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Commentary: Parental care and the proximate links between maternal effects and offspring fitness

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Abstract

Maternal effects influence the phenotype of offspring through non-genetic mechanisms, and thus are important components of individual life-histories and act as drivers of and/or constraints on phenotypic evolution. A maternal effect common in egg-laying vertebrates is provisioning of the yolk with carotenoids, organic pigments that often color sexual ornaments and are hypothesized to play positive and substantial physiological roles. In a recent study, yolks of great tit (Parus major) eggs were directly supplemented with carotenoids, and the effects on offspring fitness proxies measured (Marri and Richner in Oecologia 176:371–377, 2014a). Nestlings from supplemented broods were heavier early in development and more likely to fledge, but otherwise equivalent to control nestlings. The authors consider in detail the potential physiological mechanisms that might underlie this result, and here I expand on their Discussion by considering a non-exclusive explanation: that parents provided higher quality care to broods that received supplemental carotenoids. I discuss the general non-independence of pre- and post-hatching/parturition maternal effects when parents care for offspring, and then briefly review evidence that carotenoids specifically are tied to the intensity of avian begging displays. Finally, I detail how inclusive fitness opportunities and constraints shape the adaptive landscape in which maternal effects operate, highlighting both theoretical and applied concerns surrounding questions about the adaptiveness of maternal effects.

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References

  • Berthouly A, Helfenstein F, Richner H (2007) Cellular immune response, stress resistance and competitiveness in nestling great tits in relation to maternally transmitted carotenoids. Funct Ecol 21:335–343

    Article  Google Scholar 

  • Blount JD, Houston DC, Møller AP (2000) Why egg yolk is yellow. Trends Ecol Evol 15:47–49

    Article  PubMed  Google Scholar 

  • Dugas MB (2009) House sparrow (Passer domesticus) parents preferentially feed nestlings with mouth colours that appear carotenoid-rich. Anim Behav 78:767–772

    Article  Google Scholar 

  • Dugas MB (2012) Cross-fostering reveals that among-brood differences in ornamental mouth coloration mostly reflect rearing conditions in nestling house sparrows. Biol J Linn Soc 106:169–179

    Article  Google Scholar 

  • Dugas MB, McGraw KJ (2011) Proximate correlates of carotenoid-based mouth coloration in nestling house sparrows. Condor 111:691–700

    Article  Google Scholar 

  • Dugas MB, Yeager J, Richards-Zawacki CL (2013) Carotenoid supplementation enhances reproductive success in captive strawberry poison frogs (Oophaga pumilio). Zoo Biol 32:655–658

    Article  CAS  PubMed  Google Scholar 

  • Ewen JG, Thorogood R, Karadas F, Cassey P (2008) Condition dependence of nestling mouth colour and the effect of supplementing carotenoids on parental behaviour in the hihi (Notiomystis cincta). Oecologia 157:361–368

    Article  PubMed  Google Scholar 

  • Fitze PS, Tschirren B (2006) No evidence for survival selection on carotenoid-based nestling coloration in great tits (Parus major). J Evol Biol 19:618–624

    Article  CAS  PubMed  Google Scholar 

  • Galvan I, Amo L, Sanz JJ (2008) Ultraviolet–blue reflectance of some nestling patches mediates parental favouritism in great tits Parus major. J Avian Biol 39:277–282

    Article  Google Scholar 

  • Götmark F, Ahlström M (1997) Parental preference for red mouths of chicks in a songbird. Proc R Soc Lond B 264:959–962

    Article  Google Scholar 

  • Griggio M, Morosinotto C, Pilastro A (2009) Nestlings’ carotenoid feather ornament affects parental allocation strategy and reduces maternal survival. J Evol Biol 22:2077–2085

    Article  CAS  PubMed  Google Scholar 

  • Groothuis TGG, Müller W, von Engelhardt N, Carere C, Eising C (2005) Maternal hormone as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev 29:329–352

    Article  CAS  PubMed  Google Scholar 

  • Heeb P, Schwander T, Faoro S (2003) Nestling detectability affects parental feeding preferences in a cavity-nesting bird. Anim Behav 66:637–642

    Article  Google Scholar 

  • Helfenstein F, Berthouly A, Tanner M, Karadas F, Richner H (2008) Nestling begging intensity and parental effort in relation to prelaying carotenoid availability. Behav Ecol 19:108–115

    Article  Google Scholar 

  • Hinde CA, Buchanan KL, Kilner RM (2009) Prenatal environment effects match offspring begging to parental provisioning. Proc R Soc Lond B 276:2787–2794

    Article  Google Scholar 

  • Hunt S, Kilner RM, Langmore NE, Bennett ATD (2003) Conspicuous, ultraviolet-rich mouth colours in begging chicks. Proc R Soc Lond B 270:S25–S28

    Article  Google Scholar 

  • Isaksson C (2009) The chemical pathway of carotenoids: from plants to birds. Ardea 97:125–128

    Article  Google Scholar 

  • Isaksson C, Uller T, Andersson S (2006) Parental effects on carotenoid-based plumage coloration in nestling great tits, Parus major. Behav Ecol Sociobiol 60:556–562

    Article  Google Scholar 

  • Marri V, Richner H (2014a) Yolk carotenoids increase fledging success in great tit nestlings. Oecologia 176:371–377

    Article  PubMed  Google Scholar 

  • Marri V, Richner H (2014b) Differential effects of vitamins E and C and carotenoids on growth, resistance to oxidative stress, fledging success and plumage coloration in wild great tits. J Exp Biol 217:1476–1484

    Article  Google Scholar 

  • Marshall DJ, Uller T (2007) When is a maternal effect adaptive? Oikos 116:1957–1963

    Article  Google Scholar 

  • Mock DW, Parker GA (1997) The evolution of sibling rivalry. Oxford University Press, Oxford

    Google Scholar 

  • Mock DW, Schwagmeyer PL, Parker GA (2005) Male house sparrows deliver more food to experimentally subsidized offspring. Anim Behav 70:225–236

    Article  Google Scholar 

  • Mock DW, Dugas MB, Strickler SA (2011) Honest begging: expanding from signal of need. Behav Ecol 22:909–917

    Article  Google Scholar 

  • Moore AJ, Brodie ED III, Wolf JB (1997) Integrating phenotypes and the evolutionary process: I. Direct and indirect genetic effects of social interactions. Evolution 51:1352–1362

    Article  Google Scholar 

  • Müller W, Lessels CM, Korsten P, von Engelhardt N (2007) Manipulative signals in family conflict? On the function of maternal yolk hormones in birds. Am Nat 169:E84–E96

    Article  PubMed  Google Scholar 

  • Nur N (1984) The consequences of brood size for breeding blue tits I. Adult survival, weight change and the cost of reproduction. J Anim Ecol 53:479–496

    Article  Google Scholar 

  • Remeš V, Krist M, Bertacche V, Stradi R (2007) Maternal carotenoid supplementation does not affect breeding performance in the great tit (Parus major). Funct Ecol 21:776–783

    Article  Google Scholar 

  • Saino N, Ninni P, Calza S, Martinelli R, de Bernardi F, Møller AP (2000) Better red than dead: carotenoid-based mouth colouration reveals infection in barn swallow nestlings. Proc R Soc Lond B 267:57–61

    Article  CAS  Google Scholar 

  • Saino N, Bertacche V, Ferrari RP, Martinelli R, Møller AP, Stradi R (2002) Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proc R Soc Lond B 269:1729–1733

    Article  CAS  Google Scholar 

  • Saino N, Ferrari R, Romano M, Martinelli R, Møller AP (2003) Experimental manipulation of egg carotenoids affects immunity of barn swallow nestlings. Proc R Soc Lond B 270:2485–2489

    Article  Google Scholar 

  • Schwabl H, Lipar J (2002) Hormonal regulation of begging behaviour. In: Wright J, Leonard M (eds) The evolution of begging: competition, cooperation and communication. Kluwer, Dordrecht, pp 221–244

    Chapter  Google Scholar 

  • Svensson PA, Wong BBM (2011) Carotenoid-based signals in behavioural ecology: a review. Behaviour 148:131–189

    Article  Google Scholar 

  • Tanner M, Richner H (2008) Ultraviolet reflectance of plumage for parent-offspring communication in the great tit (Parus major). Behav Ecol 19:369–373

    Article  Google Scholar 

  • Thorogood R, Kilner RM, Karadas F, Ewen JG (2008) Spectral mouth colour of nestlings changes with carotenoid availability. Funct Ecol 22:1044–1051

    Article  Google Scholar 

  • Thorogood R, Ewen JG, Kilner RM (2011) Sense and sensitivity: responsiveness to offspring signals varies with the parents’ potential to breed again. Proc R Soc Lond B 278:2638–2645

    Article  Google Scholar 

  • Tschirren B, Fitze PS, Richner H (2003) Proximate mechanisms of variation in the carotenoid-based plumage coloration of nestling great tits (Parus major L.). J Evol Biol 16:91–100

    Article  CAS  PubMed  Google Scholar 

  • Tschirren B, Fitze PS, Richner H (2005) Carotenoid-based nestling colouration and parental favoritism in the great tit. Oecologia 243:477–482

    Article  Google Scholar 

  • Uller T (2008) Developmental plasticity and the evolution of parental effects. Trends Ecol Evol 23:432–438

    Article  PubMed  Google Scholar 

  • Walker LK, Armstrong DP, Brekke P, Chauvenet ALM, Kilner RM, Ewen JG (2013) Giving hihi a helping hand: assessment of alternative rearing diets in food supplemented populations of an endangered bird. Anim Conserv 16:538–545

    Article  Google Scholar 

  • Wolf JB, Wade MJ (2009) What are maternal effects (and what are they not)? Philos Trans R Soc Lond B 364:1107–1115

    Article  Google Scholar 

Download references

Acknowledgments

Ryan A. Martin, Michael P. Moore, Douglas W. Mock and an anonymous reviewer provided helpful comments that improved this commentary.

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Correspondence to Matthew B. Dugas.

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Communicated by Markku Orell.

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Dugas, M.B. Commentary: Parental care and the proximate links between maternal effects and offspring fitness. Oecologia 177, 1089–1092 (2015). https://doi.org/10.1007/s00442-015-3266-x

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