The information value of non-genetic inheritance in plants and animals

PLoS ONE

Volumn 10, Issue 1, 2015, Pages

  English, Sinead ^a   Pen, Ido ^b   Shea, Nicholas ^c   Uller, Tobias ^a,d  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CAMPANULASTRUM AMERICANUM; CONTROLLED STUDY; ENVIRONMENTAL CHANGE; ENVIRONMENTAL FACTOR; EVOLUTIONARY ADAPTATION; GENE FREQUENCY; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; GERMINATION; HERB; INHERITANCE; NONHUMAN; PHENOTYPE; PREDICTION; SCHISTOCERCA GREGARIA; SEED DISPERSAL; ANIMAL; GENETIC SELECTION; HEREDITY; METABOLISM; PHYSIOLOGY; PLANT;

ANIMALIA; SCHISTOCERCA GREGARIA;

ANIMALS; HEREDITY; PLANTS; SELECTION, GENETIC;

EID: 84928923233     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0116996     Document Type: Article

References (83)

1. Uller T (2012) Parental effects in development and evolution. In: Royle NJ, Smiseth PT, Kölliker M, editors. The Evolution of Parental Care. Oxford, UK: Oxford University Press. pp. 247-266.
2. Jablonka E, Lamb MJ (2014) Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral, and Symbolic Variation in the History of Life. 2nd ed. Cambridge MA: MIT Press.
3. Uller T, Helanterä H (n. d.) Heredity in evolutionary theory. In: Huneman P, Walsh D, editors. Challenges to Evolutionary Biology: Development and Heredity. Oxford: Oxford University Press.
4. Cavalli-Sforza LL, Feldman MW (1981) Cultural Transmission and Evolution: A Quantitative Approach. Princeton, New Jersey: Princeton University Press.
5. Odling-Smee FJ, Laland KN, Feldman MW (2003) Nice Construction: The Neglected Process in Evolution. Monographs in Population Biology, 37. Princeton, New Jersey: Princeton University Press.
6. Richerson PJ, Boyd R (2005) Not by Genes Alone: How Culture Transformed Human Evolution. Chicago: University of Chicago Press.
7. Cheverud JM, Wolf JB (2009) The Genetics and Evolutionary Consequences of Maternal Effects. In: Maestripieri D, editor. Maternal Effects in Mammals. Chicago: University of Chicago Press. pp. 11-37.
8. Danchin É, Charmantier A, Champagne FA, Mesoudi A, Pujol B, et al. (2011) Beyond DNA: integrating inclusive inheritance into an extended theory of evolution. Nat Rev Genet 12:475-486. doi: 10.1038/nrg3028 PMID: 21681209
9. Uller T (2014) Evolutionary Perspectives on Transgenerational Epigenetics. In: Tollefsbol T, editor. Transgenerational Epigenetics. London: Academic Press. pp. 175-186.
10. Laland K, Odling-Smee FJ, Feldman MW (1996) The evolutionary consequences of niche construction: a theoretical investigation using two-locus theory. J Evol Biol 9:293-316. doi: 10.1046/j.1420-9101. 1996.9030293.x
11. Badyaev A, Uller T (2009) Parental effects in ecology and evolution: mechanisms, processes and implications. Philos Trans R SocB 364:1169-1177. doi: 10.1098/rstb.2008.0302
12. Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403-407. doi: 10.1016/S0169-5347 (98) 01472-4 PMID: 21238360
13. Uller T (2008) Developmental plasticity and the evolution of parental effects. Trends Ecol Evol 23:432-438. doi: 10.1016/j.tree.2008.04.005 PMID: 18586350
14. Mousseau TA, Dingle H (1991) Maternal effects in insect life histories. Annu Rev Entomol 36:511-534. doi: 10.1146/annurev. en. 36.010191.002455
15. Mousseau TA, Fox CW (1998) Maternal effects as adaptations. New York: Oxford University Press.
16. Galloway LF (2005) Maternal effects provide phenotypic adaptation to local environmental conditions. NewPhytol 166:93-99. doi: 10.1111/j.1469-8137.2004.01314.x PMID: 15760354
17. Hinde CA, Buchanan KL, Kilner RM (2009) Prenatal environmental effects match offspring begging to parental provisioning. Proc Biol Sci 276:2787-2794. doi: 10.1098/rspb.2009.0375 PMID: 19419982
18. Lock JE, Smiseth PT, Moore PJ, Moore AJ (2007) Coadaptation of prenatal and postnatal maternal effects. Am Nat 170:709-718. doi: 10.1086/521963 PMID: 17926293
19. Lacey EA (1991) Parental effects on life-history traits in plants. In: Dudley EC, editor. The Unity of Evolutionary Biology. Portland, Oregon: Dioscorides Press. pp. 735-744.
20. Marshall DJ (2008) Transgenerational plasticity in the sea: context-dependent maternal effects across the life history. Ecology 89:418-427. doi: 10.1890/07-0449.1 PMID: 18409431
21. Ventura AK, Worobey J (2013) Early Influences on the Development of Food Preferences. CurrBiol 23:R401-R408. doi: 10.1016/j.cub.2013.02.037 PMID: 23660363
22. Slagsvold T, Wiebe KL (2011) Social learning in birds and its role in shaping a foraging niche. Philos Trans R Soc Lond B Biol Sci 366:969-977. doi: 10.1098/rstb.2010.0343 PMID: 21357219
23. Galef BG, Laland KN (2005) Social Learning in Animals: Empirical Studies and Theoretical Models. Bioscience 55:489. doi: 10.1641/0006-3568 (2005) 055%5B0489:SLIAES%5D2.0. CO;2
24. Thornton A, McAuliffe K (2006) Teaching in wild meerkats. Science (80-) 313:227-229. doi: 10.1126/science.1128727
25. Revardel E, Franc A, Petit RJ (2010) Sex-biased dispersal promotes adaptive parental effects. BMC Evol Biol 10:217. doi: 10.1186/1471-2148-10-217 PMID: 20637098
26. Kuijper B, Johnstone RA, Townley S (2014) The evolution of multivariate maternal effects. PLoS Comput Biol 10:e1003550. doi: 10.1371/journal.pcbi.1003550 PMID: 24722346
27. Uller T, Pen I (2011) A Theoretical Model of the Evolution of Maternal Effects Under Parent-Offspring Conflict. Evolution 65:2075-2084. doi: 10.1111/j.1558-5646.2011.01282.x PMID: 21729061
28. McElreath R, Strimling P (2008) When Natural Selection Favors Imitation of Parents. Curr Anthropol 49:307-316. doi: 10.1086/524364
29. Takahasi K (1999) Theoretical aspects of the mode of transmission in cultural inheritance. Theor Popul Biol 55:208-225. doi: 10.1006/tpbi.1998.1400 PMID: 10329519
30. Boyd R, Richerson PJ (1985) Culture and the Evolutionary Process. Chicago: Chicago University Press.
31. Daxinger L, Whitelaw E (2012) Understanding transgenerational epigenetic inheritance via the gametes in mammals. Nat Rev Genet 13:153-162. PMID: 22290458
32. Day T, Bonduriansky R (2011) A unified approach to the evolutionary consequences of genetic and nongenetic inheritance. Am Nat 178:E18-36. doi: 10.1086/660911 PMID: 21750377
33. Furrow RE, Feldman MW (2014) Genetic variation and the evolution of epigenetic regulation. Evolution 68:673-683. doi: 10.1111/evo.12225 PMID: 24588347
34. Geoghegan JL, Spencer HG (2013) The evolutionary potential of paramutation: A population-epigenetic model. Theor Popul Biol 88:1-8. doi: 10.1016/j.tpb.2013.05.001 PMID: 23689020
35. Leimar O, Hammerstein P, Van Dooren TJM (2006) A new perspective on developmental plasticity and the principles of adaptive morph determination. Am Nat 167:367-376. doi: 10.1086/499566 PMID: 16673345
36. Shea N, Pen I, Uller T (2011) Three epigenetic information channels and their different roles in evolution. J Evol Biol 24:1178-1187. doi: 10.1111/j.1420-9101.2011.02235.x PMID: 21504495
37. Shannon CE (1949) The mathematical theory of communication. In: Shannon CE, Weaver W, editors. The Mathematical Theory of Communication. Urbana: University of Illinois Press.
38. Galloway LF, Etterson JR (2007) Transgenerational plasticity is adaptive in the wild. Science 318:1134-1136. doi: 10.1126/science.1148766 PMID: 18006745
39. Simpson SJ, Sword GA (2008) Locusts. Curr Biol 18:R364-6. doi: 10.1016/j.cub.2008.02.029 PMID: 18460311
40. Leimar O (2009) Environmental and genetic cues in the evolution of phenotypic polymorphism. Evol Ecol 23:125-135. doi: 10.1007/s10682-007-9194-4
41. West-Eberhard MJ (2003) Developmental Plasticity and Evolution. Oxford University Press.
42. Wolf JB, Wade MJ (2009) What are maternal effects (and what are they not)? Philos Trans R Soc B 364:1107-1115. doi: 10.1098/rstb.2008.0238
43. Jablonka E, Raz G (2009) Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol 84:131-176. doi: 10.1086/598822 PMID: 19606595
44. Lim JP, Brunet A (2013) Bridging the transgenerational gap with epigenetic memory. Trends Genet: 1-11. doi: 10.1016/j.tig.2012.12.008
45. Odling-Smee J (2010) Niche inheritance. Evolution: the extended synthesis. pp. 175-207.
46. Levins R (1968) Evolution in Changing Environments. Princeton: Princeton University Press.
47. Alpert P, Simms E (2002) The relative advantages of plasticity and fixity in different environments: when is it good for a plant to adjust? Evol Ecol 16:285-297. doi: 10.1023/A: 1019684612767
48. Miller GA, Islam MS, Claridge TDW, Dodgson T, Simpson SJ (2008) Swarm formation in the desert locust Schistocerca gregaria: isolation and NMR analysis of the primary maternal gregarizing agent. J Exp Biol 211:370-376. doi: 10.1242/jeb.013458 PMID: 18203992
49. Roach DA, Wulff RD (1987) Maternal Effects in Plants. Annu Rev Ecol Syst 18:209-235. doi: 10.1146/annurev. es.18.110187.001233
50. Rossiter M (1996) Incidence and Consequences of Inherited Environmental Effects. Annu Rev Ecol Syst 27:451-476. doi: 10.1146/annurev. ecolsys.27.1.451
51. Donohue K (2009) Completing the cycle: maternal effects as the missing link in plant life histories. Philos Trans RSoc LondB Biol Sci 364:1059-1074. doi: 10.1098/rstb.2008.0291 PMID: 19324611
52. Donohue K, Schmitt J (1998) Maternal environmental effects in plants: adaptive plasticity? In: Mousseau TA, Fox CW, editors. Maternal effects as adaptations. New York: Oxford University Press. pp. 137-158.
53. Jacobs BS, Lesmeister SA (2012) Maternal environmental effects on fitness, fruit morphology and ballistic seed dispersal distance in an annual forb. Funct Ecol 26:588-597. doi: 10.1111/j.1365-2435. 2012.01964.x
54. Herman JJ, Sultan SE (2011) Adaptive Transgenerational Plasticity in Plants: Case Studies, Mechanisms, and Implications for Natural Populations. Front Plant Sci 2:1-10. doi: 10.3389/fpls.2011.00102
55. Marshall DJ, Uller T (2007) When is a maternal effect adaptive? Oikos 116:1957-1963. doi: 10.1111/j. 2007.0030-1299.16203.x
56. McIntyre PJ, Strauss SY (2014) Phenotypic and transgenerational plasticity promote local adaptation to sun and shade environments. Evol Ecol 28:229-246. doi: 10.1007/s10682-013-9670-y
57. Curley JP, Mashoodh R, Champagne FA (2010) Epigenetics and the origins of paternal effects. Horm Behav 59:306-314. doi: 10.1016/j.yhbeh.2010.06.018 PMID: 20620140
58. Stein LR, Bell AM (2014) Paternal programming in sticklebacks. Anim Behav 95:165-171. doi: 10. 1016/j.anbehav. 2014.07.010
59. Pener M, Simpson S (2009) Locust Phase Polyphenism: An Update. Adv In Insect Phys 36. doi:10. 1016/S0065-2806 (08) 36001-9.
60. Simpson S, McCaffery AR, Hagele BF (1999) A behavioural analysis of phase change in the desert locust. Biol Rev 74:461-480. doi: 10.1111/j.1469-185X.1999.tb00038.x
61. Simpson SJ, Miller GA (2007) Maternal effects on phase characteristics in the desert locust, Schistocerca gregaria: a review of current understanding. J Insect Physiol 53:869-876. doi: 10.1016/j. jinsphys.2007.05.011 PMID: 17624367
62. Boerjan B, Sas F, Ernst UR, Tobback J, Lemière F, et al. (2011) Locust phase polyphenism: Doesepigenetic precede endocrine regulation? GenComp Endocrinol 173:120-128. doi: 10.1016/j.ygcen. 2011.05.003 PMID: 21624368
63. Jablonka E (2012) Epigenetic inheritance and plasticity: The responsive germline. Prog Biophys Mol Biol: 1-9. doi: 10.1016/j.pbiomolbio.2012.08.014
64. Jablonka E, Oborny B, Molnár I, Kisdi E, Hofbauer J, et al. (1995) The adaptive advantage of phenotypic memory in changing environments. Philos Trans RSocB 350:133-141. doi: 10.1098/rstb.1995. 0147
65. Simpson SJ, Sword GA (2009) Phase polyphenism in locusts: mechanisms, population consequences, adaptive significance and evolution. In: Whitman DW, Ananthakrishnan TN, editors. Phenotypic plasticity of insects: mechanisms and consequences. Enfield: Science Publishers. pp. 147-189.
66. Topaz CM, D'Orsogna MR, Edelstein-Keshet L, Bernoff AJ (2012) Locust dynamics: behavioral phase change and swarming. PLoSComputBiol 8:e1002642. doi: 10.1371/journal.pcbi.1002642 PMID: 22916003
67. Kimura M (1961) Natural selection as the process of accumulating genetic information in adaptive evolution. Genet Res 2:127-140. doi: 10.1017/S0016672300000616
68. Jablonka E, Lamb MJ (2005) Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral, and Symbolic Variation in the History of Life. Cambridge MA: MIT Press.
69. Bergstrom CT, Rosvall M (2011) The transmission sense of information. Biol Philos 26:159-176. doi: 10.1007/s10539-009-9180-z
70. Danchin E (2013) Avatars of information: towards an inclusive evolutionary synthesis. Trends Ecol Evol 28:351-358. doi: 10.1016/j.tree.2013.02.010 PMID: 23540765
71. Jablonka E (2002) Information: Its Interpretation, Its Inheritance, and Its Sharing. Philos Sci 69:578-605. doi: 10.1086/344621
72. Uller T, Nakagawa S, English S (2013) Weak evidence for anticipatory parental effects in plants and animals. J Evol Biol 26:2161-2170. doi: 10.1111/jeb.12212 PMID: 23937440
73. Burgess SC, Marshall DJ (2014) Adaptive parental effects: the importance of estimating environmental predictability and offspring fitness appropriately. Oikos 123:769-776. doi: 10.1111/oik.01235
74. Moran NA (1992) The Evolutionary Maintenance of Alternative Phenotypes. Am Nat 139:971-989. doi: 10.1086/285369
75. Crean AJ, Dwyer JM, Marshall DJ (2013) Adaptive paternal effects? Experimental evidence that the paternal environment affects offspring performance. Ecology 94:2575-2582. doi: 10.1890/13-0184.1 PMID: 24400509
76. Zajitschek S, Hotzy C, Zajitschek F, Immler S (2014) Short-term variation in sperm competition causes sperm-mediated epigenetic effects on early offspring performance in the zebrafish. Proc R Soc B 281:20140422. doi: 10.1098/rspb.2014.0422 PMID: 24789902
77. Lind MI, Johansson F (2007) The degree of adaptive phenotypic plasticity is correlated with the spatial environmental heterogeneity experienced by island populations of Ranatemporaria. J Evol Biol 20:1288-1297. doi: 10.1111/j.1420-9101.2007.01353.x PMID: 17584224
78. Morgan HD, Sutherland HG, Martin DI, Whitelaw E (1999) Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 23:314-318. doi: 10.1038/15490 PMID: 10545949
79. Huestis DL, Marshall JL (2006) Interaction between maternal effects and temperature affects diapause occurrence in the cricket Allonemobius socius. Oecologia 146:513-520. doi: 10.1007/s00442-005-0232-z PMID: 16133190
80. Scharf I, Bauerfeind S, Blanckenhorn W, Schäfer M (2010) Effects of maternal and offspring environmental conditions on growth, development and diapause in latitudinal yellow dung fly populations. Clim Res 43:115-125. doi: 10.3354/cr00907
81. Parker GA, Royle NJ, Hartley IR (2002) Intrafamilial conflict and parental investment: a synthesis. Philos Trans R Soc Lond B Biol Sci 357:295-307. doi: 10.1098/rstb.2001.0950 PMID: 11958698
82. Müller W, Lessells CKM, Korsten P, Von Engelhardt N (2007) Manipulative signals in family conflict? On the function of maternal yolk hormones in birds. Am Nat 169:E84-96. doi: 10.1086/511962 PMID: 17253431
83. Platenkamp GA, Shaw RG (1993) Environmental and Genetic Maternal Effects on Seed Characters in Nemophila menziesii. Evolution (N Y) 47:540-555.