1932

Abstract

Adaptive phenotypic plasticity provides a mechanism of developmental rescue in novel and rapidly changing environments. Understanding the underlying mechanism of plasticity is important for predicting both the likelihood that a developmental response is adaptive and associated life-history trade-offs that could influence patterns of subsequent evolutionary rescue. Although evolved developmental switches may move organisms toward a new adaptive peak in a novel environment, such mechanisms often result in maladaptive responses. The induction of generalized physiological mechanisms in new environments is relatively more likely to result in adaptive responses to factors such as novel toxins, heat stress, or pathogens. Developmental selection forms of plasticity, which rely on within-individual selective processes, such as shaping of tissue architecture, trial-and-error learning, or acquired immunity, are particularly likely to result in adaptive plasticity in a novel environment. However, both the induction of plastic responses and the ability to be plastic through developmental selection come with significant costs, resulting in delays in reproduction, increased individual investment, and reduced fecundity. Thus, we might expect complex interactions between plastic responses that allow survival in novel environments and subsequent evolutionary responses at the population level.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ecolsys-110617-062622
2018-11-02
2024-10-14
Loading full text...

Full text loading...

/deliver/fulltext/es/49/1/annurev-ecolsys-110617-062622.html?itemId=/content/journals/10.1146/annurev-ecolsys-110617-062622&mimeType=html&fmt=ahah

Literature Cited

  1. Abelson ES. 2016. Brain size is correlated with endangerment status in mammals. Proc. R. Soc. B 283:20152772
    [Google Scholar]
  2. Acar M, Mettetal JT, van Oudenaarden A 2008. Stochastic switching as a survival strategy in fluctuating environments. Nat. Genet. 40:471–75
    [Google Scholar]
  3. Agrawal AA, Conner JK, Johnson MTJ, Wallsgrove R 2002. Ecological genetics of an induced plant defense against herbivores: additive genetic variance and costs of phenotypic plasticity. Evolution 56:2206–13
    [Google Scholar]
  4. Agrawal AA, Strauss SY, Stout MJ 1999. Costs of induced responses and tolerance to herbivory in male and female fitness components of wild radish. Evolution 53:1093–104
    [Google Scholar]
  5. Aitken SN, Yeaman S, Holliday JA, Wang TL, Curtis-McLane S 2008. Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol. Appl. 1:95–111
    [Google Scholar]
  6. Alberdi A, Aizpurua O, Bohmann K, Zepeda-Mendoza ML, Gilbert MTP 2016. Do vertebrate gut metagenomes confer rapid ecological adaptation?. Trends Ecol. Evol. 31:689–99
    [Google Scholar]
  7. Arai JA, Feig LA 2011. Long-lasting and transgenerational effects of an environmental enrichment on memory formation. Brain Res. Bull. 85:30–35
    [Google Scholar]
  8. Badyaev AV. 2005. Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation. Proc. R. Soc. B 72:877–86
    [Google Scholar]
  9. Baker AC. 2003. Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Evol. Syst 34:661–89
    [Google Scholar]
  10. Baldwin IT. 1998. Jasmonate-induced responses are costly but benefit plants under attack in native populations. PNAS 95:8113–18
    [Google Scholar]
  11. Barribeau SM, Schmid-Hempel P, Sadd BM 2016. Royal decree: gene expression in trans-generationally immune primed bumblebee workers mimics a primary immune response. PLOS ONE 11:e1059635
    [Google Scholar]
  12. Barrickman NL, Bastian ML, Isler K, van Schaik CP 2008. Life history costs and benefits of encephalization: a comparative test using data from long-term studies of primates in the wild. J. Hum. Evol. 54:568–90
    [Google Scholar]
  13. Beaumont HJE, Gallie J, Kost C, Ferguson GC, Rainey PB 2009. Experimental evolution of bet hedging. Nature 462:90–97
    [Google Scholar]
  14. Beever EA, Hall LE, Varner J, Loosen AE, Dunham JB et al. 2017. Behavioral flexibility as a mechanism for coping with climate change. Front. Ecol. Environ. 15:299–308
    [Google Scholar]
  15. Bell G, Collins S 2008. Adaptation, extinction and global change. Evol. Appl. 1:3–16
    [Google Scholar]
  16. Bergonzi S, Albani MC, van Themaat EVL, Nordstrom KJV, Wang RH et al. 2013. Mechanisms of age-dependent response to winter temperature in perennial flowering of Arabis alpina. Science 340:1094–97
    [Google Scholar]
  17. Berkelmans R, van Oppen MJH 2006. The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc. R. Soc. B 273:2305–12
    [Google Scholar]
  18. Best A, Hoyle A 2013. The evolution of costly acquired immune memory. Ecol. Evol. 3:2223–32
    [Google Scholar]
  19. Black AR, Dodson SI 1990. Demographic costs of Chaoborus-induced phenotypic plasticity in Daphnia pulex. Oecologia 83:117–22
    [Google Scholar]
  20. Bock KW. 2016. The UDP-glycosyltransferase (UGT) superfamily expressed in humans, insects and plants: animal-plant arms-race and co-evolution. Biochem. Pharmacol. 99:11–17
    [Google Scholar]
  21. Boettiger AN, Levine M 2009. Synchronous and stochastic patterns of gene activation in the Drosophila embryo. Science 325:471–73
    [Google Scholar]
  22. Boots M. 2011. The evolution of resistance to a parasite is determined by resources. Am. Nat. 178:214–20
    [Google Scholar]
  23. Boots M, Bowers RG 2004. The evolution of resistance through costly acquired immunity. Proc. R. Soc. B 271:715–23
    [Google Scholar]
  24. Borghans JAM, Beltman JB, De Boer RJ 2004. MHC polymorphism under host-pathogen coevolution. Immunogenetics 55:732–39
    [Google Scholar]
  25. Boulding EG, Hay T 2001. Genetic and demographic parameters determining population persistence after a discrete change in the environment. Heredity 86:313–24
    [Google Scholar]
  26. Brakefield PM, Reitsma N 1991. Phenotypic plasticity, seasonal climate and the population biology of Bicyclus butterflies (Satyridae) in Malawi. Ecol. Entomol. 16:291–303
    [Google Scholar]
  27. Bruno JF, Edmunds PJ 1997. Clonal variation for phenotypic plasticity in the coral Madracis mirabilis. Ecology 78:2177–90
    [Google Scholar]
  28. Buffelli M, Burgess RW, Feng GP, Lobe CG, Lichtman JW, Sanes JR 2003. Genetic evidence that relative synaptic efficacy biases the outcome of synaptic competition. Nature 424:430–34
    [Google Scholar]
  29. Butchart SHM, Walpole M, Collen B, van Strien A, Scharlemann JPW et al. 2010. Global biodiversity: indicators of recent declines. Science 328:1164–68
    [Google Scholar]
  30. Callahan HS, Dhanoolal N, Ungerer MC 2005. Plasticity genes and plasticity costs: a new approach using an Arabidopsis recombinant inbred population. New Phytol 166:129–39
    [Google Scholar]
  31. Carlson SM, Cunningham CJ, Westley PAH 2014. Evolutionary rescue in a changing world. Trends Ecol. Evol. 29:521–30
    [Google Scholar]
  32. Caruso CM, Maherali H, Sherrard M 2006. Plasticity of physiology in Lobelia: testing for adaptation and constraint. Evolution 60:980–90
    [Google Scholar]
  33. Cerenius L, Soderhall K 2013. Variable immune molecules in invertebrates. J. Exp. Biol. 216:4313–19
    [Google Scholar]
  34. Charmantier A, Gienapp P 2014. Climate change and timing of avian breeding and migration: evolutionary versus plastic changes. Evol. Appl. 7:15–28
    [Google Scholar]
  35. Chen WL, Koide RT, Adams TS, DeForest JL, Cheng L, Eissenstat DM 2016. Root morphology and mycorrhizal symbioses together shape nutrient foraging strategies of temperate trees. PNAS 113:8741–46
    [Google Scholar]
  36. Chevalier C, Stojanovic O, Colin DJ, Suarez-Zamorano N, Tarallo V et al. 2015. Gut microbiota orchestrates energy homeostasis during cold. Cell 163:1360–74
    [Google Scholar]
  37. Chevin L-M, Gallet R, Gomulkiewicz R, Holt RD, Fellous S 2013. Phenotypic plasticity in evolutionary rescue experiments. Philos. Trans. R. Soc. B 368:20120089
    [Google Scholar]
  38. Chevin L-M, Lande R 2010. When do adaptive plasticity and genetic evolution prevent extinction of a density regulated population. Evolution 64:1143–50
    [Google Scholar]
  39. Chevin L-M, Lande R, Mace GM 2010. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLOS Biol 8:8
    [Google Scholar]
  40. Cohen JD, McClure SM, Yu AJ 2007. Should I stay or should I go? How the human brain manages the trade-off between exploitation and exploration. Philos. Trans. R. Soc. B 362:933–42
    [Google Scholar]
  41. Congdon KA, Hammond AS, Ravosa MJ 2012. Differential limb loading in miniature pigs (Sus scrofa domesticus): a test of chondral modeling theory. J. Exp. Biol. 215:1472–83
    [Google Scholar]
  42. Cook SA, Johnson MP 1968. Adaptation to heterogeneous environments. I. Variation in heterophylly in Ranunculus flammula L. Evolution 22:496–516
    [Google Scholar]
  43. Costantini D. 2014. Does hormesis foster organism resistance to extreme events. Front. Ecol. Environ. 12:209–10
    [Google Scholar]
  44. Costantini D, Metcalfe NB, Monaghan P 2010. Ecological processes in a hormetic framework. Ecol. Lett. 13:1435–47
    [Google Scholar]
  45. Costantini D, Monaghan P, Metcalfe NB 2014. Prior hormetic priming is costly under environmental mismatch. Biol. Lett. 10:20131010
    [Google Scholar]
  46. Crispo E. 2007. The Baldwin effect and genetic assimilation: revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity. Evolution 61:2469–79
    [Google Scholar]
  47. Cumbo VR, Baird AH, van Oppen MJH 2013. The promiscuous larvae: flexibility in the establishment of symbiosis in corals. Coral Reefs 32:111–20
    [Google Scholar]
  48. Dall SRX, Giraldeau LA, Olsson O, McNamara JM, Stephens DW 2005. Information and its use by animals in evolutionary ecology. Trends Ecol. Evol. 20:187–93
    [Google Scholar]
  49. Davies PF. 1995. Flow mediated endothelial mechanotransduction. Physiol. Rev. 75:519–60
    [Google Scholar]
  50. Davis JM, Stamps JA 2004. The effect of natal experience on habitat preferences. Trends Ecol. Evol. 19:411–16
    [Google Scholar]
  51. de Kroon H, Huber H, Stuefer JF, van Groenendael JM 2005. A modular concept of phenotypic plasticity in plants. New Phytol 166:73–82
    [Google Scholar]
  52. Deak M, Horvath GV, Davletova S, Torok K, Sass L et al. 1999. Plants ectopically expressing the iron-binding protein, ferritin, are tolerant to oxidative damage and pathogens. Nat. Biotechnol. 17:192–96
    [Google Scholar]
  53. Demas G, Greives T, Chester E, French S 2012. The energetics of immunity. See Demas & Nelson 2012 259–96
  54. Demas G, Nelson R 2012. Ecoimmunology Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  55. Despres L, David JP, Gallet C 2007. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 22:298–307
    [Google Scholar]
  56. DeWitt TJ, Sih A, Wilson DS 1998. Costs and limits of phenotypic plasticity. Trends Ecol. Evol. 13:77–81
    [Google Scholar]
  57. Di Croce L, Helin K 2013. Transcriptional regulation by Polycomb group proteins. Nat. Struct. Mol. Biol. 20:1147–55
    [Google Scholar]
  58. Ding Y, Fromm M, Avramova Z 2012. Multiple exposures to drought ‘train’ transcriptional responses in Arabidopsis. Nat. Commun 3:9
    [Google Scholar]
  59. Donelson JM, Munday PL, McCormick MI, Pitcher CR 2012. Rapid transgenerational acclimation of a tropical reef fish to climate change. Nat. Clim. Change 2:30–32
    [Google Scholar]
  60. Doust LL. 1981. Population dynamics and local specialization in a clonal perennial (Ranunculus repens). 1. The dynamics of ramets in contrasting habitats. J. Ecol. 69:743–55
    [Google Scholar]
  61. Ducher G, Prouteau S, Courteix D, Benhamou CL 2004. Cortical and trabecular bone at the forearm show different adaptation patterns in response to tennis playing. J. Clin. Densitom. 7:399–405
    [Google Scholar]
  62. Dukas R. 1998. Evolutionary ecology of learning. Cognitive Ecology: The Evolutionary Ecology of Information Processing and Decision Making R Dukas 129–74 Chicago: Univ. Chicago Press
    [Google Scholar]
  63. Duncan RL, Turner CH 1995. Mechanitransduction and the functional response of bone to mechanical strain. Calcif. Tissue Int. 57:344–58
    [Google Scholar]
  64. Duputie A, Rutschmann A, Ronce O, Chuine I 2015. Phenological plasticity will not help all species adapt to climate change. Glob. Change Biol. 21:3062–73
    [Google Scholar]
  65. Ebert MS, Sharp PA 2012. Roles for microRNAs in conferring robustness to biological processes. Cell 149:515–24
    [Google Scholar]
  66. Edelaar P, Bolnick DI 2012. Non-random gene flow: an underappreciated force in evolution and ecology. Trends Ecol. Evol. 27:659–65
    [Google Scholar]
  67. Efferth T, Volm M 2017. Multiple resistance to carcinogens and xenobiotics: P-glycoproteins as universal detoxifiers. Arch. Toxicol. 91:2515–38
    [Google Scholar]
  68. Ehrenreich IM, Pfennig DW 2016. Genetic assimilation: a review of its potential proximate causes and evolutionary consequences. Ann. Bot. 117:769–79
    [Google Scholar]
  69. Eldar A, Elowitz MB 2010. Functional roles for noise in genetic circuits. Nature 467:167–73
    [Google Scholar]
  70. Eliassen S, Jorgensen C, Mangel M, Giske J 2007. Exploration or exploitation: Life expectancy changes the value of learning in foraging strategies. Oikos 116:513–23
    [Google Scholar]
  71. Ellis EC, Ramankutty N 2008. Putting people in the map: anthropogenic biomes of the world. Front. Ecol. Environ. 6:439–47
    [Google Scholar]
  72. Feder ME, Hofmann GE 1999. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 61:243–82
    [Google Scholar]
  73. Feinberg AP, Irizarry RA 2010. Stochastic epigenetic variation as a driving force of development, evolutionary adaptation, and disease. PNAS 107:1757–64
    [Google Scholar]
  74. Fischer EK, Ghalambor CK, Hoke KL 2016. Plasticity and evolution in correlated suites of traits. J. Evol. Biol. 29:991–1002
    [Google Scholar]
  75. Francis NJ, Kingston RE 2001. Mechanisms of transcriptional memory. Nat. Rev. Mol. Cell Biol. 2:409–21
    [Google Scholar]
  76. Frank S. 1996. The design of natural and artificial adaptive systems. Adaptation M Rose, G Lauder 451–505 New York: Academic
    [Google Scholar]
  77. Franklin KA. 2008. Shade avoidance. New Phytol 179:930–44
    [Google Scholar]
  78. Franks SJ, Weber JJ, Aitken SN 2014. Evolutionary and plastic responses to climate change in terrestrial plant populations. Evol. Appl. 7:123–39
    [Google Scholar]
  79. Futuyma DJ, Moreno G 1988. The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19:207–33
    [Google Scholar]
  80. Galvan I, Bonisoli-Alquati A, Jenkinson S, Ghanem G, Wakamatsu K et al. 2014. Chronic exposure to low-dose radiation at Chernobyl favours adaptation to oxidative stress in birds. Funct. Ecol. 28:1387–403
    [Google Scholar]
  81. Garud N, Good B, Hallatschek O, Pollard K 2017. Evolutionary dynamics of bacteria in the gut microbiome within and across hosts. bioRxiv 210955. https://doi.org/10.1101/210955
    [Crossref]
  82. Gerschman R, Gilbert DL, Nye SW, Dwyer P, Fenn WO 1954. Oxygen poisoning and X-irradiation: a mechanism in common. Science 119:623–26
    [Google Scholar]
  83. Ghalambor CK, McKay JK, Carrol 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]
  84. Gilbert SF, McDonald E, Boyle N, Buttino N, Gyi L et al. 2010. Symbiosis as a source of selectable epigenetic variation: taking the heat for the big guy. Philos. Trans. R. Soc. B 365:671–78
    [Google Scholar]
  85. Gilchrest BA, Park HY, Eller MS, Yaar M 1996. Mechanisms of ultraviolet light-induced pigmentation. Photochem. Photobiol. 63:1–10
    [Google Scholar]
  86. Glanville J, Zhai WW, Berka J, Telman D, Huerta G et al. 2009. Precise determination of the diversity of a combinatorial antibody library gives insight into the human immunoglobulin repertoire. PNAS 106:20216–21
    [Google Scholar]
  87. Gloss AD, Vassao DG, Hailey AL, Dittrich ACN, Schramm K et al. 2014. Evolution in an ancient detoxification pathway is coupled with a transition to herbivory in the Drosophilidae. Mol. Biol. Evol. 31:2441–56
    [Google Scholar]
  88. Gomulkiewicz R, Holt RD 1995. When does evolution by natural selection prevent extinction?. Evolution 49:201–7
    [Google Scholar]
  89. Gonzalez-Voyer A, Gonzalez-Suarez M, Vila C, Revilla E 2016. Larger brain size indirectly increases vulnerability to extinction in mammals. Evolution 70:1364–75
    [Google Scholar]
  90. Gonzalez FJ. 2005. Role of cytochromes P450 in chemical toxicity and oxidative stress: studies with CYP2E1. Mutat. Res. 569:101–10
    [Google Scholar]
  91. Gopnik A, O'Grady S, Lucas CG, Griffiths TL, Wente A et al. 2017. Changes in cognitive flexibility and hypothesis search across human life history from childhood to adolescence to adulthood. PNAS 114:7892–99
    [Google Scholar]
  92. Gordon JA, Stryker MP 1996. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J. Neurosci. 16:3274–86
    [Google Scholar]
  93. Grindstaff JL. 2008. Maternal antibodies reduce costs of an immune response during development. J. Exp. Biol. 211:654–60
    [Google Scholar]
  94. Gruber J, Tang SY, Halliwell B 2007. Evidence for a trade-off between survival and fitness caused by resveratrol treatment of Caenorhabditis elegans. Biogerontology 1100:530–42
    [Google Scholar]
  95. Guillemin K, Groppe J, Ducker K, Treisman R, Hafen E et al. 1996. The pruned gene encodes the Drosophila serum response factor and regulates cytoplasmic outgrowth during terminal branching of the tracheal system. Development 122:1353–62
    [Google Scholar]
  96. Hamann E, Puijalon S 2013. Biomechanical responses of aquatic plants to aerial conditions. Ann. Bot. 112:1869–78
    [Google Scholar]
  97. Hammond AS, Ning J, Ward CV, Ravosa MJ 2010. Mammalian limb loading and chondral modeling during ontogeny. Anat. Rec. 293:658–70
    [Google Scholar]
  98. Herman JJ, Sultan SE 2011. Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations. Front. Plant Sci. 2:102
    [Google Scholar]
  99. Hodge A. 2004. The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24
    [Google Scholar]
  100. Hoffmann A, Parsons P 1997. Extreme Environmental Change and Evolution Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  101. Honjo T, Habu S 1985. Origin of immune diversity: genetic variation and selection. Annu. Rev. Biochem. 54:803–30
    [Google Scholar]
  102. Houthoofd W, Jacobsen K, Mertens C, Vangestel S, Coomans A, Borgonie G 2003. Embryonic cell lineage of the marine nematode Pellioditis marina. Dev. Biol 258:57–69
    [Google Scholar]
  103. Hove JR, Koster RW, Forouhar AS, Acevedo-Bolton G, Fraser SE, Gharib M 2003. Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421:172–77
    [Google Scholar]
  104. Huerta R, Nowotny T, Garcia-Sanchez M, Abarbanel HDI, Rabinovich MI 2004. Learning classification in the olfactory system of insects. Neural Comput 16:1601–40
    [Google Scholar]
  105. Hull DL, Langman RE, Glenn SS 2001. A general account of selection: biology, immunology, and behavior. Behav. Brain Sci. 24:511–73
    [Google Scholar]
  106. Isler K, van Schaik CP 2009. The expensive brain: a framework for explaining evolutionary changes in brain size. J. Hum. Evol. 57:392–400
    [Google Scholar]
  107. Iwaniuk AN, Nelson JE 2003. Developmental differences are correlated with relative brain size in birds: a comparative analysis. Can. J. Zool. 81:1913–28
    [Google Scholar]
  108. Johnston LA. 2009. Competitive interactions between cells: death, growth, and geography. Science 324:1679–82
    [Google Scholar]
  109. Kaelbling LP, Littman ML, Moore AW 1996. Reinforcement learning: a survey. J. Artif. Intell. Res. 4:237–85
    [Google Scholar]
  110. Kaplan H, Hill K, Lancaster J, Hurtado AM 2000. A theory of human life history evolution: diet, intelligence, and longevity. Evol. Anthropol. 9:156–85
    [Google Scholar]
  111. Katz LC, Shatz CJ 1996. Synaptic activity and the construction of cortical circuits. Science 274:1133–38
    [Google Scholar]
  112. Kembel SW, Cahill JF 2005. Plant phenotypic plasticity belowground: a phylogenetic perspective on root foraging trade-offs. Am. Nat. 166:216–30
    [Google Scholar]
  113. Kensler TW, Wakabayash N, Biswal S 2007. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 47:89–116
    [Google Scholar]
  114. Keppler C, Ringwood AH 2001. Expression of P-glycoprotein in the gills of oysters, Crassostrea virginica: seasonal and pollutant related effects. Aquat. Toxicol. 54:195–204
    [Google Scholar]
  115. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O et al. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–82
    [Google Scholar]
  116. Kirschner M, Gerhart J 1998. Evolvability. PNAS 95:8420–27
    [Google Scholar]
  117. Koga R, Tsuchida T, Fukatsu T 2003. Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc. R. Soc. B 270:2543–50
    [Google Scholar]
  118. Kotrschal A, Rogell B, Bundsen A, Svensson B, Zajitschek S et al. 2013. Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain. Curr. Biol. 23:168–71
    [Google Scholar]
  119. Krammer PH. 2000. CD95’s deadly mission in the immune system. Nature 407:789–95
    [Google Scholar]
  120. Kregel KC. 2002. Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J. Appl. Physiol. 92:2177–86
    [Google Scholar]
  121. Kubinak J, Nelson A, Ruff J, Potts W 2012. Trade-offs limiting MHC heterozygosity. See Demas & Nelson 2012 225–58
  122. Kurtz J, Armitage SAO 2006. Alternative adaptive immunity in invertebrates. Trends Immunol 27:493–96
    [Google Scholar]
  123. Kussell E, Leibler S 2005. Phenotypic diversity, population growth, and information in fluctuating environments. Science 309:2075–78
    [Google Scholar]
  124. Lande R. 1998. Anthropogenic, ecological and genetic factors in extinction and conservation. Res. Popul. Ecol. 40:259–69
    [Google Scholar]
  125. Lande R. 2009. Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J. Evol. Biol. 22:1435–46
    [Google Scholar]
  126. Langkilde T, Thawley CJ, Robbins TR 2017. Behavioral adaptations to invasive species: benefits, costs, and mechanisms of change. Adv. Study Behav. 49:199–235
    [Google Scholar]
  127. Laughlin SB, van Steveninck RRD, Anderson JC 1998. The metabolic cost of neural information. Nat. Neurosci. 1:36–41
    [Google Scholar]
  128. Laverty TM, Plowright RC 1988. Flower handling by bumblebees: a comparison of specialists and generalists. Anim. Behav. 36:733–40
    [Google Scholar]
  129. Ledon-Rettig CC, Pfennig DW, Crespi EJ 2010. Diet and hormonal manipulation reveal cryptic genetic variation: implications for the evolution of novel feeding strategies. Proc. R. Soc. B 277:3569–78
    [Google Scholar]
  130. Levy SF, Siegal ML 2008. Network hubs buffer environmental variation in Saccharomyces cerevisiae. PLOS Biol 6:2588–604
    [Google Scholar]
  131. Ley RE, Peterson DA, Gordon JI 2006. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–48
    [Google Scholar]
  132. Li XC, Baudry J, Berenbaum MR, Schuler MA 2004. Structural and functional divergence of insect CYP6B proteins: from specialist to generalist cytochrome P450. PNAS 101:2939–44
    [Google Scholar]
  133. Li XC, Schuler MA, Berenbaum MR 2007. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu. Rev. Entomol. 52:231–53
    [Google Scholar]
  134. Litman GW, Rast JP, Shamblott MJ, Haire RN, Hulst M et al. 1993. Phylogenetic diversification of immunoglobulin genes and the antibody repertoire. Mol. Biol. Evol. 10:60–72
    [Google Scholar]
  135. Lochmiller RL, Deerenberg C 2000. Trade-offs in evolutionary immunology: Just what is the cost of immunity?. Oikos 88:87–98
    [Google Scholar]
  136. Luo LQ, O'Leary DDM 2005. Axon retraction and degeneration in development and disease. Annu. Rev. Neurosci. 28:127–56
    [Google Scholar]
  137. Lynch M. 2010. Rate, molecular spectrum, and consequences of human mutation. PNAS 107:961–68
    [Google Scholar]
  138. Maklakov AA, Immler S, Gonzalez-Voyer A, Ronn J, Kolm N 2011. Brains and the city: Big-brained passerine birds succeed in urban environments. Biol. Lett. 7:730–32
    [Google Scholar]
  139. Marshall KE, Sinclair BJ 2010. Repeated stress exposure results in a survival-reproduction trade-off in Drosophila melanogaster. Proc. R. Soc. B 277:963–69
    [Google Scholar]
  140. Martin LB, Navara KJ, Weil ZM, Nelson RJ 2007. Immunological memory is compromised by food restriction in deer mice Peromyscus maniculatus. Am. J. Physiol 292:R316–20
    [Google Scholar]
  141. Marzluff J, Shulenberger E, Endlicher W, Alberti M, Bradley G et al., eds. 2008. Urban Ecology: An International Perspective on the Interaction Between Humans and Nature New York: Springer
    [Google Scholar]
  142. Mattson MP. 2008. Hormesis and disease resistance: activation of cellular stress response pathways. Hum. Exp. Toxicol. 27:155–62
    [Google Scholar]
  143. Mazzocchi F. 2008. Complexity in biology: exceeding the limits of reductionism and determinism using complexity theory. EMBO Rep 9:10–14
    [Google Scholar]
  144. McAdams HH, Arkin A 1997. Stochastic mechanisms in gene expression. PNAS 94:814–19
    [Google Scholar]
  145. Menegaz RA, Sublett SV, Figueroa SD, Hoffman TJ, Ravosa MJ, Aldridge K 2010. Evidence for the influence of diet on cranial form and robusticity. Anat. Rec. 293:630–41
    [Google Scholar]
  146. Mery F, Kawecki TJ 2004. An operating cost of learning in Drosophila melanogaster. Anim. Behav 68:589–98
    [Google Scholar]
  147. Meyer A. 1987. Phenotypic plasticity and heterochrony in Cichlasoma managuense (Pisces, Chichlidae) and their implications for speciation in cichlid fishes. Evolution 41:1357–69
    [Google Scholar]
  148. Miller-Jensen K, Dey SS, Schaffer DV, Arkin AP 2011. Varying virulence: epigenetic control of expression noise and disease processes. Trends Biotechnol 29:517–25
    [Google Scholar]
  149. Mitchell SE, Read AF 2005. Poor maternal environment enhances offspring disease resistance in an invertebrate. Proc. R. Soc. B 272:2601–7
    [Google Scholar]
  150. Mladenovic N, Hansen P 1997. Variable neighborhood search. Comput. Oper. Res. 24:1097–100
    [Google Scholar]
  151. Moczek AP, Emlen DJ 2000. Male horn dimorphism in the scarab beetle, Onthophagus taurus: Do alternative reproductive tactics favor alternative phenotypes?. Anim. Behav. 59:459–66
    [Google Scholar]
  152. Moore SW. 2003. Scrambled eggs: mechanical forces as ecological factors in early development. Evol. Dev 5:61–66
    [Google Scholar]
  153. Moran NA. 1992. The evolutionary maintenance of alternative phenotypes. Am. Nat. 139:971–89
    [Google Scholar]
  154. Moret Y, Schmid-Hempel P 2000. Survival for immunity: the price of immune system activation for bumblebee workers. Science 290:1166–68
    [Google Scholar]
  155. Murren CJ, Auld JR, Callahan H, Ghalambor CK, Handelsman CA et al. 2015. Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity. Heredity 115:293–301
    [Google Scholar]
  156. Nielsen ME. 2017. No geographic variation in thermoregulatory colour plasticity and limited variation in heat-avoidance behaviour in Battus philenor caterpillars. J. Evol. Biol. 30:1919–28
    [Google Scholar]
  157. Nijhout HF. 1999. Control mechanisms of polyphenic development in insects: In polyphenic development, environmental factors alter same aspects of development in an orderly and predictable way. Bioscience 49:181–92
    [Google Scholar]
  158. Niklas KJ. 2009. Functional adaptation and phenotypic plasticity at the cellular and whole plant level. J. Biosci. 34:613–20
    [Google Scholar]
  159. Oppenheim RW. 1991. Cell death during development of the nervous system. Annu. Rev. Neurosci. 14:453–501
    [Google Scholar]
  160. Papaj DR, Prokopy RJ 1989. Ecological and evolutionary aspects of learning in phytophagous insects. Annu. Rev. Entomol. 34:315–50
    [Google Scholar]
  161. Pette D, Staron RS 2000. Myosin isoforms, muscle fiber types, and transitions. Microsc. Res. Tech. 50:500–9
    [Google Scholar]
  162. Pigliucci M, Murren CJ 2003. Genetic assimilation and a possible evolutionary paradox: Can macroevolution sometimes be so fast as to pass us by. Evolution 57:1455–64
    [Google Scholar]
  163. Pillai P, Gouhier TC, Vollmer SV 2017. Ecological rescue of host-microbial systems under environmental change. Theor. Ecol. 10:51–63
    [Google Scholar]
  164. Price TD, Qvarnström A, Irwin DE 2003. The role of phenotypic plasticity in driving genetic evolution. Proc. R. Soc. B 270:1433–40
    [Google Scholar]
  165. Purchase CF, Moreau DTR 2012. Stressful environments induce novel phenotypic variation: hierarchical reaction norms for sperm performance of a pervasive invader. Ecol. Evol. 2:2562–71
    [Google Scholar]
  166. Purves D, Lichtman JW 1980. Elimination of synapses in the developing nervous system. Science 210:153–57
    [Google Scholar]
  167. Ragsdale EJ, Muller MR, Rodelsperger C, Sommer RJ 2013. A developmental switch coupled to the evolution of plasticity acts through a sulfatase. Cell 155:922–33
    [Google Scholar]
  168. Raj A, Peskin CS, Tranchina D, Vargas DY, Tyagi S 2006. Stochastic mRNA synthesis in mammalian cells. PLOS Biol 4:1707–19
    [Google Scholar]
  169. Raj A, van Oudenaarden A 2008. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135:216–26
    [Google Scholar]
  170. Rajewsky K. 1996. Clonal selection and learning in the antibody system. Nature 381:751–58
    [Google Scholar]
  171. Rautio M, Korhola A 2002. UV-induced pigmentation in subarctic Daphnia. Limnol. Oceanogr 47:295–99
    [Google Scholar]
  172. Ravigne V, Dieckmann U, Olivieri I 2009. Live where you thrive: Joint evolution of habitat choice and local adaptation facilitates specialization and promotes diversity. Am. Nat. 174:E141–69
    [Google Scholar]
  173. Reznick D, Nunney L, Tessier A 2000. Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol. Evol. 15:421–25
    [Google Scholar]
  174. Riechers DE, Kreuz K, Zhang Q 2010. Detoxification without intoxication: Herbicide safeners activate plant defense gene expression. Plant Physiol 153:3–13
    [Google Scholar]
  175. Risau W. 1997. Mechanisms of angiogenesis. Nature 386:671–74
    [Google Scholar]
  176. Roff D. 2001. Life History Evolution Sunderland, MA: Sinauer
    [Google Scholar]
  177. Romiguier J, Gayral P, Ballenghien M, Bernard A, Cahais V et al. 2014. Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature 515:261–43
    [Google Scholar]
  178. Ruiz-Gonzalez MX, Moret Y, Brown MJF 2009. Rapid induction of immune density-dependent prophylaxis in adult social insects. Biol. Lett. 5:781–83
    [Google Scholar]
  179. Rutherford SL, Lindquist S 1998. Hsp90 as a capacitor for morphological evolution. Nature 396:336–42
    [Google Scholar]
  180. Sachs T. 2004. Self-organization of tree form: a model for complex social systems. J. Theor. Biol. 230:197–202
    [Google Scholar]
  181. Sachs T, Novoplansky A, Cohen D 1993. Plants as competing populations of redundant organs. Plant Cell Environ 16:765–70
    [Google Scholar]
  182. Sanchis-Moysi J, Idoate F, Izquierdo M, Calbet JAL, Dorado C 2011. Iliopsoas and gluteal muscles are asymmetric in tennis players but not in soccer players. PLOS ONE 6:10
    [Google Scholar]
  183. Scheiner SM. 2016. Habitat choice and temporal variation alter the balance between adaptation by genetic differentiation, a jack-of-all-trades strategy, and phenotypic plasticity. Am. Nat. 187:633–46
    [Google Scholar]
  184. Schlichting CD. 2008. Hidden reaction norms, cryptic genetic variation, and evolvability. Year in Evolutionary Biology 2008187–203 Oxford, UK: Blackwell
    [Google Scholar]
  185. Schlichting CD, Pigliucci M 1998. Phenotypic Evolution: A Reaction Norm Perspective Sunderland, MA: Sinauer
    [Google Scholar]
  186. Schluter J, Foster KR 2012. The evolution of mutualism in gut microbiota via host epithelial selection. PLOS Biol 10:e1001424
    [Google Scholar]
  187. Schmid-Hempel P. 2003. Variation in immune defence as a question of evolutionary ecology. Proc. R. Soc. B 270:357–66
    [Google Scholar]
  188. Schramm K, Vassao DG, Reichelt M, Gershenzon J, Wittstock U 2012. Metabolism of glucosinolate-derived isothiocyanates to glutathione conjugates in generalist lepidopteran herbivores. Insect Biochem. Mol. Biol. 42:174–82
    [Google Scholar]
  189. Schuler MA. 2011. P450s in plant-insect interactions. Biochim. Biophys. Acta 1814:36–45
    [Google Scholar]
  190. Shephard AM, Bharwani A, Durisko Z, Andrews PW 2016. Reverse engineering the febrile system. Q. Rev. Biol. 91:419–57
    [Google Scholar]
  191. Shettleworth S. 1998. Cognition, Evolution and Behavior Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  192. Sih A, Ferrari MCO, Harris DJ 2011. Evolution and behavioural responses to human-induced rapid environmental change. Evol. Appl. 4:367–87
    [Google Scholar]
  193. Sikkink KL, Reynolds RM, Cresko WA, Phillips PC 2015. Environmentally induced changes in correlated responses to selection reveal variable pleiotropy across a complex genetic network. Evolution 69:1128–42
    [Google Scholar]
  194. Singh S, Brocker C, Koppaka V, Chen Y, Jackson BC et al. 2013. Aldehyde dehydrogenases in cellular responses to oxidative/electrophilic stress. Free Radic. Biol. Med. 56:89–101
    [Google Scholar]
  195. Snell-Rood EC. 2012. Selective processes in development: implications for the costs and benefits of phenotypic plasticity. Integr. Comp. Biol. 52:31–42
    [Google Scholar]
  196. Snell-Rood EC. 2013. An overview of the evolutionary causes and consequences of behavioural plasticity. Anim. Behav. 85:1004–11
    [Google Scholar]
  197. Snell-Rood EC, Burger M, Hutton Q, Moczek AP 2016. Effects of parental care on the accumulation and release of cryptic genetic variation: review of mechanisms and a case study of dung beetles. Evol. Ecol. 30:251–65
    [Google Scholar]
  198. Snell-Rood EC, Cash A, Han MV, Kijimoto T, Andrews J, Moczek AP 2011a. Developmental decoupling of alternative phenotypes: insights from the transcriptomes of horn polyphenic beetles. Evolution 65:231–45
    [Google Scholar]
  199. Snell-Rood EC, Cothran R, Espeset A, Jeyasingh P, Hobbie S, Morehouse N 2015a. Life-history evolution in the anthropocene: effects of increasing nutrients on traits and trade-offs. Evol. Appl. 8:635–49
    [Google Scholar]
  200. Snell-Rood EC, Davidowitz G, Papaj DR 2011b. Reproductive trade-offs of learning in a butterfly. Behav. Ecol. 22:291–302
    [Google Scholar]
  201. Snell-Rood EC, Swanson EM, Young RL 2015b. Life history as a constraint on plasticity: Developmental timing is correlated with phenotypic variation in birds. Heredity 115:379–88
    [Google Scholar]
  202. Snell-Rood EC, Van Dyken JD, Cruickshank T, Wade M, Moczek A 2010. Toward a population genetic framework of developmental evolution: costs, limits, and consequences of phenotypic plasticity. BioEssays 32:71–81
    [Google Scholar]
  203. Sol D. 2009. Revisiting the cognitive buffer hypothesis for the evolution of large brains. Biol. Lett. 5:130–33
    [Google Scholar]
  204. Sol D, Duncan RP, Blackburn TM, Cassey P, Lefebvre L 2005. Big brains, enhanced cognition, and response of birds to novel environments. PNAS 102:5460–65
    [Google Scholar]
  205. Speck T, Burgert I 2011. Plant stems: functional design and mechanics. Annu. Rev. Mater. Res. 41:169–93
    [Google Scholar]
  206. Sporns O, Tononi G, Edelman GM 2000. Connectivity and complexity: the relationship between neuroanatomy and brain dynamics. Neural Netw 13:909–22
    [Google Scholar]
  207. Stamps JA, Frankenhuis WE 2016. Bayesian models of development. Trends Ecol. Evol. 31:260–68
    [Google Scholar]
  208. Stearns SC. 2000. Life history evolution: successes, limitations, and prospects. Naturwissenschaften 87:476–86
    [Google Scholar]
  209. Steinger T, Roy BA, Stanton ML 2003. Evolution in stressful environments II: adaptive value and costs of plasticity in response to low light in Sinapis arvensis. J. Evol. Biol 16:313–23
    [Google Scholar]
  210. Sultan SE, Spencer HG 2002. Metapopulation structure favors plasticity over local adaptation. Am. Nat. 160:271–83
    [Google Scholar]
  211. Tamori Y, Deng WM 2011. Cell competition and its implications for development and cancer. J. Genet. Genom. 38:483–95
    [Google Scholar]
  212. Telemeco RS, Fletcher B, Levy O, Riley A, Rodriguez-Sanchez Y et al. 2017. Lizards fail to plastically adjust nesting behavior or thermal tolerance as needed to buffer populations from climate warming. Glob. Change Biol. 23:1075–84
    [Google Scholar]
  213. Thattai M, van Oudenaarden A 2004. Stochastic gene expression in fluctuating environments. Genetics 167:523–30
    [Google Scholar]
  214. Turner PE, Elena SF 2000. Cost of host radiation in an RNA virus. Genetics 156:1465–70
    [Google Scholar]
  215. Van Buskirk J 2000. The costs of an inducible defense in anuran larvae. Ecology 81:2813–21
    [Google Scholar]
  216. Van Buskirk J, Steiner UK 2009. The fitness costs of developmental canalization and plasticity. J. Evol. Biol. 22:852–60
    [Google Scholar]
  217. Van de Peer T, Verheyen K, Kint V, Van Cleemput E, Muys B 2017. Plasticity of tree architecture through interspecific and intraspecific competition in a young experimental plantation. For. Ecol. Manag. 385:1–9
    [Google Scholar]
  218. van Kleunen M, Fischer M, Schmid B 2000. Costs of plasticity in foraging characteristics of the clonal plant Ranunculus reptans. Evolution 54:1947–55
    [Google Scholar]
  219. van Noordwijk AJ, de Jong G 1986. Acquisition and allocation of resources: their influence on variation in life history tactics. Am. Nat. 128:137–42
    [Google Scholar]
  220. van Praag H, Kempermann G, Gage FH 2000. Neural consequences of environmental enrichment. Nat. Rev. Neurosci. 1:191–98
    [Google Scholar]
  221. Van Tienderen PH 1991. Evolution of generalists and specialists in spatially heterogeneous environments. Evolution 45:1317–31
    [Google Scholar]
  222. Visser ME. 2008. Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc. R. Soc. B 275:649–59
    [Google Scholar]
  223. Wainwright PC, Osenberg CW, Mittelbach GG 1991. Trophic polymorphism in the pumpkinseed sunfish (Lepomis gibbosus Linnaeus): effects of environment on ontogeny. Funct. Ecol. 5:40–55
    [Google Scholar]
  224. Wang WX, Vinocur B, Shoseyov O, Altman A 2004. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–52
    [Google Scholar]
  225. Watson FL, Puttmann-Holgado R, Thomas F, Lamar DL, Hughes M et al. 2005. Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309:1874–78
    [Google Scholar]
  226. Weinig C, Johnston J, German ZM, Demink LM 2006. Local and global costs of adaptive plasticity to density in Arabidopsis thaliana. Am. Nat 167:826–36
    [Google Scholar]
  227. Weinstein JA, Jiang N, White RA, Fisher DS, Quake SR 2009. High-throughput sequencing of the zebrafish antibody repertoire. Science 324:807–10
    [Google Scholar]
  228. West-Eberhard MJ. 2003. Developmental Plasticity and Evolution New York: Oxford Univ. Press
    [Google Scholar]
  229. Wheeler DE. 1991. The developmental basis of worker caste polymorphism in ants. Am. Nat. 138:1218–38
    [Google Scholar]
  230. Whitlock MC. 1996. The red queen beats the jack-of-all-trades: the limitations on the evolution of phenotypic plasticity and niche breadth. Am. Nat. 148:S65–S77
    [Google Scholar]
  231. Wilson K, Reeson AF 1998. Density-dependent prophylaxis: evidence from Lepidoptera-baculovirus interactions?. Ecol. Entomol. 23:100–1
    [Google Scholar]
  232. Wood CW, Brodie ED 2015. Environmental effects on the structure of the G-matrix. Evolution 69:2927–40
    [Google Scholar]
  233. Yi HY, Chowdhury M, Huang YD, Yu XQ 2014. Insect antimicrobial peptides and their applications. Appl. Microbiol. Biotechnol. 98:5807–22
    [Google Scholar]
  234. Zuk M, Stoehr AM 2002. Immune defense and host life history. Am. Nat. 160:S9–22
    [Google Scholar]
/content/journals/10.1146/annurev-ecolsys-110617-062622
Loading
/content/journals/10.1146/annurev-ecolsys-110617-062622
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error