Early Life Nutrition and the Programming of the Phenotype

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Development Strategies and Biodiversity

Part of the book series: Fascinating Life Sciences ((FLS))

Abstract

Early developmental nutrition profoundly influences phenotypic trajectories and affects adult morphology, physiology, behaviour, longevity and fitness across taxa. During early life, the interplay amongst quantitative (e.g., caloric intake), qualitative (macro- and micronutrient balance) and temporal (nutrient restrictions, predictability) aspects of early diet imposes constraints, as animals seek to balance their nutritional demands to optimise their development. The physiological mechanisms controlling food intake are established during early development, and environmental conditions at this time may play a role in determining long-term fitness. For vertebrates, the physiological axis regulating food intake interacts with the physiological response to environmental stressors and this may induce long-term programming of feeding behaviour and the adult phenotype. The diverse phenotypic and fitness consequences across ontogeny are dependent on both the magnitude and duration of ‘non-optimal’ nutrition during early development, as well as the degree of developmental plasticity in trait development. During early development, nutrition directly, or indirectly, affects cellular proliferation, migration, and differentiation. At this time, the capacity for compensation for periods of nutritional restriction is reduced and there are critical developmental windows of increased susceptibility, with potential for irreversible phenotypic plasticity. Such trait-specific critical windows for nutritional sensitivity may have adaptive explanations, favouring early life plasticity in relation to both environmental cues and environmental predictability. Whether responses to nutritional deficiencies represent developmental constraints or adaptive responses for future environmental conditions is in many cases unclear. Furthermore, transgenerational impacts of early life diet are documented in a small range of species, but the ecological and evolutionary relevance of these effects and capacity for selection on the underlying mechanisms remain uncertain. Future research that seeks to better detail the mechanistic understanding of how complex nutritional trade-offs alter developmental trajectories to specifically influence fitness offers considerable potential to benefit humans and animals, across diverse environmental settings.

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References

  • Adler MI, Cassidy EJ, Fricke C, Bonduriansky R (2013) The lifespan-reproduction trade-off under dietary restriction is sex-specific and context-dependent. Exp Gerontol 48:539–548

    PubMed  Google Scholar 

  • Aiken CE, Ozanne SE (2014) Transgenerational developmental programming. Hum Reprod Update 20:63–75

    PubMed  Google Scholar 

  • Aiken C, Tarry-Adkins J, Ozanne S (2015) Transgenerational developmental programming of ovarian reserve. Sci Rep 5:1–10

    Google Scholar 

  • Al-Chokhachy R, Kovach RP, Sepulveda A, Strait J, Shepard BB, Muhlfeld CC (2019) Compensatory growth offsets poor condition in native trout populations. Freshw Biol 64:2120–2130

    Google Scholar 

  • Allen RM, Marshall DJ (2013) Phenotypic links among life-history stages are complex and context-dependent in a marine invertebrate: interactions among offspring size, larval nutrition and postmetamorphic density. Funct Ecol 27:1358–1366

    Google Scholar 

  • Alonso-Alvarez C, Bertrand S, Faivre B, Sorci G (2007) Increased susceptibility to oxidative damage as a cost of accelerated somatic growth in zebra finches. Funct Ecol 21:873–879

    Google Scholar 

  • Alvarez D, Nicieza AG (2002) Effects of temperature and food quality on anuran larval growth and metamorphosis. Funct Ecol 16:640–648

    Google Scholar 

  • Anderson T, Pond D (2000) Stoichiometric theoryextended to micronutrients: comparison of the rolesof essential fatty acids, carbon, and nitrogen in thenutrition of marine copepods. Limnol Oceanogr 45:1162–1167

    CAS  Google Scholar 

  • Anderson OS, Sant KE, Dolinoy DC (2012) Nutrition and epigenetics: an interplay of dietary methyl donors, one-carbon metabolism and DNA methylation. J Nutr Biochem 23:853–859

    CAS  PubMed  PubMed Central  Google Scholar 

  • Armstrong VL, Brunet PM, He C, Nishimura M, Poole HL, Spector FJ (2006) What is so critical?: A commentary on the reexamination of critical periods. Dev Psychobiol 48:326–331

    PubMed  Google Scholar 

  • Arnold KE, Ramsay SL, Donaldson C, Adam A (2007) Parental prey selection affects risk-taking behaviour and spatial learning in avian offspring. Proc R Soc B Biol Sci 274:2563–2569

    Google Scholar 

  • Auer SK, Arendt JD, Chandramouli R, Reznick DN (2010) Juvenile compensatory growth has negative consequences for reproduction in Trinidadian guppies (Poecilia reticulata). Ecol Lett 13:998–1007

    PubMed  Google Scholar 

  • Auer SK, Salin K, Rudolf AM, Anderson GJ, Metcalfe NB (2015) Flexibility in metabolic rate confers a growth advantage under changing food availability. J Anim Ecol 84:1405–1411

    PubMed  PubMed Central  Google Scholar 

  • Aw WC et al (2018) Genotype to phenotype: diet-by-mitochondrial DNA haplotype interactions drive metabolic flexibility and organismal fitness. PLoS Genet 14

    Google Scholar 

  • Badyaev AV, Foresman KR, Fernandes MV (2000) Stress and developmental stability: vegetation removal causes increased fluctuating asymmetry in shrews. Ecology 81:336–345

    Google Scholar 

  • Bale TL et al (2010) Early life programming and neurodevelopmental disorders. Biol Psychiatry 68:314–319

    PubMed  PubMed Central  Google Scholar 

  • Bardua C et al (2021) Size, microhabitat, and loss of larval feeding drive cranial diversification in frogs. Nat Commun 12:2503

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barker DJ, Gluckman PD, Godfrey KM, Harding JE, Owens JA, Robinson JS (1993) Fetal nutrition and cardiovascular disease in adult life. Lancet 341(8850):938–941. https://doi.org/10.1016/0140-6736(93)91224-a

    Article  CAS  PubMed  Google Scholar 

  • Bateson P, Horn G (1994) Imprinting and recognition memory: a neural net model. Anim Behav 48:695–715

    Google Scholar 

  • Bateson P et al (2004) Developmental plasticity and human health. Nature 430:419–421

    CAS  PubMed  Google Scholar 

  • Beldade P, Mateus ARA, Keller RA (2011) Evolution and molecular mechanisms of adaptive developmental plasticity. Mol Ecol 20:1347–1363

    PubMed  Google Scholar 

  • Bell BA, Phan ML, Meillere A, Evans JK, Leitner S, Vicario DS, Buchanan KL (2018) Influence of early-life nutritional stress on songbird memory formation. Proc R Soc B Biol Sci 285

    Google Scholar 

  • Bender MC, Hu C, Pelletier C, Denver RJ (2018) To eat or not to eat: ontogeny of hypothalamic feeding controls and a role for leptin in modulating life-history transition in amphibian tadpoles Proc R Soc B Biol Sci 285

    Google Scholar 

  • Berghänel A, Heistermann M, Schülke O, Ostner J (2017) Prenatal stress accelerates offspring growth to compensate for reduced maternal investment across mammals. Proc Natl Acad Sci 114:E10658–E10666

    PubMed  PubMed Central  Google Scholar 

  • Bertram C, Khan O, Ohri S, Phillips DI, Matthews SG, Hanson MA (2008) Transgenerational effects of prenatal nutrient restriction on cardiovascular and hypothalamic-pituitary-adrenal function. J Physiol Lond 586:2217–2229

    CAS  PubMed  PubMed Central  Google Scholar 

  • Birkhead T, Fletcher F, Pellatt EJ (1999) Nestling diet, secondary sexual traits and fitness in the zebra finch. Proc R Soc Lond Ser B Biol Sci 266:385–390

    Google Scholar 

  • Bize P, Metcalfe N, Roulin A (2006) Catch-up growth strategies differ between body structures: interactions between age and structure-specific growth in wild nestling Alpine Swifts. Funct Ecol 2006:857–864

    Google Scholar 

  • Bjorndal KA, Bolten AB, Dellinger T, Delgado C, Martins HR (2003) Compensatory growth in oceanic loggerhead sea turtles: response to a stochastic environment. Ecology 84:1237–1249

    Google Scholar 

  • Blanckenhorn WU (2000) The evolution of body size: what keeps organisms small? Q Rev Biol 75:385–407

    CAS  PubMed  Google Scholar 

  • Blount JD, Metcalfe NB, Arnold KE, Surai PF, Devevey GL, Monaghan P (2003a) Neonatal nutrition, adult antioxidant defences and sexual attractiveness in the zebra finch. Proc R Soc B Biol Sci 270:1691–1696

    CAS  Google Scholar 

  • Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003b) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127

    CAS  PubMed  Google Scholar 

  • Boggs CL (2009) Understanding insect life histories and senescence through a resource allocation lens. Funct Ecol 23:27–37

    Google Scholar 

  • Boggs CL, Freeman KD (2005) Larval food limitation in butterflies: effects on adult resource allocation and fitness. Oecologia 144:353–361

    PubMed  Google Scholar 

  • Boggs C, Niitepold K (2016) Effects of larval dietary restriction on adult morphology, with implications for flight and life history. Entomol Exp Appl 159:189–196

    Google Scholar 

  • Boonekamp JJ, Mulder E, Verhulst S (2018) Canalisation in the wild: effects of developmental conditions on physiological traits are inversely linked to their association with fitness. Ecol Lett 21:857–864

    PubMed  Google Scholar 

  • Bornstein MH (1989) Sensitive periods in development: structural characteristics and causal interpretations. Psychol Bull 105:179–197

    CAS  PubMed  Google Scholar 

  • Boswell T, Dunn IC (2015) Regulation of the avian central melanocortin system and the role of leptin. Gen Comp Endocrinol 221:278–283

    CAS  PubMed  Google Scholar 

  • Boswell T, Dunn IC (2017) Regulation of agouti-related protein and pro-opiomelanocortin gene expression in the avian arcuate nucleus Front Endocrinol 13

    Google Scholar 

  • Boyce WT, Sokolowski MB, Robinson GE (2020) Genes and environments, development and time. Proc Natl Acad Sci U S A 117:23235–23241

    CAS  PubMed  PubMed Central  Google Scholar 

  • Breton C (2013) The hypothalamus-adipose axis is a key target of developmental programming by maternal nutritional manipulation. J Endocrinol 216:R19–R31

    CAS  PubMed  Google Scholar 

  • Briga M, Koetsier E, Boonekamp JJ, Jimeno B, Verhulst S (2017) Food availability affects adult survival trajectories depending on early developmental conditions. Proc R Soc B 284:20162287. https://doi.org/10.1098/rspb.2016.2287

    Article  PubMed  PubMed Central  Google Scholar 

  • Brillat-Savarin J (1826) Physiologie du goût: Méditations de gastronomie transcendante, France. https://openlibrary.org/

  • Brust V, Krueger O, Naguib M, Krause ET (2014) Lifelong consequences of early nutritional conditions on learning performance in zebra finches (Taeniopygia guttata). Behav Process 103:320–326

    Google Scholar 

  • Brzęk P, Kohl K, Caviedes-Vidal E, Karasov WH (2009) Developmental adjustments of house sparrow (Passer domesticus) nestlings to diet composition. J Exp Biol 212:1284–1293

    PubMed  Google Scholar 

  • Brzęk P, Lessner KM, Caviedes-Vidal E, Karasov WH (2010) Low plasticity in digestive physiology constrains feeding ecology in diet specialist, zebra finch (Taeniopygia guttata). J Exp Biol 213:798–807

    PubMed  Google Scholar 

  • Brzęk P, Kohl KD, Caviedes-Vidal E, Karasov WH (2011) Fully reversible phenotypic plasticity of digestive physiology in young house sparrows: lack of long-term effect of early diet composition. J Exp Biol 214:2755–2760

    PubMed  Google Scholar 

  • Bubliy OA, Loeschcke V, Imasheva AG (2001) Genetic variation of morphological traits in Drosophila melanogaster under poor nutrition: isofemale lines and offspring–parent regression. Heredity 86:363–369

    CAS  PubMed  Google Scholar 

  • Buchanan KL, Spencer KA, Goldsmith AR, Catchpole CK (2003) Song is an honest signal of past developmental stress in the European starling (Sturnus vulgaris). Proc R Soc B 270:1149–1156

    CAS  PubMed  PubMed Central  Google Scholar 

  • Buchanan KL, Leitner S, Spencer KA, Goldsmith AR, Catchpole CK (2004) Developmental stress selectively affects the song control nucleus HVC in the zebra finch. Proc R Soc B Biol Sci 271:2381–2386

    Google Scholar 

  • Buchanan KL, Grindstaff JL, Pravosudov VV (2013) Condition dependence, developmental plasticity, and cognition: implications for ecology and evolution. Trends Ecol Evol 28:290–296

    PubMed  PubMed Central  Google Scholar 

  • Buescher J, Musselman L, Wilson C, Lang T, Keleher M, Baranski T, Duncan J (2013) Evidence for transgenerational metabolic programming in Drosophila. Dis Model Mech 6:1123–1132

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burggren W (2018) Developmental phenotypic plasticity helps bridge stochastic weather events associated with climate change J Exp Biol 221

    Google Scholar 

  • Burggren WW (2020) Phenotypic switching resulting from developmental plasticity: fixed or reversible? Front Physiol 10:1634

    PubMed  PubMed Central  Google Scholar 

  • Buttstedt A, Ihling CH, Pietzsch M, Moritz RF (2016) Royalactin is not a royal making of a queen. Nature 537:E10–E12

    CAS  PubMed  Google Scholar 

  • Buyannemekh K, Zito JB, Tomaszycki ML (2020) Early life nutritional stress affects song learning but not underlying neural circuitry in zebra finches. Behav Neurosci 134:222–232

    PubMed  Google Scholar 

  • Calkins K, Devaskar SU (2011) Fetal origins of adult disease. Curr Probl Pediatr Adolesc Health Care 41:158–176

    PubMed  PubMed Central  Google Scholar 

  • Candolin U (2000) Changes in expression and honesty of sexual signalling over the reproductive lifetime of sticklebacks. Proc R Soc B Biol Sci 267:2425–2430

    CAS  Google Scholar 

  • Capellan E, Nicieza A (2007) Non-equivalence of growth arrest induced by predation risk or food limitation: context-dependent compensatory growth in anuran tadpoles. J Anim Ecol 76:1026–1035

    CAS  PubMed  Google Scholar 

  • Careau V, Buttemer WA, Buchanan KL (2014) Early-developmental stress, repeatability, and canalization in a suite of physiological and behavioral traits in female zebra finches. Integr Comp Biol 54:539–554

    CAS  PubMed  Google Scholar 

  • Casagrande S, Pinxten R, Zaid E, Eens M (2016) Positive effect of dietary lutein and cholesterol on the undirected song activity of an opportunistic breeder. PeerJ 4:e2512

    PubMed  PubMed Central  Google Scholar 

  • Cassy S, Picard M, Crochet S, Derouet M, Keisler D, Taouis M (2004) Peripheral leptin effect on food intake in young chickens is influenced by age and strain. Domest Anim Endocrinol 27:51–61

    CAS  PubMed  Google Scholar 

  • Catoni C, Peters A, Schaefer H (2008) Life history trade-offs are influenced by the diversity, availability and interactions of dietary antioxidants. Anim Behav 76:1107–1119

    Google Scholar 

  • Chen JH, Cottrell EC, Ozanne SE (2010) Early growth and ageing. Nestle Nutr Workshop Ser Pediatr Program 65:41–54

    PubMed  Google Scholar 

  • Clark RM, Zera AJ, Behmer ST (2015) Nutritional physiology of life-history trade-offs: how food protein–carbohydrate content influences life-history traits in the wing-polymorphic cricket Gryllus firmus. J Exp Biol 218:298–308

    PubMed  Google Scholar 

  • Clinchy M, Zanette L, Boonstra R, Wingfield JC, Smith JNM (2004) Balancing food and predator pressure induces chronic stress in songbirds. Proc R Soc B Biol Sci 271:2473–2479

    Google Scholar 

  • Colombo J (1982) The critical period concept: research, methodology, and theoretical issues. Psychol Bull 91:260–275

    CAS  PubMed  Google Scholar 

  • Cooper EB, Kruuk LEB (2018) Ageing with a silver-spoon: a meta-analysis of the effect of developmental environment on senescence. Evol Lett 2:460–471

    PubMed  PubMed Central  Google Scholar 

  • Costantini D, Angeletti D, Strinati C, Trisolino P, Carlini A, Nascetti G, Carere C (2018) Dietary antioxidants, food deprivation and growth affect differently oxidative status of blood and brain in juvenile European seabass (Dicentrarchus labrax). Comp Biochem Physiol Part A Mol Integr Physiol 216:1–7

    CAS  Google Scholar 

  • Coudrain V, Rittiner S, Herzog F, Tinner W, Entling MH (2016) Landscape distribution of food and nesting sites affect larval diet and nest size, but not abundance of Osmia bicornis. Insect Sci 23:746–753

    PubMed  Google Scholar 

  • Cox L et al (2014) Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell 158:705–721

    CAS  PubMed  PubMed Central  Google Scholar 

  • Crespi EJ, Unkefer MK (2014) Development of food intake controls: neuroendocrine and environmental regulation of food intake during early life. Horm Behav 66:74–85

    CAS  PubMed  Google Scholar 

  • Crespi EJ, Williams TD, Jessop TS, Delehanty B (2013) Life history and the ecology of stress: how do glucocorticoid hormones influence life-history variation in animals? Funct Ecol 27:93–106

    Google Scholar 

  • Cridge AG, Leask MP, Duncan EJ, Dearden PK (2015) What do studies of insect polyphenisms tell us about nutritionally-triggered epigenomic changes and their consequences? Nutrients 7:1787–1797

    CAS  PubMed  PubMed Central  Google Scholar 

  • Criscuolo F, Monaghan P, Nasir L, Metcalfe NB (2008) Early nutrition and phenotypic development: 'catch-up' growth leads to elevated metabolic rate in adulthood. Proc R Soc B Biol Sci 275:1565–1570

    Google Scholar 

  • Cromwell G, Hays V, Overfield J (1970) Effect of dietary ascorbic acid on performance and plasma cholesterol levels of growing swine. J Anim Sci 31:63–66

    CAS  PubMed  Google Scholar 

  • Dallman MF, Strack AM, Akana SF, Bradbury MJ, Hanson ES, Scribner KA, Smith M (1993) Feast and famine - critical role of glucocorticoids with insulin in daily energy-flow. Front Neuroendocrinol 14:303–347

    CAS  PubMed  Google Scholar 

  • Davies LR, Schou MF, Kristensen TN, Loeschcke V (2018) Linking developmental diet to adult foraging choice in Drosophila melanogaster. J Exp Biol 221:jeb175554

    PubMed  Google Scholar 

  • de Ayala R, Martinelli R, Saino N (2006) Vitamin E supplementation enhances growth and condition of nestling barn swallows (Hirundo rustica). Behav Ecol Sociobiol 60:619–630

    Google Scholar 

  • De Block M, Stoks R (2008) Short-term larval food stress and associated compensatory growth reduce adult immune function in a damselfly. Ecol Entomol 33:796–801

    Google Scholar 

  • Deeming D (2004) Post-hatching phenotypic effects of incubation in reptiles. In: Deeming D (ed) Reptilian incubation: environment, evolution and behaviour. Springer, New York, pp 229–251

    Google Scholar 

  • Dehorter N, Del Pino I (2020) Shifting developmental trajectories during critical periods of brain formation. Front Cell Neurosci 14:283

    CAS  PubMed  PubMed Central  Google Scholar 

  • Descamps S, Boutin S, Berteaux D, McAdam AG, Gaillard JM (2008) Cohort effects in red squirrels: the influence of density, food abundance and temperature on future survival and reproductive success. J Anim Ecol 77:305–314

    PubMed  Google Scholar 

  • Diaz-Munoz M, Vazquez-Martinez O, Aguilar-Roblero R, Escobar C (2000) Anticipatory changes in liver metabolism and entrainment of insulin, glucagon, and corticosterone in food-restricted rats. Am J Phys Regul Integr Comp Phys 279:R2048–R2056

    CAS  Google Scholar 

  • Dietrich MO, Horvath TL (2013) Hypothalamic control of energy balance: insights into the role of synaptic plasticity. Trends Neurosci 36:65–73

    CAS  PubMed  Google Scholar 

  • Dmitriew C (2011) The evolution of growth trajectories:what limits growth rate? Biol Rev 86:97–116

    PubMed  Google Scholar 

  • Dobbing J, Sands J (1979) Comparative aspects of the brain growth spurt. Early Hum Dev 3:79–83

    CAS  PubMed  Google Scholar 

  • Dougherty LR (2021) Meta-analysis reveals that animal sexual signalling behaviour is honest and resource based. Nat Ecol Evol 5:688–699

    PubMed  Google Scholar 

  • Douhard M et al (2014) Fitness consequences of environmental conditions at different life stages in a long-lived vertebrate. Proc R Soc B Biol Sci 281:20140276

    Google Scholar 

  • Drent R, Daan S (1980) The prudent parent: energetic adjustments in avian breeding 1. Ardea 55:225–252

    Google Scholar 

  • Dufty AM Jr, Clobert J, Møller AP (2002) Hormones, developmental plasticity and adaptation. Trends Ecol Evol 17:190–196

    Google Scholar 

  • Dunn G, Bale T (2009) Maternal high-fat diet promotes body length increases and insulin insensitivity insecond-generation mice. Endocrinology 150:4999–5009

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duxbury EM, Chapman T (2020) Sex-specific responses of life span and fitness to variation in developmental versus adult diets in Drosophila melanogaster. J Gerontol Ser A 75:1431–1438

    Google Scholar 

  • Elser J (2006) Biological stoichiometry: a chemical bridge between ecosystem ecology and evolutionary biology. Am Nat 168:S25–S35

    PubMed  Google Scholar 

  • Elser J et al (2000) Nutritional constraints interrestrial and freshwater food webs. Nature 408:578–580

    CAS  PubMed  Google Scholar 

  • English S, Barreaux AM (2020) The evolution of sensitive periods in development: insights from insects. Curr Opin Behav Sci 36:71–78

    Google Scholar 

  • English S, Uller T (2016) Does early-life diet affect longevity? A meta-analysis across experimental studies. Biol Lett 12:20160291

    PubMed  PubMed Central  Google Scholar 

  • English S, Fawcett TW, Higginson AD, Trimmer PC, Uller T (2016) Adaptive use of information during growth can explain long-term effects of early life experiences. Am Nat 187:620–632

    PubMed  Google Scholar 

  • Fagiolini M, Jensen CL, Champagne FA (2009) Epigenetic influences on brain development and plasticity. Curr Opin Neurobiol 19:207–212

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fanson B, Taylor P (2012) Protein:carbohydrate ratios explain life span patterns found in Queensland fruit fly on diets varying in yeast:sugar ratios. Age 34:1361–1368

    CAS  PubMed  Google Scholar 

  • Farrell T, Kriengwatana B, MacDougall-Shackleton SA (2015) Developmental stress and correlated cognitive traits in songbirds. Comp Cogn Behav Rev 10:1–23

    Google Scholar 

  • Farrell TM, Morgan A, MacDougall-Shackleton SA (2016) Developmental stress impairs performance on an association task in male and female songbirds, but impairs auditory learning in females only. Anim Cogn 19:1–14

    PubMed  Google Scholar 

  • Fauchald P, Tveraa T, Henaug C, Yoccoz N (2004) Adaptive regulation of body reserves in reindeer, Rangifer tarandus: a feeding experiment. Oikos 107:583–591

    Google Scholar 

  • Faulk C, Dolinoy DC (2011) Timing is everything: the when and how of environmentally induced changes in the epigenome of animals. Epigenetics 6:791–797

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fawcett TW, Frankenhuis WE (2015) Adaptive explanations for sensitive windows in development. Front Zool 12:S3

    PubMed  PubMed Central  Google Scholar 

  • Ferreira A, Milán M (2015) Dally proteogly can mediates the autonomous and nonautonomous effects on tissue growth caused by activation of the PI3K and TOR pathways. PLoS Biol 13:e1002239

    PubMed  PubMed Central  Google Scholar 

  • Fisher MC, Zeisel SH, Mar MH, Sadler TW (2002) Perturbations in choline metabolism cause neural tube defects in mouse embryos in vitro. FASEB J 16:619–621

    CAS  PubMed  Google Scholar 

  • Fisher MO, Nager RG, Monaghan P (2006) Compensatory growth impairs adult cognitive performance. PLoS Biol 4:1462–1466

    CAS  Google Scholar 

  • Flatt T (2005) The evolutionary genetics of canalization. Q Rev Biol 80:287–316

    PubMed  Google Scholar 

  • Flatt T (2020) Life-history evolution and the genetics of fitness components in Drosophila melanogaster. Genetics 214:3–48

    CAS  PubMed  Google Scholar 

  • Fokidis HB, Roziers MBD, Sparr R, Rogowski C, Sweazea K, Deviche P (2012) Unpredictable food availability induces metabolic and hormonal changes independent of food intake in a sedentary songbird. J Exp Biol 215:2920–2930

    PubMed  Google Scholar 

  • Fontana L, Partridge L, Longo VD (2010) Dietary restriction, growth factors and aging: from yeast to humans. Science 328:321–326

    CAS  PubMed  PubMed Central  Google Scholar 

  • Forgie AJ, Drall KM, Bourque SL, Field CJ, Kozyrskyj AL, Willing BP (2020) The impact of maternal and early life malnutrition on health: a diet-microbe perspective. BMC Med 18:135

    PubMed  PubMed Central  Google Scholar 

  • Frankenhuis W, Fraley C (2017) What do evolutionary models teach us about sensitive periods in psychological development? Eur Psychol 22:141–150

    Google Scholar 

  • Frankenhuis WE, Walasek N (2020) Modeling the evolution of sensitive periods. Dev Cogn Neurosci 41:100715

    PubMed  Google Scholar 

  • Fretham SJB, Carlson ES, Wobken J, Tran PV, Petryk A, Georgieff MK (2012) Temporal manipulation of transferrin-receptor-1-dependent iron uptake identifies a sensitive period in mouse hippocampal neurodevelopment. Hippocampus 22:1691–1702

    CAS  PubMed  PubMed Central  Google Scholar 

  • Friedman JM (2009) Leptin at 14 y of age: an ongoing story. Am J Clin Nutr 89:973S–979S

    CAS  PubMed  PubMed Central  Google Scholar 

  • Friedman-Einat M, Eyal Seroussi E (2019) Avian leptin: bird’s-eye view of the evolution of vertebrate energy-balance control. Trends Endocrinol Metab 30:819–832

    CAS  PubMed  Google Scholar 

  • Frydlova P et al (2020) Determinate growth is predominant and likely ancestral in squamate reptiles. Proc R Soc B Biol Sci 287:20202737

    Google Scholar 

  • Fuentealba A, Bauce É (2012) Carry-over effect of host nutritional quality on performance of spruce budworm progeny. Bull Entomol Res 102:275–284

    CAS  PubMed  Google Scholar 

  • Gaillard J-M, Loison A, ToÏgo C, Delorme D, Van Laere G (2003) Cohort effects and deer population dynamics. Ecoscience 10:412–420

    Google Scholar 

  • Gawne R, McKenna KZ, Levin M (2020) Competitive and coordinative interactions between body parts produce adaptive developmental outcomes. BioEssays 42:e1900245

    PubMed  Google Scholar 

  • Georgieff M, Brunette K, Tran P (2015) Early life nutrition and neural plasticity. Dev Psychopathol 27:411–423

    PubMed  PubMed Central  Google Scholar 

  • Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407

    Google Scholar 

  • Gilbert S (2001) Ecological developmental biology: developmental biology meets the real world. Dev Biol 233:1–12

    CAS  PubMed  Google Scholar 

  • Gluckman PD, Hanson MA (2004) Living with the past: evolution, development, and patterns of disease. Science 305:1733–1736

    CAS  PubMed  Google Scholar 

  • Gluckman P, Hanson M (2006) The conceptual basis for the developmental origins of health and disease. In: Gluckman P, Hanson M (eds) Developmental origins of health and disease. CUP, Cambridge, pp 33–50

    Google Scholar 

  • Gluckman PD, Hanson MA, Spencer HG (2005) Predictive adaptive responses and human evolution. Trends Ecol Evol 20:527–533

    PubMed  Google Scholar 

  • Gluckman PD, Hanson MA, Low FM (2011) The role of developmental plasticity and epigenetics in human health. Birth Defects Res C Embryo Tod Rev 93:12–18

    CAS  Google Scholar 

  • Gniuli D, Calcagno A, Caristo ME, Mancuso A, Macchi V, Mingrone G, Vettor R (2008) Effects of high-fat diet exposure during fetal life on type 2 diabetes development in the progeny. J Lipid Res 49:1936–1945

    CAS  PubMed  Google Scholar 

  • Goldstein E, Sponaugle S (2020) Juvenile reef fish growth and survival related to subregional patterns of primary production. Mar Biol 167:1–10

    Google Scholar 

  • Gonzalez PN, Lotto FP, Hallgrímsson B (2014) Canalization and developmental instability of the fetal skull in a mouse model of maternal nutritional stress. Am J Phys Anthropol 154:544–553

    PubMed  PubMed Central  Google Scholar 

  • Gonzalez PN, Gasperowicz M, Barbeito-Andres J, Klenin N, Cross JC, Hallgrimsson B (2016) Chronic protein restriction in mice impacts placental function and maternal body weight before fetal growth. PLoS One 11

    Google Scholar 

  • Goodship N, Buchanan K (2006) Nestling testosterone is associatedwith begging behaviour and fledging success in the pied flycatcher, Ficedula hypoleuca. Proc R Soc B Biol Sci 273:71–76

    CAS  Google Scholar 

  • Goymann W, Lupi S, Kaiya H, Cardinale M, Fusani L (2017) Ghrelin affects stopover decisions and food intake in a long-distance migrant. Proc Natl Acad Sci U S A 114:1946–1951

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grafen A (1988) On the uses of data on lifetime reproductive success. In: Clutton-Brock T (ed) Reproductive success. University of Chicago Press, Chicago, pp 454–471

    Google Scholar 

  • Gray DA, Eckhardt G (2001) Is cricket courtship song condition dependent? Anim Behav 62:871–877

    Google Scholar 

  • Grieg-Smith P (1982) Song-rates and parental care by individual male stonechats (Saxicola torquata). Anim Behav 30:245–252

    Google Scholar 

  • Grove K, Allen S, Grayson B, Smith M (2003) Postnatal development of the hypothalamic neuropeptide Y system. Neuroscience 1116:393–406

    Google Scholar 

  • Grove K, Grayson B, Glavas M, **ao X, Smith M (2005) Development of metabolic systems. Physiol Behav 86:646–660

    CAS  PubMed  Google Scholar 

  • Guzman C, Cabrera R, Cardenas M, Larrea F, Nathanielsz PW, Zambrano E (2006) Protein restriction during fetal and neonatal development in the rat alters reproductive function and accelerates reproductive ageing in female progeny. J Physiol Lond 572:97–108

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hales CN, Barker DJ (1992) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35:595–601

    CAS  PubMed  Google Scholar 

  • Hales CN, Barker DJ (2001) The thrifty phenotype hypothesis. Br Med Bull 60:5–20

    CAS  PubMed  Google Scholar 

  • Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, Osmond C, Winter PD (1991) BMJ 303(6809):1019–1022. https://doi.org/10.1136/bmj.303.6809.1019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall ME, Blount JD, Forbes S, Royle NJ (2010) Does oxidative stress mediate the trade-off between growth and self-maintenance in structured families? Funct Ecol 24:365–373

    Google Scholar 

  • Han J-H et al (2007) Neuronal competition and selection during memory formation. Science 316:457–460

    CAS  PubMed  Google Scholar 

  • Hanson M, Gluckman P (2014) Early developmental conditioning of later health and disease: physiology or pathophysiology? Physiol Rev 94:1027–1076

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison XA, Blount JD, Inger R, Norris DR, Bearhop S (2011) Carry-over effects as drivers of fitness differences in animals. J Anim Ecol 80:4–18

    PubMed  Google Scholar 

  • Harrison S, Raubenheimer D, Simpson S, Godin J-GJ, Bertram S (2014) Towards a synthesis of frameworks in nutritional ecology: interacting effects of protein, carbohydrate and phosphorus on field cricket fitness. Proc R Soc B Biol Sci 281:20140539

    Google Scholar 

  • Hawlena D, Schmitz O (2010) Herbivore physiological response to predation risk and implications for ecosystem nutrient dynamics. Proc Natl Acad Sci 107:15503–15507

    CAS  PubMed  PubMed Central  Google Scholar 

  • Haywood S, Perrins CM (1992) Is clutch size in birds affected by environmental conditions during growth? Proc R Soc Lond Ser B Biol Sci 249:195–197

    CAS  Google Scholar 

  • Hayward AD, Rickard IJ, Lummaaa V (2013) Influence of early-life nutrition on mortality and reproductive success during a subsequent famine in a preindustrial population. Proc Natl Acad Sci U S A 110(34):13886–13891

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hector KL, Nakagawa S (2012) Quantitative analysis of compensatory and catch-up growth in diverse taxa. J Anim Ecol 81:583–593

    PubMed  Google Scholar 

  • Hector K, Bishop P, Nakagawa S (2012) Consequences of compensatory growth in an amphibian. J Zool 286:93–101

    Google Scholar 

  • Heijmans BT et al (2008) Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A 105:17046–17049

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heilbronn L, Ravussin E (2003) Calorie restriction and aging: review of the literature and implications for studies in humans. Am J Clin Nutr 78:361–369

    CAS  PubMed  Google Scholar 

  • Heissenberger S, de Pinho GM, Martin JG, Blumstein DT (2020) Age and location influence the costs of compensatory and accelerated growth in a hibernating mammal. Behav Ecol 31:826–833

    Google Scholar 

  • Hensch T (2004) Critical period regulation. Annu Rev Neurosci 27:549–579

    CAS  PubMed  Google Scholar 

  • Hibshman JD, Hung A, Baugh LR (2016) Maternal diet and insulin-like signaling control intergenerational plasticity of progeny size and starvation resistance. PLoS Genet 12:e1006396

    PubMed  PubMed Central  Google Scholar 

  • Hoffmann A (2003) Associating environmental stress with developmental stability: problems and patterns. In: Polak M (ed) Developmental instability: causes and consequences. OUP, New York, pp 387–401

    Google Scholar 

  • Hoffmann A, Woods R (2001) Trait variability and stress: canalization, developmental stability and the need for a broad approach. Ecol Lett 4:97–101

    Google Scholar 

  • Hoffmann AA, Woods RE, Collins E, Wallin K, White A, McKenzie JA (2005) Wing shape versus asymmetry as an indicator of changing environmental conditions in insects. Aust J Entomol 44:233–243

    Google Scholar 

  • Honarmand M, Goymann W, Naguib M (2010) Stressful dieting: nutritional conditions but not compensatory growth elevate corticosterone levels in zebra finch nestlings and fledglings. PLoS One 5:e12930

    PubMed  PubMed Central  Google Scholar 

  • Honarmand M, Thompson CK, Schatton A, Kipper S, Scharff C (2016) Early developmental stress negatively affects neuronal recruitment to avian song system nucleus HVC. Dev Neurobiol 76:107–118

    PubMed  Google Scholar 

  • Hooper AK, Spagopoulou F, Wylde Z, Maklakov AA, Bonduriansky R (2017) Ontogenetic timing as a condition-dependent life history trait: high-condition males develop quickly, peak early, and age fast. Evolution 71:671–685

    PubMed  Google Scholar 

  • Hopwood PE, Moore AJ, Royle NJ (2014) Effects of resource variation during early life and adult social environment on contest outcomes in burying beetles: a context-dependent silver spoon strategy? Proc R Soc B Biol Sci 281:20133102

    Google Scholar 

  • Hoshizaki S (2019) Catch-up growth in the rhinoceros beetle Trypoxylus dichotomus (Coleoptera: Scarabaeidae): smaller neonates gain relatively more body mass during larval development. Entomol Sci 22:373–380

    Google Scholar 

  • Hou ZX, Fuiman LA (2020) Nutritional programming in fishes: insights from mammalian studies. Rev Fish Biol Fish 30:67–92

    Google Scholar 

  • Houslay TM, Hunt J, Tinsley MC, Bussiere LF (2015) Sex differences in the effects of juvenile and adult diet on age-dependent reproductive effort. J Evol Biol 28:1067–1079

    CAS  PubMed  Google Scholar 

  • Howells RJ et al (2017) From days to decades: short-and long-term variation in environmental conditions affect offspring diet composition of a marine top predator. Mar Ecol Prog Ser 583:227–242

    Google Scholar 

  • Hu F, Crespi E, Denver R (2008) Programming neuroendocrine stress axis activity by exposure to glucocorticoids during postembryonic development of the frog Xenopus laevis. Endocrinology 149:5470–54781

    CAS  PubMed  Google Scholar 

  • Hullar M, Fu B (2014) Diet, the gut microbiome, and epigenetics. Cancer J 20:170–175

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hunt J, Brooks R, Jennions MD, Smith MJ, Bentsen CL, Bussiere LF (2004) High-quality male field crickets invest heavily in sexual display but die young. Nature 432:1024–1027

    CAS  PubMed  Google Scholar 

  • Hunt J, Brooks RC, Jennions M (2005) Female mate choice as a condition-dependent life-history trait. Am Nat 166(1):79–92

    PubMed  Google Scholar 

  • Isler K, Van Schaik CP (2006) Metabolic costs of brain size evolution. Biol Lett 2:557–560

    PubMed  PubMed Central  Google Scholar 

  • Jennings B, Ozanne S, Dorling M, Hales C (1999) Early growth determines longevity in male rats and may be related to telomere shortening in the kidney. FEBS Lett 448:4–8

    CAS  PubMed  Google Scholar 

  • Jennions MD, Moller AP, Petrie M (2001) Sexually selected traits and adult survival: a meta-analysis. Q Rev Biol 76:3–36

    CAS  PubMed  Google Scholar 

  • Jesperen L, Toft S (2003) Compensatory growth following early nutritional stress in the Wolf Spider Pardosa prativaga. Funct Ecol 17:737–746

    Google Scholar 

  • Jimenez-Chillaron JC, Ramon-Krauel M, Ribo S, Diaz R (2016) Transgenerational epigenetic inheritance of diabetes risk as a consequence of early nutritional imbalances. Proc Nutr Soc 75:78–89

    PubMed  Google Scholar 

  • Johnson MH (2005) Sensitive periods in functional brain development: problems and prospects. Dev Psychobiol 46:287–292

    PubMed  Google Scholar 

  • Johnson H, Solensky M, Satterfield D, Davis A (2014) Does skip** a meal matter to a butterfly’s appearance? Effects of larval food stress on wing morphology and color in monarch butterflies. PLoS One 9:e93492

    PubMed  PubMed Central  Google Scholar 

  • Joy TK, Arik AJ, Corby-Harris V, Johnson AA, Riehle MA (2010) The impact of larval and adult dietary restriction on lifespan, reproduction and growth in the mosquito Aedes aegypti. Exp Gerontol 45:685–690

    PubMed  PubMed Central  Google Scholar 

  • Judge KA, Ting JJ, Gwynne DT (2008) Condition dependence of male life span and calling effort in a field cricket. Evolution 62:868–878

    PubMed  Google Scholar 

  • Judge KA, Ting JJ, Gwynne DT (2014) Condition dependence of female choosiness in a field cricket. J Evol Biol 27(11):2529–2540

    CAS  PubMed  Google Scholar 

  • Kacelnik A, Cotton PA, Stirling L, Wright J (1995) Food allocation among nestling starlings: sibling competition and the scope of parental choice. Proc R Soc Lond Ser B Biol Sci 259:259–263

    Google Scholar 

  • Kasomovic M (2013) The multidimensional consequences of the juvenile environment: towards an integrative view of the adult phenotype. Anim Behav 85:1049–1059

    Google Scholar 

  • Kaspi R, Mossinson S, Drezner T, Kamensky B, Yuval B (2002) Effects of larval diet on development rates and reproductive maturation of male and female Mediterranean fruit flies. Physiol Entomol 27:29–38

    Google Scholar 

  • Kasumovic MM (2013) The multidimensional consequences of the juvenile environment: towards an integrative view of the adult phenotype. Anim Behav 85:1049–1059

    Google Scholar 

  • Kasumovic MM, Andrade MC (2006) Male development tracks rapidly shifting sexual versus natural selection pressures. Curr Biol 16:R242–R243

    CAS  PubMed  Google Scholar 

  • Kasumovic MM, Brooks RC, Andrade MC (2009) Body condition but not dietary restriction prolongs lifespan in a semelparous capital breeder. Biol Lett 5:636–638

    PubMed  PubMed Central  Google Scholar 

  • Kelly C, Neyer A, Gress B (2014) Sex-specific life history responses to nymphal diet quality and immune status in a field cricket. J Evol Biol 27:381–390

    CAS  PubMed  Google Scholar 

  • Kitaysky A, Kitaiskaia E, Wingfield J, Piatt J (2001a) Dietary restriction causes chronic elevation of corticosterone and enhances stress response in red-legged kittiwake chicks. J Comp Physiol B 171:701–709

    CAS  PubMed  Google Scholar 

  • Kitaysky A, Wingfield J, Piatt J (2001b) Corticosterone facilitates begging and affects resource allocation in the black-legged kittiwake. Behav Ecol 12:619–625

    Google Scholar 

  • Kitaysky AS, Kitaiskaia EV, Piatt JF, Wingfield JC (2006) A mechanistic link between chick diet and decline in seabirds? Proc R Soc B Biol Sci 273:445–450

    CAS  Google Scholar 

  • Klingenberg CP (2019) Phenotypic plasticity, developmental instability, and robustness: the concepts and how they are connected. Front Ecol Evol 7. https://doi.org/10.3389/fevo.2019.00056

  • Koyama T, Mirth CK (2018) Unravelling the diversity of mechanisms through which nutrition regulates body size in insects. Curr Opin Insect Sci 25:1–8

    PubMed  Google Scholar 

  • Krause ET, Naguib M (2011) Compensatory growth affects exploratory behaviour in zebra finches, Taeniopygia guttata. Anim Behav 81:1295–1300

    Google Scholar 

  • Krause E, Honarmand M, Wetzel K, Naguib M (2009) Early fasting is long lasting: differences in early nutritional conditions reappear under stressful conditions in adult female zebra finches. PLoS One 4:e5015

    PubMed  PubMed Central  Google Scholar 

  • Kriengwatana B, MacDougall-Shackleton SA (2015) No trade-offs between lipid stores and structural growth in juvenile zebra finches undergoing nutritional stress during development. Physiol Biochem Zool 88:208–215

    PubMed  Google Scholar 

  • Kriengwatana B, Wada H, Macmillan A, MacDougall-Shackleton SA (2013) Juvenile nutritional stress affects growth rate, adult organ mass, and innate immune function in zebra finches (Taeniopygia guttata). Physiol Biochem Zool 86:769–781

    PubMed  Google Scholar 

  • Kriengwatana B, Wada H, Schmidt K, Taves M, Soma K, MacDougall-Shackleton S (2014) Effects of nutritional stress during different developmental periods on song and the hypothalamic-pituitary-adrenal axis in zebra finches. Horm Behav 65:285–293

    CAS  PubMed  Google Scholar 

  • Kriengwatana B, Farrell T, Aitken S, Garcia L, MacDougall-Shackleton S (2015) Early-life nutritional stress affects associative learning and spatial memory but not performance on a novel object test. Behaviour 152:195–218

    Google Scholar 

  • Krittika S, Lenka A, Yadav P (2019) Evidence of dietary protein restriction regulating pupation height, development time and lifespan in Drosophila melanogaster. Biol Open 8:bio042952

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kupferberg SJ (1997) The role of larval diet in anuran metamorphosis. Am Zool 37:146–159

    CAS  Google Scholar 

  • Langley-Evans SC (2009) Nutritional programming of disease: unravelling the mechanism. J Anat 215:36–51

    PubMed  Google Scholar 

  • Langley-Evans S (2015) Nutrition in early life and the programming of adult disease: a review. J Hum Nutr Diet 28:1–14

    PubMed  Google Scholar 

  • Langley-Evans SC, Sculley DV (2006) The association between birthweight and longevity in the rat is complex and modulated by maternal protein intake during fetal life. FEBS Lett 580:4150–4153

    CAS  PubMed  Google Scholar 

  • Lee KP, Jang T (2014) Exploring the nutritional basis of starvation resistance in D rosophila melanogaster. Funct Ecol 28:1144–1155

    Google Scholar 

  • Lee KP et al (2008) Lifespan and reproduction in Drosophila: new insights from nutritional geometry. Proc Natl Acad Sci 105:2498–2503

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee P, Kwon S-T, Roh C (2012) Caterpillars use developmental plasticity and diet choice to overcome the early life experience of nutritional imbalance. Anim Behav 84:785–793

    Google Scholar 

  • Lee KP, Kim J-S, Min K-J (2013) Sexual dimorphism in nutrient intake and life span is mediated by mating in Drosophila melanogaster. Anim Behav 86:987–992

    Google Scholar 

  • Leimar O, Karlsson B, Wiklund C (1994) Unpredictable food and sexual size dimorphism in insects. Proc R Soc B Biol Sci 258:121–125

    CAS  Google Scholar 

  • Leonhardt M, Lesage J, Croix D, Dutriez-Casteloot I, Beauvillain J, Dupouy J (2003) Effects of perinatal maternal food restriction on pituitary-gonadal axis and plasma leptin level in rat pup at birth and weaning and on timing of puberty. Biol Reprod 68:390–400

    CAS  PubMed  Google Scholar 

  • Lessells C (2002) Parentally biased favouritism: why should parents specialize in caring for different offspring? Philos Trans R Soc Lond B Biol Sci 357:381–403

    CAS  PubMed  PubMed Central  Google Scholar 

  • Levin B (2006) Metabolic imprinting: critical impact of the perinatal environment on the regulation of energy homeostasis. Philos Trans R Soc Lond 361:1107–1121

    CAS  Google Scholar 

  • Levine S (1967) Maternal and environmental influences on adrenocortical responses to stress in weanling rats. Science 156:258–260

    CAS  PubMed  Google Scholar 

  • Levine S (2005) Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrinology 30:939–946

    PubMed  Google Scholar 

  • Li CCY, Maloney CA, Cropley JE, Suter CM (2010) Epigenetic programming by maternal nutrition: sha** future generations. Epigenomics 2:539–549

    CAS  PubMed  Google Scholar 

  • Li Y et al (2011) Exposure to the Chinese famine in early life and the risk of metabolic syndrome in adulthood. Diabetes Care 34:1014–1018

    PubMed  PubMed Central  Google Scholar 

  • Lindsay E, Metcalfe N, Llewellyn M (2019) The potential role of the gut microbiota in sha** host energetics and metabolic rate. J Anim Ecol 89:2415–2426

    Google Scholar 

  • Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348

    PubMed  Google Scholar 

  • Longo VD, Di Tano M, Mattson MP, Guidi N (2021) Intermittent and periodic fasting, longevity and disease. Nat Aging 1:47–59

    PubMed  PubMed Central  Google Scholar 

  • Lucas A (1991) Programming by early nutrition in man. CIBA Found Symp 156:38–50

    CAS  PubMed  Google Scholar 

  • Lucassen PJ, Naninck EFG, van Goudoever JB, Fitzsimons C, Joels M, Korosi A (2013) Perinatal programming of adult hippocampal structure and function; emerging roles of stress, nutrition and epigenetics. Trends Neurosci 36:621–631

    CAS  PubMed  Google Scholar 

  • Lumeng CN, Saltiel AR (2011) Inflammatory links between obesity and metabolic disease. J Clin Investig 121:2111–2117

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lumey LH, Khalangot MD, Vaiserman AM (2015) Association between type 2 diabetes and prenatal exposure to the Ukraine famine of 1932-33: a retrospective cohort study. Lancet Diabetes Endocrinol 3:787–794

    CAS  PubMed  Google Scholar 

  • Lynn SE, Breuner CW, Wingfield JC (2003) Short-term fasting affects locomotor activity, corticosterone, and corticosterone binding globulin in a migratory songbird. Horm Behav 43:150–157

    CAS  PubMed  Google Scholar 

  • MacDonald IF, Kempster B, Zanette L, MacDougall-Shackleton SA (2006) Early nutritional stress impairs development of a song-control brain region in both male and female juvenile song sparrows (Melospiza melodia) at the onset of song learning. Proc R Soc B Biol Sci 273:2559–2564

    Google Scholar 

  • Madsen T, Shine R (2000) Silver spoons and snake body sizes: prey availability early in life influences long-term growth rates of free-ranging pythons. J Anim Ecol 69:952–958

    Google Scholar 

  • Magoolagan L, Mawby PJ, Whitehead FA, Sharp SP (2018) The effect of early life conditions on song traits in male dippers (Cinclus cinclus). PLoS One 13. https://doi.org/10.1371/journal.pone.0205101

  • Maklakov AA et al (2008) Sex-specific fitness effects of nutrient intake on reproduction and lifespan. Curr Biol 18:1062–1066

    CAS  PubMed  Google Scholar 

  • Marasco V, Boner W, Griffiths K, Heidinger B, Monaghan P (2018) Environmental conditions shape the temporal pattern of investment in reproduction and survival. Proc R Soc Lond B 285:20172442

    Google Scholar 

  • Marín O (2016) Developmental timing and critical windows for the treatment of psychiatric disorders. Nat Med 22:1229–1238

    PubMed  Google Scholar 

  • Marshall DJ, Morgan SG (2011) Ecological and evolutionary consequences of linked life-history stages in the sea. Curr Biol 21:R718–R725

    CAS  PubMed  Google Scholar 

  • Marshall DJ, Burgess SC, Connallon T (2016) Global change, life-history complexity and the potential for evolutionary rescue. Evol Appl 9:1189–1201

    PubMed  PubMed Central  Google Scholar 

  • Martínez D et al (2014) In utero undernutrition in male mice programs liver lipid metabolism in the second-generation offspring involving altered Lxra DNA methylation. Cell Metab 19:941–951

    PubMed  Google Scholar 

  • Martin-Gronert MS, Tarry-Adkins JL, Cripps RL, Chen JH, Ozanne SE (2008) Maternal protein restriction leads to early life alterations in the expression of key molecules involved in the aging process in rat offspring. Am J Phys Regul Integr Comp Phys 294:R494–R500

    CAS  Google Scholar 

  • Masoro EJ (2005) Overview of caloric restriction and ageing. Mech Ageing Dev 126:913–922

    CAS  PubMed  Google Scholar 

  • Masuyama H, Mitsui T, Nobumoto E, Hiramatsu Y (2015) The effects of high-fat diet exposure in utero on the obesogenic and diabetogenic traits through epigenetic changes in adiponectin and leptin gene expression for multiple generations in female mice. Endocrinology 156:2482–2491

    CAS  PubMed  Google Scholar 

  • Matthews SG (2002) Early programming of the hypothalamo-pituitary-adrenal axis. Trends Endocrinol Metab 13:373–380

    CAS  PubMed  Google Scholar 

  • Maurange C, Lanet E (2014) Building a brain under nutritional restriction: insights on sparing and plasticity from Drosophila studies. Front Physiol 5:117

    PubMed  PubMed Central  Google Scholar 

  • Mautz BS, Rode NO, Bonduriansky R, Rundle HD (2019) Comparing ageing and the effects of diet supplementation in wild vs. captive antler flies, Protopiophila litigata. J Anim Ecol 88:1913–1924

    PubMed  Google Scholar 

  • May CM, Doroszuk A, Zwaan BJ (2015) The effect of developmental nutrition on life span and fecundity depends on the adult reproductive environment in Drosophila melanogaster. Ecol Evol 5:1156–1168

    PubMed  PubMed Central  Google Scholar 

  • McCay C, Crowell M, Maynard L (1935) The effect of retarded growth upon the length of life span and upon the ultimate body size: one figure. J Nutr 10:63–79

    CAS  Google Scholar 

  • McCue MD (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol A Mol Integr Physiol 156:1–18

    PubMed  Google Scholar 

  • McGowan P, Meaney M, Szyf M (2008) Diet and the epigenetic (re)programming of phenotypic differences in behavior. Brain Res 1237:12–24

    CAS  PubMed  PubMed Central  Google Scholar 

  • McMillen IC, Robinson JS (2005) Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 85:571–633

    CAS  PubMed  Google Scholar 

  • Meaney M (2001) Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24:1161–1192

    CAS  PubMed  Google Scholar 

  • Meaney MJ, Szyf M, Seckl JR (2007) Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends Mol Med 13:269–277

    CAS  PubMed  Google Scholar 

  • Meck WH, Williams CL (2003) Metabolic imprinting of choline by its availability during gestation: implications for memory and attentional processing across the lifespan. Neurosci Biobehav Rev 27:385–399

    CAS  PubMed  Google Scholar 

  • Meck W, Smith R, Williams C (1988) Prenatal and postnatal choline supplementation produced long-term facilitation of spatial memory. Dev Psychobiol 21:339–353

    CAS  PubMed  Google Scholar 

  • Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260

    PubMed  Google Scholar 

  • Metcalfe NB, Monaghan P (2003) Growth versus lifespan: perspectives from evolutionary ecology. Exp Gerontol 38:935–940

    PubMed  Google Scholar 

  • Michel GF, Tyler AN (2005) Critical period: a history of the transition from questions of when, to what, to how. Dev Psychobiol 46:156–162

    PubMed  Google Scholar 

  • Milton CC, Huynh B, Batterham P, Rutherford SL, Hoffmann AA (2003) Quantitative trait symmetry independent of Hsp90 buffering: distinct modes of genetic canalization and developmental stability. Proc Natl Acad Sci 100:13396–13401

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moatt JP, Savola E, Regan JC, Nussey DH, Walling CA (2020) Lifespan extension via dietary restriction: time to reconsider the evolutionary mechanisms? BioEssays 42:1900241

    Google Scholar 

  • Moczek AP et al (2011) The role of developmental plasticity in evolutionary innovation. Proc R Soc B Biol Sci 278:2705–2713

    Google Scholar 

  • Molteni R, Barnard RJ, Ying Z, Roberts CK, Gomez-Pinilla F (2002) A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience 112:803–814

    CAS  PubMed  Google Scholar 

  • Monaghan P (2008) Early growth conditions, phenotypic development and environmental change. Philos Trans R Soc B Biol Sci 363:1635–1645

    Google Scholar 

  • Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 12:75–92

    PubMed  Google Scholar 

  • Moore MP, Martin RA (2019) On the evolution of carry-over effects. J Anim Ecol 88:1832–1844

    PubMed  Google Scholar 

  • Moran NP, Sanchez-Tojar A, Schielzeth H, Reinhold K (2021) Poor nutritional condition promotes high-risk behaviours: a systematic review and meta-analysis. Biol Rev 96:269–288

    PubMed  Google Scholar 

  • Morisson M et al (2017) Nutritional programming and effect of ancestor diet in birds. Springer, New York

    Google Scholar 

  • Mueller CA (2018) Critical Windows in animal development: interactions between environment, phenotype, and time. In: Development and environment. Springer, New York, pp 41–72

    Google Scholar 

  • Murren CJ et al (2015) Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity. Heredity 115:293–301

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nakagawa S, Lagisz M, Hector KL, Spencer HG (2012) Comparative and meta-analytic insights into life extension via dietary restriction. Aging Cell 11:401–409

    CAS  PubMed  Google Scholar 

  • Neuringer M, Connor WE, Lin DS, Barstad L, Luck S (1986) Biochemical and functional effects of prenatal and postnatal omega 3 fatty acid deficiency on retina and brain in rhesus monkeys. Proc Natl Acad Sci 83:4021–4025

    CAS  PubMed  PubMed Central  Google Scholar 

  • Newman AEM, MacDougall-Shackleton SA, An Y-S, Kriengwatana B, Soma KK (2010) Corticosterone and dehydroepiandrosterone have opposing effects on adult neuroplasticity in the Avian Song Control System. J Comp Neurol 518:3662–3678

    CAS  PubMed  Google Scholar 

  • Nijhout HF (2015) A developmental–physiological perspective on the development and evolution of phenotypic plasticity. Concep Change Biol 2015:147–173

    Google Scholar 

  • Nijhout H, Davidowitz G (2003) Developmental perspectives on phenotypic variation, canalization, and fluctuating asymmetry. Oxford University Press, New York

    Google Scholar 

  • Nijhout H, Emlen D (1998) Competition among body parts in the development and evolution of insect morphology. Proc Natl Acad Sci U S A 95:3685–3689

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nijhout HF, German R (2012) Developmental causes of allometry: new models and implications for phenotypic plasticity and evolution. Integr Comp Biol 52:43–52

    PubMed  PubMed Central  Google Scholar 

  • Nijhout H, McKenna K (2019) Allometry, scaling, and ontogeny of form—an introduction to the symposium. Integr Comp Biol 59:1275–1280

    PubMed  Google Scholar 

  • Noguera JC, Metcalfe NB, Surai PF, Monaghan P (2015) Are you what you eat? Micronutritional deficiencies during development influence adult personality-related traits. Anim Behav 101:129–140

    Google Scholar 

  • Nowicki S, Searcy WA, Peters S (2002) Brain development, song learning and mate choice in birds: a review and experimental test of the “nutritional stress hypothesis”. J Comp Physiol A 188:1003–1014

    CAS  Google Scholar 

  • Nylin S, Gotthard K (1998) Plasticity in life-history traits. Annu Rev Entomol 43:63–83

    CAS  PubMed  Google Scholar 

  • O'Connor CM, Norris DR, Crossin GT, Cooke SJ (2014) Biological carryover effects: linking common concepts and mechanisms in ecology and evolution. Ecosphere 5:1–11

    Google Scholar 

  • Ozanne SE, Hales CN (2004) Catch-up growth and obesity in male mice. Nature 427:411–412

    CAS  PubMed  Google Scholar 

  • Painter RC, Osmond C, Gluckman P, Hanson M, Phillips D, Roseboom TJ (2008) Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG Int J Obstet Gynaecol 115:1243–1249

    CAS  Google Scholar 

  • Panchanathan K, Frankenhuis WE (2016) The evolution of sensitive periods in a model of incremental development. Proc R Soc B Biol Sci 283. https://doi.org/10.1098/rspb.2015.2439

  • Partridge L, Gems D, Withers DJ (2005) Sex and death: what is the connection? Cell 120:461–472

    CAS  PubMed  Google Scholar 

  • Pechenik JA (2006) Larval experience and latent effects—metamorphosis is not a new beginning. Integr Comp Biol 46:323–333

    PubMed  Google Scholar 

  • Pechenik JA, Wendt DE, Jarrett JN (1998) Metamorphosis is not a new beginning: larval experience influences juvenile performance. Bioscience 48:901–910

    Google Scholar 

  • Pellegroms B, Van Dongen S, Van Dyck H, Lens L (2009) Larval food stress differentially affects flight morphology in male and female speckled woods (Pararge aegeria). Ecol Entomol 34:387–393

    Google Scholar 

  • Pentinat T, Ramon-Krauel M, Cebria J, Diaz R, Jimenez-Chillaron JC (2010) Transgenerational inheritance of glucose intolerance in a mouse model of neonatal overnutrition. Endocrinology 151:5617–5623

    CAS  PubMed  Google Scholar 

  • Piersma T, Drent J (2003) Phenotypic flexibility and the evolution of organismal design. Trends Ecol Evol 18:228–233

    Google Scholar 

  • Pigeon G, Festa-Bianchet M, Pelletier F (2017) Long-term fitness consequences of early environment in a long-lived ungulate. Proc R Soc B Biol Sci 284:20170222

    Google Scholar 

  • Pigeon G et al (2019) Silver spoon effects are constrained under extreme adult environmental conditions. Ecology 100:e02886

    PubMed  Google Scholar 

  • Poças GM, Crosbie AE, Mirth CK (2020) When does diet matter? The roles of larval and adult nutrition in regulating adult size traits in Drosophila melanogaster. J Insect Physiol. https://doi.org/10.1016/j.**sphys.2020.104051

  • Pollock CJ, Capilla-Lasheras P, McGill RA, Helm B, Dominoni DM (2017) Integrated behavioural and stable isotope data reveal altered diet linked to low breeding success in urban-dwelling blue tits (Cyanistes caeruleus). Sci Rep 7:1–14

    CAS  Google Scholar 

  • Ponton F, Morimoto J, Robinson K, Kumar SS, Cotter SC, Wilson K, Simpson SJ (2020) Macronutrients modulate survival to infection and immunity in Drosophila. J Anim Ecol 89:460–470

    PubMed  Google Scholar 

  • Pravosudov VV, Lavenex P, Omanska A (2005) Nutritional deficits during early development affect hippocampal structure and spatial memory later in life. Behav Neurosci 119:1368–1374

    CAS  PubMed  Google Scholar 

  • Radder RS, Warner DA, Shine R (2007) Compensating for a bad start: catch-up growth in juvenile lizards (Amphibolurus muricatus, Agamidae). J Exp Zool A Ecol Genet Physiol 307:500–508

    PubMed  Google Scholar 

  • Radford EJ et al (2014) In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science 345

    Google Scholar 

  • Ramos-Lopez O, Riezu-Boj JI, Milagro FI, Martinez JA (2019) Epigenetics of undernutrition. In: Patel VB, Preedy VR (eds) Handbook of nutrition, diet, and epigenetics. Springer, Cham, pp 457–481

    Google Scholar 

  • Rao R, Georgieff MK (2007) Iron in fetal and neonatal nutrition. Semin Fetal Neonatal Med 12:54–63

    PubMed  Google Scholar 

  • Ratsika A, Codagnone MC, O’Mahony S, Stanton C, Cryan JF (2021) Priming for life: early life nutrition and the microbiota-gut-brain axis. Nutrients 13:423. https://doi.org/10.3390/nu13020423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raubenheimer D (1993) A multi-levelanalysis of feeding behaviour: the geometry of nutritional decisions. Philos Trans R Soc Lond B342:381–402

    Google Scholar 

  • Raubenheimer D, Simpson S (1993) The geometry of compensatory feeding in the locust. Anim Behav 45:953–964

    Google Scholar 

  • Regan JC, Froy H, Walling CA, Moatt JP, Nussey DH (2020) Dietary restriction and insulin-like signalling pathways as adaptive plasticity: a synthesis and re-evaluation. Funct Ecol 34:107–128

    Google Scholar 

  • Rehman N, Varghese J (2021) Larval nutrition influences adult fat stores and starvation resistance in Drosophila. PLoS One 16

    Google Scholar 

  • Reichling T, German R (2000) Bones, muscles and visceral organs of protein-malnourished rats (Rattus norvegicus) grow more slowly but for longer durations to reach normal final size. J Nutr 130:2326–2332

    CAS  PubMed  Google Scholar 

  • Rice D, Barone S (2000) Critical periods of vulnerability for the develo** nervous system: evidence from humans and animal models. Environ Health Perspect 108:511–533

    PubMed  PubMed Central  Google Scholar 

  • Richardson KM, Parlato EH, Walker LK, Parker KA, Ewen JG, Armstrong DP (2019) Links between personality, early natal nutrition and survival of a threatened bird. Philos Trans R Soc B Biol Sci 374:20190373

    Google Scholar 

  • Rion S, Kawecki TJ (2007) Evolutionary biology of starvation resistance: what we have learned from Drosophila. J Evol Biol 20:1655–1664

    CAS  PubMed  Google Scholar 

  • Ritschard M, Brumm H (2012) Zebra finch song reflects current food availability. Evol Ecol 26:801–812

    Google Scholar 

  • Roberts L, Taylor J, Gough P, Forman D, Garcia de Leaniz C (2014) Silver spoons in the rough: can environmental enrichment improve survival of hatchery Atlantic salmon Salmo salar in the wild? J Fish Biol 85:1972–1991

    CAS  PubMed  Google Scholar 

  • Robertson B-A et al (2017) Food restriction reduces neurogenesis in the avian hippocampal formation. PLoS One 12:e0189158

    PubMed  PubMed Central  Google Scholar 

  • Roseboom TJ, Painter RC, van Abeelen AF, Veenendaal MV, de Rooij SR (2011) Hungry in the womb: what are the consequences? Lessons from the Dutch famine. Maturitas 70:141–145

    PubMed  Google Scholar 

  • Runagall-McNaull A, Bonduriansky R, Crean A (2015) Dietary protein and lifespan acrossthe metamorphic boundary:protein-restricted larvae develop into short-lived adults. Sci Rep 5:11783

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ryo M, Aguilar-Trigueros CA, Pinek L, Muller LA, Rillig MC (2019) Basic principles of temporal dynamics. Trends Ecol Evol 34:723–733

    PubMed  Google Scholar 

  • Saastamoinen M, Van der Sterren D, Vastenhout N, Zwaan BJ, Brakefield PM (2010) Predictive adaptive responses: condition-dependent impact of adult nutrition and flight in the tropical butterfly Bicyclus anynana. Am Nat 176:686–698

    PubMed  Google Scholar 

  • Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89

    CAS  PubMed  Google Scholar 

  • Sayer AA, Dunn R, Langley-Evans S, Cooper C (2001) Prenatal exposure to a maternal low protein diet shortens life span in rats. Gerontology 47:9–14

    Google Scholar 

  • Schenk S, Saberi M, Olefsky JM (2008) Insulin sensitivity: modulation by nutrients and inflammation. J Clin Investig 118:2992–3002

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt KL, MacDougall-Shackleton EA, MacDougall-Shackleton SA (2012) Developmental stress has sex-specific effects on nestling growth and adult metabolic rates but no effect on adult body size or body composition in song sparrows. J Exp Biol 215:3207–3217

    PubMed  Google Scholar 

  • Schmidt KL, Moore SD, MacDougall-Shackleton EA, MacDougall-Shackleton SA (2013) Early-life stress affects song complexity, song learning and volume of the brain nucleus RA in adult male song sparrows. Anim Behav 86:25–35

    Google Scholar 

  • Schmidt KL, MacDougall-Shackleton EA, Soma KK, MacDougall-Shackleton SA (2014) Developmental programming of the HPA and HPG axes by early-life stress in male and female song sparrows. Gen Comp Endocrinol 196:72–80

    CAS  PubMed  Google Scholar 

  • Schrader M, Travis J (2012) Variation in offspring size with birth order in placental fish: a role for asymmetric sibling competition? Evolution 66:272–279

    PubMed  Google Scholar 

  • Schulz LC (2010) The Dutch hunger winter and the developmental origins of health and disease. Proc Natl Acad Sci U S A 107:16757–16758

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schwartz MW, Woods SC, Porte D, Seeley RJ, Baskin DG (2000) Central nervous system control of food intake. Nature 404:661–671

    CAS  PubMed  Google Scholar 

  • Scofield HN, Mattila HR (2015) Honey bee workers that are pollen stressed as larvae become poor foragers and waggle dancers as adults. PLoS One 10:e0121731

    PubMed  PubMed Central  Google Scholar 

  • Sealey W, Gatlin D (2002) Dietary vitamin C and vitamin E interact to influence growth and tissue composition of juvenile hybrid striped bass (Morone chrysops x M. saxatilis) but have limted effects on immune responses. J Nutr 132:748–755

    CAS  PubMed  Google Scholar 

  • Sebens KP (1987) The ecology of indeterminate growth in animals. Annu Rev Ecol Syst 18:371–407

    Google Scholar 

  • Selman C et al (2006) Life-long vitamin C supplementation in combination with cold exposure does not affect oxidative damage or lifespan in mice, but decreases expression of antioxidant protection genes. Mech Ageing Dev 127:897–904

    CAS  PubMed  Google Scholar 

  • Sentinella AT, Crean AJ, Bonduriansky R (2013) Dietary protein mediates a trade-off between larval survival and the development of male secondary sexual traits. Funct Ecol 27:1134–1144

    Google Scholar 

  • Serobyan V, Sommer R (2017) Developmental systems of plasticity and trans-generational epigenetic inheritance in nematodes. Curr Opin Genet Dev 45:51–57

    CAS  PubMed  Google Scholar 

  • Shanley DP, Kirkwood TB (2000) Calorie restriction and aging: a life-history analysis. Evolution 54:740–750

    CAS  PubMed  Google Scholar 

  • Shasa D, Odhiambo J, Long N, Tuersunjiang N, Nathanielsz P, Ford S (2015) Multigenerational impact of maternal overnutrition/obesity inthe sheep on the neonatal leptin surge in granddaughters. Int J Obes 39:695–701

    CAS  Google Scholar 

  • Shin B, Dai Y, Thamotharan M, Gibson L, Devaskar S (2012) Pre- and postnatal calorie restriction perturbs early hypothalamic neuropeptide and energy balance. J Neurosci Res 90:1169–1182

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sillanpää S, Salminen J-P, Eeva T (2010) Fluctuating asymmetry in great tit nestlings in relation to diet quality, calcium availability and pollution exposure. Sci Total Environ 408:3303–3309

    PubMed  Google Scholar 

  • Simerly R (2008) Hypothalamic substrates of metabolic imprinting. Physiol Behav 94:79–89

    CAS  PubMed  Google Scholar 

  • Simpson S, Raubenheimer D (2012) The nature of nutrition: a unifying framework from animal adaptation to human obesity. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Simpson S, Sibly R, Lee K, Behmer S, Raubenheimer D (2004) Optimal foraging when regulating intake of multiple nutrients. Anim Behav 68:1299–1311

    Google Scholar 

  • Simpson SJ, Le Couteur DG, Raubenheimer D (2015) Putting the balance back in diet. Cell 161:18–23

    CAS  PubMed  Google Scholar 

  • Simpson SJ, Le Couteur DG, Raubenheimer D, Solon-Biet SM, Cooney GJ, Cogger VC, Fontana L (2017) Dietary protein, aging and nutritional geometry. Ageing Res Rev 39:78–86

    CAS  PubMed  Google Scholar 

  • Smith AC, Shima JS (2011) Variation in the effects of larval history on juvenile performance of a temperate reef fish. Austral Ecol 36:830–838

    Google Scholar 

  • Snell-Rood EC, Espeset A, Boser CJ, White WA, Smykalski R (2014) Anthropogenic changes in sodium affect neural and muscle development in butterflies. Proc Natl Acad Sci U S A 111:10221–10226

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sohal RS, Weindruch R (1996) Oxidative stress, caloric restriction, and aging. Science 273:59–63

    CAS  PubMed  PubMed Central  Google Scholar 

  • South S, House C, Moore A, Simpson S, Hunt J (2011) Male cockroaches prefer a high carbohydrate diet that makes them more attractive to females: implications for the study of condition dependence. Evolution 65:1594–1606

    CAS  PubMed  Google Scholar 

  • Spagopoulou F, Teplitsky C, Chantepie S, Lind MI, Gustafsson L, Maklakov AA (2020) Silver-spoon upbringing improves early-life fitness but promotes reproductive ageing in a wild bird. Ecol Lett 23:994–1002

    PubMed  Google Scholar 

  • Spencer K, Buchanan K, Goldsmith A, Catchpole C (2003) Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata). Horm Behav 44:132–139

    CAS  PubMed  Google Scholar 

  • Spencer KA, Evans NP, Monaghan P (2009) Postnatal stress in birds: a novel model of glucocorticoid programming of the hypothalamic-pituitary-adrenal axis. Endocrinology 150:1931–1934

    CAS  PubMed  Google Scholar 

  • Spencer SJ, D’Angelo H, Soch A, Watkins LR, Maier SF, Barrientos RM (2017) High-fat diet and aging interact to produce neuroinflammation and impair hippocampal- and amygdalar-dependent memory. Neurobiol Aging 58:88–101

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stamps JA, Krishnan VV (2017) Age-dependent changes in behavioural plasticity: insights from Bayesian models of development. Anim Behav 126:53–67

    Google Scholar 

  • Stearns SC, Kawecki TJ (1994) Fitness sensitivity and the canalization of life-history traits. Evolution 48:1438–1450

    PubMed  Google Scholar 

  • Stefana MI, Driscoll PC, Obata F, Pengelly AR, Newell CL, MacRae JI, Gould AP (2017) Developmental diet regulates Drosophila lifespan via lipid autotoxins. Nat Commun 8

    Google Scholar 

  • Sterner R, Elser J (2002) Ecological stoichimetry: the biology of elements from molecules to the biosphere. Princeton UniversityPress, Princeton, NJ

    Google Scholar 

  • Stige L, Hessen D, Vøllestad L (2004) Severe food stress has no detectable impact on developmental instability in Daphnia magna. Oikos 107:519–530

    Google Scholar 

  • Suzuki TA (2017) Links between natural variation in the microbiome and host fitness in wild mammals. Integr Comp Biol 57:756–769

    CAS  PubMed  Google Scholar 

  • Swaddle JP, Witter MS (1994) Food, feathers and fluctuating asymmetries. Proc R Soc Lond Ser B Biol Sci 255:147–152

    Google Scholar 

  • Tachibana T, Tsutsui K (2016) Neuropeptide control of feeding behavior in birds and its difference with mammals. Front Neurosci 10:485

    PubMed  PubMed Central  Google Scholar 

  • Tarry-Adkins JL et al (2007) Protein restriction in lactation confers nephroprotective effects in the male rat and is associated with increased antioxidant expression. Am J Physiol Regul Integr Comp Physiol 293:R1259–R1266

    CAS  PubMed  Google Scholar 

  • Templeman NM, Murphy CT (2018) Regulation of reproduction and longevity by nutrient-sensing pathways. J Cell Biol 217:93–106

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas MSC, Johnson MH (2008) New advances in understanding sensitive periods in brain development. Curr Dir Psychol Sci 17:1–5

    Google Scholar 

  • Tilman D, Clark M (2014) Global diets link environmental sustainability and human health. Nature 515:518

    CAS  PubMed  Google Scholar 

  • Tremaroli V, Backhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489:242–249

    CAS  PubMed  Google Scholar 

  • Tu MP, Tatar M (2003) Juvenile diet restriction and the aging and reproduction of adult Drosophila melanogaster. Aging Cell 2:327–333

    CAS  PubMed  Google Scholar 

  • Uller T, Nakagawa S, English S (2013) Weak evidence for anticipatory parental effects in plants and animals. J Evol Biol 26:2161–2170

    CAS  PubMed  Google Scholar 

  • Valtonen T, Kangassalo K, Polkki M, Rantala M (2012) Transgenerational effects of parental larval diet on offspring development time, adult body size and pathogen resistance in Drosophila melanogaster. PLoS One 7:e31611

    CAS  PubMed  PubMed Central  Google Scholar 

  • Van Buskirk J, Steiner UK (2009) The fitness costs of developmental canalization and plasticity. J Evol Biol 22:852–860

    PubMed  Google Scholar 

  • Van De Pol M, Bruinzeel LW, Heg D, Van Der Jeugd HP, Verhulst S (2006) A silver spoon for a golden future: long-term effects of natal origin on fitness prospects of oystercatchers (Haematopus ostralegus). J Anim Ecol 75:616–626

    PubMed  Google Scholar 

  • Van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128:137–142

    Google Scholar 

  • Vantaux A, Lefèvre T, Cohuet A, Dabiré KR, Roche B, Roux O (2016) Larval nutritional stress affects vector life history traits and human malaria transmission. Sci Rep 6

    Google Scholar 

  • Verhulst S, Holveck M-J, Riebel K (2006) Long-term effects of manipulated natal brood size on metabolic rate in zebra finches. Biol Lett 2:478–480

    PubMed  PubMed Central  Google Scholar 

  • Vickers M (2014) Early life nutrition, epigenetics and programming of later life disease. Nutrients 6:2165–2178

    CAS  PubMed  PubMed Central  Google Scholar 

  • Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150:563–565

    Google Scholar 

  • Warne RW, Crespi EJ (2015) Larval growth rate and sex determine resource allocation and stress responsiveness across life stages in juvenile frogs. J Exp Zool A Ecol Genet Physiol 323:191–201

    CAS  PubMed  Google Scholar 

  • Weimerskirch H, Barbraud C, Lys P (2000) Sex differences in parental investment and chick growth in wandering albatrosses: fitness consequences. Ecology 81:309–318

    Google Scholar 

  • Wells JC (2007) Flaws in the theory of predictive adaptive responses. Trends Endocrinol Metab 18:331–337

    CAS  PubMed  Google Scholar 

  • West-Eberhard M (2003) Developmental plasticity and evolution. Oxford University Press, Oxford, UK

    Google Scholar 

  • Wilkin TA, King LE, Sheldon BC (2009) Habitat quality, nestling diet, and provisioning behaviour in great tits Parus major. J Avian Biol 40:135–145

    Google Scholar 

  • Wingfield JC, Maney DL, Breuner CW, Jacobs JD, Lynn S, Ramenofsky M, Richardson RD (1998) Ecological bases of hormone-behavior interactions: the “emergency life history stage”. Am Zool 38:191–206

    CAS  Google Scholar 

  • Witter MS, Swaddle JP, Cuthill IC (1995) Periodic food availability and strategic regulation of body-mass in the European starling, Sturnus vulgaris. Funct Ecol 9:568–574

    Google Scholar 

  • Woodgate JL, Leitner S, Catchpole CK, Berg ML, Bennett ATD, Buchanan KL (2011) Developmental stressors that impair song learning in males do not appear to affect female preferences for song complexity in the zebra finch. Behav Ecol 22:566–573

    Google Scholar 

  • Yamada K, Soma M (2016) Diet and birdsong: short-term nutritional enrichment improves songs of adult Bengalese finch males. J Avian Biol 47:865–870

    Google Scholar 

  • Zahavi A (1975) Mate selection-a selection for a handicap. J Theor Biol 53:205–214

    CAS  PubMed  Google Scholar 

  • Zajitschek F, Hunt J, Jennions MD, Hall MD, Brooks RC (2009) Effects of juvenile and adult diet on ageing and reproductive effort of male and female black field crickets, Teleogryllus commodus. Funct Ecol 2009:602–611

    Google Scholar 

  • Zambrano E et al (2005) A maternal low protein diet during pregnancy and lactation in the rat impairs male reproductive development. J Physiol Lond 563:275–284

    CAS  PubMed  Google Scholar 

  • Zambrano E, Ibanez C, Martinez-Samayoa PM, Lomas-Soria C, Durand-Carbajal M, Rodriguez-Gonzalez GL (2016) Maternal obesity: lifelong metabolic outcomes for offspring from poor developmental trajectories during the perinatal period. Arch Med Res 47:1–12

    PubMed  Google Scholar 

  • Zann R, Cash E (2008) Developmental stress impairs song complexity but not learning accuracy in non-domesticated zebra finches (Taeniopygia guttata). Behav Ecol Sociobiol 62:391–400

    Google Scholar 

  • Zeisel SH (2006) The fetal origins of memory: The role of dietary choline in optimal brain development. J Pediatr 149:S131–S136

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YY, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM (1994) Positional cloning of the mouse obese gene and its human homolog. Nature 372:425–432

    CAS  PubMed  Google Scholar 

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Buchanan, K.L., Meillère, A., Jessop, T.S. (2022). Early Life Nutrition and the Programming of the Phenotype. In: Costantini, D., Marasco, V. (eds) Development Strategies and Biodiversity. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-030-90131-8_6

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