Ontogeny of the thyroid hormones and cortisol in the gilthead sea bream, Sparus aurata. Gen Comp Endocrinol 142:186–192PubMedCrossRefGoogle Scholar
  43. Weiss SL, Johnston G, Moore MC (2007) Corticosterone stimulates hatching of late-term tree lizard embryos. Comp Biochem Physiol A Mol Integr Physiol 146:360–365PubMedCrossRefGoogle Scholar
  44. Welberg LAM, Seckl JR (2001) Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol 13:113–128PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.School of Marine and Tropical BiologyJames Cook UniversityTownsvilleAustralia
  2. 2.Australian Institute of Marine ScienceTownsville MCAustralia

Personalised recommendations