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Developmental Plasticity and Heterokairy

  • John I. SpicerEmail author
  • Oliver Tills
  • Manuela Truebano
  • Simon D. Rundle
Chapter

Abstract

There is a resurgence of interest in using phenotypic plasticity, ‘the environmentally sensitive production of alternative phenotypes by given genotypes’, as a framework in the study of evolutionary biology. The term developmental plasticity describes a more specific strand of investigation dealing with how alterations to developmental processes and outcomes shape such environmentally induced variation. Nested within developmental plasticity is the notion of heterokairy, the potential of a single genotype to alter the timing of a developmental event (e.g. onset of a particular structure, function or components of that function), in response to an environmental signal or influence. Here we make a case for using the term heterokairy as a way of focusing on altered timing across different biological disciplines, and we suggest a road map for such an approach. Heterokairy as an interdisciplinary term could be used to (a) bring together the substantial knowledge currently available of environmentally sensitive, genetic and hormonal control of the timing of developmental transitions, (b) embed the study of altered timing of developmental events within developmental plasticity and (c) highlight the role that plasticity can play in adaptive evolution, particularly in response to global environmental change.

References

  1. Adolph EF (1968) Origins of physiological variation. Academic Press, New YorkGoogle Scholar
  2. Arnqvist G, Johansson F (1998) Ontogenetic reaction norms of predator-induced defensive morphology in dragonfly larvae. Ecology 79:1847–1858Google Scholar
  3. Arthur W (2004) Biased embryos and evolution. Cambridge University Press, CambridgeGoogle Scholar
  4. Atchley WR, Zhu J (1997) Developmental quantitative genetics, conditional epigenetic variability and growth in mice. Genetics 147:765–776PubMedPubMedCentralGoogle Scholar
  5. Auld JR, Agrawal AA, Relyea RA (2010) Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc R Soc B Biol Sci 277:503–511Google Scholar
  6. Bagatto B (2005) Ontogeny of cardiovascular control in zebrafish (Danio rerio): effects of developmental environment. Comp Biochem Physiol A Mol Integr Physiol 141:391–400PubMedGoogle Scholar
  7. Bateson P, Barker D, Clutton-Brock T, Deb D, D’Udine B, Foley RA, Gluckman P, Godfrey K, Kirkwood T, Lahr MM, McNamara J, Metcalfe NB, Monaghan P, Spencer HG, Sultan SE (2004) Developmental plasticity and human health. Nature 430:419–421PubMedGoogle Scholar
  8. Bateson P, Gluckman P (2011) Plasticity, robustness, development and evolution. Cambridge University Press, CambridgeGoogle Scholar
  9. Bäurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125:655–664PubMedGoogle Scholar
  10. Bavis RW, Young KM, Barry KJ, Boller MR, Klein PM, Ovrutsky AR, Rampersad DA (2010) Chronic hyperoxia alters the early and late phases of the hypoxic ventilatory response in neonatal rats. J Appl Physiol 109:796–803PubMedPubMedCentralGoogle Scholar
  11. Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F (2012) Impacts of climate change on the future of biodiversity. Ecol Lett 15:365–377PubMedPubMedCentralGoogle Scholar
  12. Benard MF (2015) Warmer winters reduce frog fecundity and shift breeding phenology, which consequently alters larval development and metamorphic timing. Glob Chang Biol 21:1058–1065PubMedGoogle Scholar
  13. Black JL, Burggren WW (2004) Acclimation to hypothermic incubation in developing chicken embryos (Gallus domesticus). J Exp Biol 207:1543–1552PubMedGoogle Scholar
  14. Blacker HA, Orgeig S, Daniels CB (2004) Hypoxia control of the development of the surfactant system in the chicken: evidence for physiological heterokairy. Am J Physiol Regul Integr Comp Physiol 287:R403–R410PubMedGoogle Scholar
  15. Bradshaw WE (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155Google Scholar
  16. Bradshaw WE, Holzapfel CM (2010) Light, time, and the physiology of biotic response to rapid climate change in animals. Annu Rev Physiol 72:147–166PubMedGoogle Scholar
  17. Burggren WW (1992) The importance of an ontogenic perspective in physiological studies: amphibian cardiology as a case study. In: Wood SC, Weber R, Hargens A, Millard R (eds) Physiological adaptations in vertebrates: respiration, circulation and metabolism. Dekker, New York, pp 235–253Google Scholar
  18. Burggren WW (1998) Studying physiological development: past, present and future. Biol Bull Nat Taiwan Normal Univ 33:71–84Google Scholar
  19. Burggren WW (2000) Developmental physiology, animal models, and the August Krogh principle. Zoology 102:148–156Google Scholar
  20. Burggren WW (2005) Developing animals flout assumptions of ecological physiology. Comp Biochem Physiol A Mol Integr Physiol 141:430–439PubMedGoogle Scholar
  21. Burggren WW (2006) Complexity change during physiological development. In: Warburton S, Burggren W, Pelster B, Reiber CL, Spicer JI (eds) Comparative developmental physiology: contributions, tools and trends. Oxford University Press, Oxford, pp 174–190Google Scholar
  22. Burggren WW, Bemis T (1990) Studying physiological evolution: paradigms and pitfalls. In: Nltecki MH (ed) Evolutionary innovations: patterns and processes. Oxford University Press, Oxford, pp 191–228Google Scholar
  23. Burggren WW, Just JJ (1992) Developmental changes in amphibian physiological systems. In: Feder ME, Burggren WW (eds) Environmental physiology of the Amphibia. University of Chicago Press, Chicago, pp 467–530Google Scholar
  24. Burggren WW, Reyna KS (2011) Developmental trajectories, critical windows and phenotypic alteration during cardio-respiratory development. Respir Physiol Neurobiol 178:13–21PubMedGoogle Scholar
  25. Burggren WW, Warburton S (2005) Comparative developmental physiology: an interdisciplinary convergence. Annu Rev Physiol 67:203–223PubMedPubMedCentralGoogle Scholar
  26. Cleland EE, Allen JM, Crimmin TM, Dunne JA, Pau S, Travers SE, Zavaleta ES, Wolkovich EM (2012) Phenological tracking enables positive species responses to climate change. Ecology 93:1765–1771PubMedGoogle Scholar
  27. Collin R, Roof KE, Spangler A (2016) Hatching plasticity in the tropical gastropod Nerita scabricosta. Invertebr Biol 135:87–96Google Scholar
  28. Corse E, Neve G, Sinama M, Pech N, Costedoat C, Chappaz R, Gilles A (2012) Plasticity of ontogenetic trajectories in cyprinids: a source of evolutionary novelties. Biol J Linn Soc 106:342–355Google Scholar
  29. Crispo E (2007) The Baldwin effect and genetic assimilation: revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity. Evolution 61:2469–2479PubMedGoogle Scholar
  30. Darwin C (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. John Murray, LondonGoogle Scholar
  31. De Jong IML, Colbert MW, Witte F, Richardson MK (2009) Polymorphism in developmental timing: intraspecific heterochrony in a Lake Victoria cichlid. Evol Dev 11:625–635PubMedGoogle Scholar
  32. De Smit L, Bruggeman DV, Tona JK, Debonne M, Onagbesan O, Arckens L, De Baerdemaeker J, Decuypere E (2006) Embryonic developmental plasticity of the chick: increased CO2 during early stages of incubation changes the developmental trajectories during prenatal and postnatal growth. Comp Biochem Physiol A Mol Integr Physiol 145:166–175PubMedGoogle Scholar
  33. De Witt TJ (2016) Expanding the phenotypic plasticity paradigm to broader views of trait space and ecological function. Curr Zool 62:463–473Google Scholar
  34. DeWitt TJ, Scheiner SM (eds) (2004) Phenotypic plasticity: functional and conceptual approaches. Oxford University Press, OxfordGoogle Scholar
  35. Dimichele L, Taylor MH (1980) The environmental control of hatching in Fundulus heteroclitus. J Exp Zool 214:181–187Google Scholar
  36. Drost HG, Janitza P, Grosse I, Quint M (2017) Cross-kingdom comparison of the developmental hourglass. Curr Opin Genet Dev 45:69–75PubMedGoogle Scholar
  37. Evans DH (2008) Teleost fish osmoregulation: what have we learned since August Krogh, Homer Smith and Ancel Keys. Am J Physiol Regul Integr Comp Physiol 295:R704–R713PubMedGoogle Scholar
  38. Faunes F, Larraín J (2016) Conservation in the involvement of heterochronic genes and hormones during developmental transitions. Dev Biol 416:3–17PubMedGoogle Scholar
  39. Feder MA, Bennett AF, Burggren WW, Huey RB (eds) (1987) New directions in ecological physiology. Cambridge University Press, New YorkGoogle Scholar
  40. Feder MA, Bennett AF, Huey RB (2000) Evolutionary physiology. Annu Rev Ecol Syst 31:315–341Google Scholar
  41. Forrest J, Miller-Rushing AJ (2010) Towards a synthetic understanding of the role of phenology in ecology and evolution. Philos Trans R Soc B 365:3101–3112Google Scholar
  42. Forsman A (2015) Rethinking phenotypic plasticity and its consequences for individuals, populations and species. Heredity 115:276–284PubMedGoogle Scholar
  43. Forward RB, Tankersley RA, Rittschof D (2001) Cues for metamorphosis of brachyuran crabs: an overview. Am Zool 41:1108–1122Google Scholar
  44. Fusco G, Minelli A (2010) Phenotypic plasticity in development and evolution: facts and concepts. Philos Trans R Soc B 365:547–556Google Scholar
  45. Garland T Jr, Carter PA (1994) Evolutionary physiology. Annu Rev Physiol 56:579–621PubMedGoogle Scholar
  46. Gebauer P, Paschke K, Anger K (2003) Delayed metamorphosis in decapod crustaceans: evidence and consequences. Rev Chil Hist Nat 76:169–175Google Scholar
  47. Ghalambor CK, Hoke KL, Ruell EW, Fischer EK, Reznick DN, Hughes KA (2015) Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature. Nature 525:372–375PubMedGoogle Scholar
  48. 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 21:394–407Google Scholar
  49. Gomez-Mestre I, Buchholz DR (2006) Developmental plasticity mirrors differences among taxa in spadefoot toads linking plasticity and diversity. Proc Natl Acad Sci U S A 103:19021–19026PubMedPubMedCentralGoogle Scholar
  50. Gould SJ (1977) Ontogeny and phylogeny. Belknap, CambridgeGoogle Scholar
  51. Gould SJ, Lewontin RC (1979) The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond B Biol Sci 205:581–598PubMedGoogle Scholar
  52. Harvey W (1628) An anatomical disputation concerning the movement of the heart and blood in living creatures. Translated by Whitteridge G (1976). Blackwell, OxfordGoogle Scholar
  53. Heyland A, Hodin J (2004) Heterochronic developmental shift caused by thyroid hormone in larval sand dollars and its implications for phenotypic plasticity and the evolution of nonfeeding development. Evolution 58:524–538PubMedGoogle Scholar
  54. Hjelm J, Svanbäck R, Byström P, Persson L, Wahlström E (2001) Diet-dependent body morphology and ontogenetic reaction norms in Eurasian perch. Oikos 95:311–323Google Scholar
  55. Huijser P, Schmid M (2011) The control of developmental phase transitions in plants. Development 138:4117–4129PubMedGoogle Scholar
  56. IPCC (2014) Climate change 2014: synthesis report. Contribution of working groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team, Pachauri RK, Meyer LA (eds.)]. IPCC, Geneva, p 151Google Scholar
  57. Jones WHS (1931) Hippocrates volume IV on the Universe by Heraclitus. Loebe Classical LibraryGoogle Scholar
  58. Keyte AL, Smith KK (2014) Heterochrony and developmental timing mechanisms: changing ontogenies in evolution. Semin Cell Dev Biol 34:99–107PubMedGoogle Scholar
  59. Laland K, Uller T, Feldman M, Sterelny K, Müller GB, Moczek A, Jablonka E, Odling-Smee J (2014) Does evolutionary theory need a rethink? Nature 514:161–164PubMedGoogle Scholar
  60. Le Rouzic A, Carlborg Ö (2008) Evolutionary potential of hidden genetic variation. Trends Ecol Evol 23:33–37PubMedGoogle Scholar
  61. Loman J (2009) Primary and secondary phenology. Does it pay a frog to spawn early? J Zool (Lond) 279:64–70Google Scholar
  62. Longo LD (2013) The rise of fetal and neonatal physiology. Basic science to clinical care. Perspectives in Physiology, vol 1. Springer, New YorkGoogle Scholar
  63. Martin K, Bailey K, Moravek C, Carlson K (2011) Taking the plunge: Californian grunion embryos emerge rapidly with environmentally cued hatching. Integr Comp Biol 51:26–37PubMedGoogle Scholar
  64. Martin KL (1999) Ready and waiting: delayed hatching and extended incubation of anamniotic vertebrate terrestrial eggs. Am Zool 39:279–288Google Scholar
  65. Mateus ARA, Narques-Pita M, Oostra V, Lafuente E, Brakefield PM, Zwaan BJ, Beldade P (2014) Adaptive developmental plasticity: compartmentalized responses to environmental cues and to corresponding internal signals provide phenotypic flexibility. BMC Biol 12:97PubMedPubMedCentralGoogle Scholar
  66. McCormick SD (2001) Endocrine control of osmoregulation in teleost fish. Am Zool 41:781–794Google Scholar
  67. McCormick SD (2009) Evolution of the hormonal control of animal performance: insights from the seaward migration of salmon. Integr Comp Biol 49:408–422PubMedGoogle Scholar
  68. McCormick SD (2013) Smolt physiology and endocrinology. Fish Physiol 32:199–251Google Scholar
  69. McCormick SD, Saunders RI (1987) Preparatory physiological adaptations for marine life in salmonids: osmoregulation, growth and metabolism. Am Fish Soc Symp 1:211–229Google Scholar
  70. Mendez-Sachez JF, Burggren W (2012) Modulation of the onset of air-breathing of the Siamese fighting fish and the blue gourami. FASEB J 31:1071–1079Google Scholar
  71. Mendez-Sanchez JF, Burggren W (2014) Environmental modulation of the onset of air-breathing and survival of Betta splendens and Trichopodus trichopterus. J Fish Biol 84:794–807PubMedGoogle Scholar
  72. Miller-Rushing AJ, Høye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Philos Trans R Soc B 365:3177–3186Google Scholar
  73. Moczek AP, Sultan S, Foster S, Ledón-Rettig C, Dworkin I, Nijhout HF, Abouheif E, Pfennig DW (2011) The role of developmental plasticity in evolutionary innovation. Proc R Soc Lond B Biol Sci 278:2705–2713Google Scholar
  74. Monaghan P, Haussmann MF (2015) The positive and negative consequences of stressors during early life. Early Hum Dev 91:643–647PubMedPubMedCentralGoogle Scholar
  75. Moravek CL, Martin K (2011) Life goes on: delayed hatching, extended incubation, and heterokairy in development of embryonic California grunion, Leuresthes tenuis. Copeia 2011:308–314Google Scholar
  76. Moss EG (2007) Heterochronic genes and the nature of developmental time. Curr Biol 17:R425–R434PubMedGoogle Scholar
  77. Mourabit S, Rundle SD, Spicer JI, Sloman KA (2010) Alarm substance from adult zebrafish alters early embryonic development in offspring. Biol Lett 6:525–528PubMedPubMedCentralGoogle Scholar
  78. Mueller CA, Eme J, Burggren WW, Roghair RD, Rundle SD (2015) Challenges and opportunities in developmental integrative physiology. Comp Biochem Physiol A Mol Integr Physiol 184:113–124PubMedPubMedCentralGoogle Scholar
  79. Muratori FB (2010) Heterokairy as an anti-predator strategy for parasitic species. Commun Integr Biol 3:309–312PubMedPubMedCentralGoogle Scholar
  80. Muratori FB, Borlee S, Messing RH (2010) Induced niche shift as an anti-predator response for an endoparasitoid. Proc R Soc Lond B Biol Sci 277:1475–1480Google Scholar
  81. Murren CJ, Auld JR, Callahan H, Ghalambor CK, Handelsman CA, Heskel MA, Kingsolver JG, Maclean HJ, Masel J, Maughan H et al (2015) Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity. Heredity 115:293–301PubMedPubMedCentralGoogle Scholar
  82. Needham J (1933) On the dissociability of the fundamental processes in ontogenesis. Biol Rev 8:180–223Google Scholar
  83. Noble D, Jablonka E, Joyner MJ, Müller GB, Omholt SW (2014) Evolution evolves: physiology returns to centre stage. J Physiol 592:2237–2244PubMedPubMedCentralGoogle Scholar
  84. Orgeig S, Daniels CB (2009) Environmental selection pressures shaping the pulmonary surfactant system of adult and developing lungs. In: Glass ML, Wood SC (eds) Cardio-respiratory control in vertebrates. Springer, Berlin, pp 205–239Google Scholar
  85. Oyarzun FX, Strathmann RR (2011) Plasticity of hatching and the duration of planktonic development in marine invertebrates. Integr Comp Biol 51:81–90PubMedGoogle Scholar
  86. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669Google Scholar
  87. Pechenik JA (1990) Delayed metamorphosis by larvae of benthic marine invertebrates: does it occur? Is there a price to pay? Ophelia 32:63–94Google Scholar
  88. Pecl GT, Araujo MB, Bell J, Blanchard J, Bonebrake TC, Chen I, Clark TD, Colwell RK, Danielsen F, Evengard B, Robinson S et al (2017) Biodiversity redistribution under climate change: impacts on ecosystems and human well-being. Science 355:1–9Google Scholar
  89. Pedersen S, Berg PR, Culling M, Danzmann RG, Glebe B, Leadbetter S, Lien S, Moen T, Vandersteen W, Boulding EG (2013) Quantitative trait loci for precocious parr maturation, early smoltification, and adult maturation in double-backcrossed trans-Atlantic salmon (Salmo salar). Aquaculture 410-411:164–171Google Scholar
  90. Piersma T, Drent J (2003) Phenotypic flexibility and the evolution of organismal design. Trends Ecol Evol 18:228–233Google Scholar
  91. Pigliucci M (1998) Developmental phenotypic plasticity: where internal programming meets external environment. Curr Opin Plant Biol 1:87–91PubMedGoogle Scholar
  92. Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. Johns Hopkins University Press, BaltimoreGoogle Scholar
  93. Pigliucci M (2010) Genotype-phenotype mapping and the end of the ‘genes as blueprint’ metaphor. Philos Trans R Soc B 365:557–566Google Scholar
  94. Pigliucci M, Müller GB (2010) Evolution: the extended synthesis. MIT Press, CambridgeGoogle Scholar
  95. Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209:2362–2367PubMedGoogle Scholar
  96. Pigliucci M, Schlichting CD (1995) Ontogenetic reaction norms in Lobelia siphilitica (Lobeliaceae): response to shading. Ecology 76:2134–2144Google Scholar
  97. Pilgliucci M, Schlichting CD, Jones CS, Schwenk K (1996) Developmental reaction norms: the interactions among allometry, ontogeny and plasticity. Plant Species Biol 11:69–85Google Scholar
  98. Podrabsky JE, Romney AL, Culpepper KM (2016) Alternative developmental pathways. In: Berois N, García G, de Sá RO (eds) Annual fishes. Life history strategy, diversity and evolution. CRC Press, Taylor & Francis Group, Boca Raton, pp 63–74Google Scholar
  99. Poe S (2004) A test for patterns of modularity in sequences of developmental events. Evolution 58:1852–1855PubMedGoogle Scholar
  100. Polin RA, Fox WW, Abman SH (2011) Fetal and neonatal physiology (2 volumes). Saunders, Elsevier, PhiladelphiaGoogle Scholar
  101. Poullet N, Vielle A, Gimond C, Carvalho S, Teotónio H, Braendle C (2016) Complex heterochrony underlies the evolution of Caenorhabditis elegans hermaphrodite sex allocation. Evolution 70:2357–2369PubMedGoogle Scholar
  102. Price TC, Qvarnström A, Irwin DE (2003) The role of phenotypic plasticity in driving genetic evolution. Proc R Soc B 270:1433–1440PubMedGoogle Scholar
  103. Raff EC, Raff RA (2000) Dissociability, modularity, evolvability. Evol Dev 2:235–237PubMedGoogle Scholar
  104. Raff RA, Kaufman TC (1983) Embryos, genes and evolution. MacMillan, New YorkGoogle Scholar
  105. Raff RA, Wray GA (1989) Heterochrony: developmental mechanisms and evolutionary results. J Evol Biol 2:409–434Google Scholar
  106. Raff RR (1992) Direct-Developing Sea urchins and the evolutionary reorganisation of early development. BioEssays 14:211–218PubMedGoogle Scholar
  107. Riedl R (1978) Order in living systems: a systems analysis of evolution. Wiley, New YorkGoogle Scholar
  108. Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60PubMedGoogle Scholar
  109. Rougvie AE (2005) Intrinsic and extrinsic regulators of developmental timing: from miRNAs to nutritional cues. Development 132:3787–3798PubMedGoogle Scholar
  110. Rudin-Bitterli TS, Spicer JI, Rundle SD (2016) Differences in the timing of cardio-respiratory development determine whether marine gastropod embryos survive or die in hypoxia. J Exp Biol 219:1076–1085PubMedGoogle Scholar
  111. Rudolf VHW, Singh M (2013) Disentangling climate change effects on species interactions: effect of temperature, phenological shifts, and body size. Oecologia 173:1043–1052PubMedGoogle Scholar
  112. Rundle SD, Smirthwaite JJ, Colbert MW, Spicer JI (2011) Predator cues alter the timing of developmental events in gastropod embryos. Biol Lett 7:285–287PubMedGoogle Scholar
  113. Rundle SD, Spicer JI (2017) Heterokairy: a significant form of developmental plasticity? Biol Lett 12:20160509Google Scholar
  114. Russell GA, Rezende EL, Hammond KA (2008) Development partly determines the aerobic performance of adult deer mice, Peromyscus maniculatus. J Exp Biol 211:35–41PubMedGoogle Scholar
  115. Sakamoto T, McCormick SD, Hirano T (1993) Osmoregulatory actions of growth hormone and its mode of action in salmonids: a review. Fish Physiol Biochem 11:155–164PubMedGoogle Scholar
  116. Sarkar S (2004) From the Reaktionsnorm to the evolution of adaptive plasticity: a historical sketch, 1909-1999. In: DeWitt TJ, Scheiner SM (eds) Phenotypic plasticity: functional and conceptual approaches. Oxford University Press, Oxford, pp 10–30Google Scholar
  117. Schlichting CD, Pigliucci M (1998) Phenotypic evolution: a reaction norm perspective. Sinauer Associates, SunderlandGoogle Scholar
  118. Scoville AG, Pfrender ME (2010) Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators. Proc Natl Acad Sci U S A 107:4260–4263PubMedPubMedCentralGoogle Scholar
  119. Sikkink KL, Reynolds RM, Tuarte CM, Cresko WA, Phillips C (2014) Rapid evolution of phenotypic plasticity and shifting thresholds of genetic assimilation in the nematode Caenorhabditis remanei. Genes Genomes Genet 4:1103–1112Google Scholar
  120. Sloan AW (1978) William Harvey, physician and scientist. S Afr Med J 54:247–252PubMedGoogle Scholar
  121. Spicer JI (1995) Ontogeny of respiratory function in crustaceans exhibiting either direct or indirect development. J Exp Zool 272:413–418Google Scholar
  122. Spicer JI (2006) A physiological approach to heterochrony. In: Warburton S, Burggren W, Pelster B, Reiber CL, Spicer JI (eds) Comparative developmental physiology: contributions, tools and trends. Oxford University Press, New York, pp 191–202Google Scholar
  123. Spicer JI, Burggren WW (2003) Development of physiological regulatory systems: altering the timing of crucial events. Zoology 106:91–99PubMedGoogle Scholar
  124. Spicer JI, El-Gamal MM (1999) Hypoxia accelerates the development of respiratory regulation in brine shrimp – but at a cost. J Exp Biol 202:3637–3646PubMedGoogle Scholar
  125. Spicer JI, Eriksson SP (2003) Does the development of respiratory regulation always accompany the transition from pelagic larvae to benthic fossorial postlarvae in the Norway lobster Nephrops norvegicus (L)? J Exp Mar Biol Ecol 295:219–243Google Scholar
  126. Spicer JI, Rundle SD (2006) Out of place and out of time – towards a more integrated approach to heterochrony. Anim Biol 56:487–502Google Scholar
  127. Spicer JI, Rundle SD (2007) Plasticity in the timing of physiological development: physiological heterokairy – what is it, how frequent is it, and does it matter? Comp Biochem Physiol A Mol Integr Physiol 148:712–719PubMedGoogle Scholar
  128. Spicer JI, Rundle SD, Tills O (2011) Studying the altered timing of physiological events during development: it’s about time…or is it? Respir Physiol Neurobiol 178:3–12PubMedGoogle Scholar
  129. Stearns SC (1989) The evolutionary significance of phenotypic plasticity. Bioscience 39:436–445Google Scholar
  130. Strathmann RR, Fenaux L, Strathmann MF (1992) Heterochronic developmental plasticity in larval sea urchins and its implications for evolution of nonfeeding larvae. Evolution 46:972–986PubMedGoogle Scholar
  131. Sulston JE, Horvitz HR (1977) Post-embryonic cell lineages of the nematode Caenorhabditis elegans. Dev Biol 56:110–156PubMedGoogle Scholar
  132. Sulston JE, Horvitz HR (1981) Abnormal cell lineages in mutants of the nematode Caenorhabditis elegans. Dev Biol 82:41–55PubMedGoogle Scholar
  133. Sun LD, Ye M, Hao H, Wang NT, Wang YQ, Cheng TR, Zhang QX, Wu RL (2014) A model framework for identifying genes that guide the evolution of heterochrony. Mol Biol Evol 31:2238–2247PubMedGoogle Scholar
  134. Suzuki Y, Nijhout HF (2006) Evolution of a polyphenism by genetic accommodation. Science 311:650–652PubMedGoogle Scholar
  135. Tills O, Rundle SD, Salinger M, Haun T, Pfenninger M, Spicer JI (2011) A genetic basis for intraspecific differences in developmental timing? Evol Dev 13:542–548PubMedGoogle Scholar
  136. Tills O, Rundle SD, Spicer JI (2013a) Parent-offspring similarity in the timing of developmental events: a potential link between ontogeny and phylogeny. Proc R Soc Lond B Biol Sci 280:2013479Google Scholar
  137. Tills O, Rundle SD, Spicer JI (2013b) Variance in developmental event timing occurs predominantly at low biological levels: implications for heterochrony. Biol J Linn Soc 110:581–590Google Scholar
  138. Tills O, Spicer JI, Rundle SD (2010) Salinity-induced heterokairy in an upper-estuarine population of the snail Radix balthica (Mollusca: Pulmonata). Aquat Biol 9:95–105Google Scholar
  139. Van Buskirk J (2002) A comparative test of the adaptive plasticity hypothesis: relationships between habitat and phenotype in anuran larvae. Am Nat 160:87–102PubMedGoogle Scholar
  140. Van Dyck H, Bonte D, Puls R, Gotthard K, Maes D (2015) The lost generation hypothesis: could climate change drive ectotherms into a developmental trap? Oikos 124:54–61Google Scholar
  141. Varsamos S, Nebel C, Charmantier G (2005) Ontogeny of osmoregulation in postembryonic fish: a review. Comp Biochem Physiol A Mol Integr Physiol 141:401–429PubMedGoogle Scholar
  142. Voss SR, Smith JJ (2005) Evolution of salamander life cycles: a major-effect quantitative trait locus contributes to discrete and continuous variation for metamorphic timing. Genetica 170:275–281Google Scholar
  143. Wade AA, Hand BK, Kovach RP, Muhlfeld CC, Waples RS, Luikart G (2017) Assessments of species’ vulnerability to climate change: from pseudo to science. Biodivers Conserv 26:223–229Google Scholar
  144. Wagner D (2016) Making flowers at the right time. Dev Cell 37:208–210PubMedGoogle Scholar
  145. Wagner D (2017) Key developmental transitions during flower morphogenesis and their regulation. Curr Opin Genet Dev 45:44.  https://doi.org/10.1016/j.gde.2017.01.018 CrossRefPubMedGoogle Scholar
  146. Warburton SJ, Burggren WW, Pelster B, Reiber CL, Spicer JI (eds) (2006) Comparative developmental physiology. Oxford University Press, New YorkGoogle Scholar
  147. Warkentin KM (2007) Oxygen, gills, and embryo behaviour: mechanisms of adaptive plasticity in hatching. Comp Biochem Physiol A Mol Integr Physiol 148:720–731PubMedGoogle Scholar
  148. Warkentin KM (2011) Environmentally cued hatching across taxa: embryos respond to risk and opportunity. Integr Comp Biol 51:14–25PubMedGoogle Scholar
  149. West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 20:249–278Google Scholar
  150. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, OxfordGoogle Scholar
  151. West-Eberhard MJ (2005) Developmental plasticity and the origin of species differences. Proc Natl Acad Sci U S A 102:6543–6549PubMedPubMedCentralGoogle Scholar
  152. Wood HA (2014) Mosaic physiology from developmental noise: within organism physiological diversity as an alternative to phenotypic plasticity and phenotypic flexibility. J Exp Biol 217:35–45Google Scholar
  153. Wund MA, Baker JA, Clancy B, Golub JL, Fosterk SA (2008) A test of the “flexible stem” model of evolution: ancestral plasticity, genetic accommodation and morphological divergence in the three-spine stickleback radiation. Am Nat 172:449–462PubMedGoogle Scholar
  154. Yang LH, Rudolf VHW (2010) Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecol Lett 13:1–10PubMedGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • John I. Spicer
    • 1
    Email author
  • Oliver Tills
    • 1
  • Manuela Truebano
    • 1
  • Simon D. Rundle
    • 1
  1. 1.Marine Biology and Ecology Research Centre, School of Biological and Marine SciencesUniversity of PlymouthPlymouthUK

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