Hostname: page-component-5d59c44645-jqctd Total loading time: 0 Render date: 2024-03-01T05:45:58.963Z Has data issue: false hasContentIssue false

A model of optimal timing for a predictive adaptive response

Published online by Cambridge University Press:  13 January 2021

Hamish G. Spencer*
Affiliation:
Department of Zoology, University of Otago, Dunedin, New Zealand
Anthony B. Pleasants
Affiliation:
AL Rae Centre for Genetics and Sheep Breeding, Ruakura Research Centre, Massey University, Hamilton, New Zealand
Peter D. Gluckman
Affiliation:
Liggins Institute, University of Auckland, Auckland, New Zealand
Graeme C. Wake
Affiliation:
AL Rae Centre for Genetics and Sheep Breeding, Ruakura Research Centre, Massey University, Hamilton, New Zealand School of Natural and Computational Sciences, Massey University, Auckland, New Zealand
*
Address for correspondence: Hamish G. Spencer, Department of Zoology, University of Otago, Dunedin, New Zealand. Email: hamish.spencer@otago.ac.nz

Abstract

Predictive adaptive responses (PARs) are a form of developmental plasticity in which the developmental response to an environmental cue experienced early in life is delayed and yet, at the same time, the induced phenotype anticipates (i.e., is completely developed before) exposure to the eventual environmental state predicted by the cue, in which the phenotype is adaptive. We model this sequence of events to discover, under various assumptions concerning the cost of development, what lengths of delay, developmental time, and anticipation are optimal. We find that in many scenarios modeled, development of the induced phenotype should be completed at the exact same time that the environmental exposure relevant to the induced phenotype begins: that is, in contrast to our observed cases of PARs, there should be no anticipation. Moreover, unless slow development is costly, development should commence immediately after the cue: there should be no delay. Thus, PARs, which normally have non-zero delays and/or anticipation, are highly unusual. Importantly, the exceptions to these predictions of zero delays and anticipation occurred when developmental time was fixed and delaying development was increasingly costly. We suggest, therefore, that PARs will only evolve under three kinds of circumstances: (i) there are strong timing constraints on the cue and the environmental status, (ii) delaying development is costly, and development time is either fixed or slow development is costly, or (iii) when the period between the cue and the eventual environmental change is variable and the cost of not completing development before the change is high. These predictions are empirically testable.

Type
Original Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Pigliucci, M. Phenotypic Plasticity: Beyond Nature and Nurture, 2001. Johns Hopkins University Press, Baltimore.Google Scholar
West-Eberhard, MJ. Developmental Plasticity and Evolution, 2003. Oxford University Press, New York.CrossRefGoogle Scholar
Moran, NA. The evolutionary maintenance of alternative phenotypes. Am Nat. 1992; 139, 971989.CrossRefGoogle Scholar
Agrawal, AA, Karban, R. Why induced defenses may be favored over constitutive strategies in plants. In The Ecology and Evolution of Inducible Defenses (eds. Tollrian, R, Harvell, CD), 1999; pp. 4561. Princeton University Press, Princeton.Google Scholar
Sultan, SE, Spencer, HG. Metapopulation structure favors plasticity over local adaptation. Am Nat. 2002; 160, 271283.CrossRefGoogle ScholarPubMed
Gabriel, W, Luttbeg, B, Sih, A, Tollrian, R. Environmental tolerance, heterogeneity, and the evolution of reversible plastic responses. Am Nat. 2005; 166, 339353.CrossRefGoogle ScholarPubMed
Padilla, DK, Adolph, SC. Plastic inducible morphologies are not always adaptive: the importance of time delays in a stochastic environment. Evol Ecol. 1996; 10, 105117.CrossRefGoogle Scholar
Panchanathan, K, Frankenhuis, WE. The evolution of sensitive periods in a model of incremental development. Proc R Soc B. 2016; 283, 20152439.CrossRefGoogle Scholar
Hales, CN, Barker, DJP. The thrifty phenotype hypothesis. Brit Med Bull. 2001; 60, 520.CrossRefGoogle ScholarPubMed
Gluckman, PD, Hanson, MA. The developmental origins of the metabolic syndrome. Trends Endocrin Metab. 2004; 15, 183187.CrossRefGoogle ScholarPubMed
Gluckman, PD, Hanson, MA. The Fetal Matrix: Evolution, Development and Disease, 2004. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Gluckman, PD, Hanson, MA, Spencer, HG. Predictive adaptive responses and human evolution. Trends Ecol Evol. 2005; 20, 527533.CrossRefGoogle ScholarPubMed
Bateson, P, Gluckman, PD, Hanson, MA. The biology of developmental plasticity and the Predictive Adaptive Response hypothesis. J Physiol. 2014; 592, 23572368.CrossRefGoogle ScholarPubMed
Lee, TM, Zucker, I. Vole infant development is influenced perinatally by maternal photoperiodic history. Am J Physiol. 1988; 255, R831R838.Google ScholarPubMed
Lee, TM, Spears, N, Tuthill, CR, Zucker, I. Maternal melatonin treatment influences rates of neonatal development of meadow vole pups. Biol Reprod. 1989; 40, 495502.CrossRefGoogle ScholarPubMed
Pener, MP, Yerushalmi, Y. The physiology of locust phase polymorphism: an update. J Insect Physiol. 1998; 44, 365377.CrossRefGoogle ScholarPubMed
Applebaum, SW, Heifetz, Y. Density-Dependent physiological phase in insects. Annu Rev Entomol. 1999; 44, 317341.CrossRefGoogle ScholarPubMed
Forrester, TE, Badaloo, AV, Boyne, MS, et al. Prenatal factors contribute to the emergence of kwashiorkor or marasmus in severe undernutrition: evidence for the predictive adaptation model. PLoS ONE. 2012; 7, e35907.CrossRefGoogle ScholarPubMed
Nettle, D, Frankenhuis, WE, Rickard, IJ. The evolution of predictive adaptive responses in human life history. Proc R Soc B. 2013; 280, 20131343.CrossRefGoogle ScholarPubMed
Rickard, IJ, Frankenhuis, WE, Nettle, D. Why are childhood family factors associated with timing of maturation? A role for internal prediction. Persp Psychol Sci. 2014; 9, 315.CrossRefGoogle ScholarPubMed
DeWitt, TJ, Sih, A, Wilson, DS. Costs and limits of phenotypic plasticity. Trends Ecol Evol. 1998; 13, 7781.CrossRefGoogle ScholarPubMed
Auld, JR, Agrawal, AA, Relyea, RA. Re-Evaluating the costs and limits of adaptive phenotypic plasticity. Proc R Soc B. 2010; 277, 503511.CrossRefGoogle ScholarPubMed
Nishimura, K. Inducible plasticity: optimal waiting time for the development of an inducible phenotype. Evol Ecol Res. 2006; 8, 553559.Google Scholar
Wake, GC, Pleasants, AB, Beadle, A, Gluckman, PD. A model for phenotype change in a stochastic framework. Math Biosci Engin. 2010; 7, 719728.Google Scholar
Scheiner, SM. The genetics of phenotypic plasticity. XII. Temporal and spatial heterogeneity. Ecol Evol. 2013; 3: 45964609 CrossRefGoogle ScholarPubMed
Edelstein-Keshet, L. Mathematical Models in Biology, 1988. McGraw-Hill, Boston.Google Scholar
Kuzawa, CW. Fetal origins of developmental plasticity: are fetal cues reliable predictors of future nutritional environments? Am J Hum Biol. 2005; 17, 521.CrossRefGoogle ScholarPubMed
Kuzawa, CW. Adipose tissue in human infancy and childhood: an evolutionary perspective. Yearbook Phys Anthrop. 1998; 41, 177209.3.0.CO;2-B>CrossRefGoogle Scholar
Mericq, V, Ong, KK, Bazaes, R, et al. Longitudinal changes in insulin sensitivity and secretion from birth to age three years in small- and appropriate-for-gestational-age children. Diabetologia. 2005; 48, 26092614.CrossRefGoogle ScholarPubMed
Supplementary material: File

Spencer et al. supplementary material

Spencer et al. supplementary material

Download Spencer et al. supplementary material(File)
File 688 KB