1932

Abstract

Myriad mechanisms have evolved to adapt to changing environments. Environmental stimuli alter organisms’ physiology to create memories of previous environments. Whether these environmental memories can cross the generational barrier has interested scientists for centuries. The logic of passing on information from generation to generation is not well understood. When is it useful to remember ancestral conditions, and when might it be deleterious to continue to respond to a context that may no longer exist? The key might be found in understanding the environmental conditions that trigger long-lasting adaptive responses. We discuss the logic that biological systems may use to remember environmental conditions. Responses spanning different generational timescales employ different molecular machineries and may result from differences in the duration or intensity of the exposure. Understanding the molecular components of multigenerational inheritance and the logic underlying beneficial and maladaptive adaptations is fundamental to understanding how organisms acquire and transmit environmental memories across generations.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-020923-114620
2023-10-16
2024-06-15
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/39/1/annurev-cellbio-020923-114620.html?itemId=/content/journals/10.1146/annurev-cellbio-020923-114620&mimeType=html&fmt=ahah

Literature Cited

  1. Allshire RC, Madhani HD. 2018. Ten principles of heterochromatin formation and function. Nat. Rev. Mol. Cell Biol. 19:229–44. https://doi.org/10.1038/nrm.2017.119
    [Crossref] [Google Scholar]
  2. Alvarado S, Mak T, Liu S, Storey KB, Szyf M. 2015. Dynamic changes in global and gene-specific DNA methylation during hibernation in adult thirteen-lined ground squirrels, Ictidomys tridecemlineatus. J. Exp. Biol. 218:1787–95. https://doi.org/10.1242/jeb.116046
    [Crossref] [Google Scholar]
  3. Anway MD, Leathers C, Skinner MK. 2006. Endocrine disruptor vinclozolin induced epigenetic transgenerational adult-onset disease. Endocrinology 147:5515–23. https://doi.org/10.1210/en.2006-0640
    [Crossref] [Google Scholar]
  4. Arey RN, Murphy CT. 2017. Conserved regulators of cognitive aging: from worms to humans. Behav. Brain Res. 322:299–310. https://doi.org/10.1016/j.bbr.2016.06.035
    [Crossref] [Google Scholar]
  5. Arey RN, Stein GM, Kaletsky R, Kauffman A, Murphy CT. 2018. Activation of Gαq signaling enhances memory consolidation and slows cognitive decline. Neuron 98:562–574.e5. https://doi.org/10.1016/j.neuron.2018.03.039
    [Crossref] [Google Scholar]
  6. Baduel P, Colot V. 2021. The epiallelic potential of transposable elements and its evolutionary significance in plants. Philos. Trans. R. Soc. B 376:20200123 https://doi.org/10.1098/rstb.2020.0123
    [Crossref] [Google Scholar]
  7. Balla KM, Troemel ER. 2013. Caenorhabditis elegans as a model for intracellular pathogen infection. Cell. Microbiol. 15:1313–22. https://doi.org/10.1111/cmi.12152
    [Crossref] [Google Scholar]
  8. Baugh LR, Day T. 2020. Nongenetic inheritance and multigenerational plasticity in the nematode C. elegans. eLife 9:e58498 https://doi.org/10.7554/eLife.58498
    [Crossref] [Google Scholar]
  9. Beets I, Zels S, Vandewyer E, Demeulemeester J, Caers J et al. 2022. System-wide mapping of neuropeptide-GPCR interactions in C. elegans. bioRxiv 2022.10.30.514428. https://doi.org/10.1101/2022.10.30.514428
    [Crossref]
  10. Berry S, Hartley M, Olsson TSG, Dean C, Howard M. 2015. Local chromatin environment of a Polycomb target gene instructs its own epigenetic inheritance. eLife 4:e07205 https://doi.org/10.7554/eLife.07205
    [Crossref] [Google Scholar]
  11. Bleker LS, de Rooij SR, Painter RC, Ravelli AC, Roseboom TJ. 2021. Cohort profile: the Dutch famine birth cohort (DFBC)—a prospective birth cohort study in the Netherlands. BMJ Open 11:e042078 https://doi.org/10.1136/bmjopen-2020-042078
    [Crossref] [Google Scholar]
  12. Boscardin C, Manuella F, Mansuy IM. 2022. Paternal transmission of behavioural and metabolic traits induced by postnatal stress to the 5th generation in mice. Environ. Epigenet. 8:dvac024 https://doi.org/10.1093/eep/dvac024
    [Crossref] [Google Scholar]
  13. Boulinier T, Staszewski V. 2008. Maternal transfer of antibodies: raising immuno-ecology issues. Trends Ecol. Evol. 23:282–88. https://doi.org/10.1016/j.tree.2007.12.006
    [Crossref] [Google Scholar]
  14. Bouyer D, Kramdi A, Kassam M, Heese M, Schnittger A et al. 2017. DNA methylation dynamics during early plant life. Genome Biol. 18:179 https://doi.org/10.1186/s13059-017-1313-0
    [Crossref] [Google Scholar]
  15. Bozler J, Kacsoh BZ, Bosco G. 2019. Transgenerational inheritance of ethanol preference is caused by maternal NPF repression. eLife 8:e45391 https://doi.org/10.7554/eLife.45391
    [Crossref] [Google Scholar]
  16. Brennecke J, Malone CD, Aravin AA, Sachidanandam R, Stark A, Hannon GJ. 2008. An epigenetic role for maternally inherited piRNAs in transposon silencing. Science 322:1387–92. https://doi.org/10.1126/science.1165171
    [Crossref] [Google Scholar]
  17. Burkhardt RW. 2013. Lamarck, evolution, and the inheritance of acquired characters. Genetics 194:793–805. https://doi.org/10.1534/genetics.113.151852
    [Crossref] [Google Scholar]
  18. Burton NO, Burkhart KB, Kennedy S. 2011. Nuclear RNAi maintains heritable gene silencing in Caenorhabditis elegans. PNAS 108:19683–88. https://doi.org/10.1073/pnas.1113310108
    [Crossref] [Google Scholar]
  19. Burton NO, Furuta T, Webster AK, Kaplan REW, Baugh LR et al. 2017. Insulin-like signalling to the maternal germline controls progeny response to osmotic stress. Nat. Cell Biol. 19:252–57. https://doi.org/10.1038/ncb3470
    [Crossref] [Google Scholar]
  20. Burton NO, Greer EL. 2022. Multigenerational epigenetic inheritance: transmitting information across generations. Semin. Cell Dev. Biol. 127:121–32. https://doi.org/10.1016/j.semcdb.2021.08.006
    [Crossref] [Google Scholar]
  21. Burton NO, Riccio C, Dallaire A, Price J, Jenkins B et al. 2020. Cysteine synthases CYSL-1 and CYSL-2 mediate C. elegans heritable adaptation to P. vranovensis infection. Nat. Commun. 11:1741 https://doi.org/10.1038/s41467-020-15555-8
    [Crossref] [Google Scholar]
  22. Burton NO, Willis A, Fisher K, Braukmann F, Price J et al. 2021. Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs. eLife 10:e73425 https://doi.org/10.7554/eLife.73425
    [Crossref] [Google Scholar]
  23. Busto GU, Cervantes-Sandoval I, Davis RL. 2010. Olfactory learning in Drosophila. Physiology 25:338–46. https://doi.org/10.1152/physiol.00026.2010
    [Crossref] [Google Scholar]
  24. Carcea I, Caraballo NL, Marlin BJ, Ooyama R, Riceberg JS et al. 2021. Oxytocin neurons enable social transmission of maternal behaviour. Nature 596:553–57. https://doi.org/10.1038/s41586-021-03814-7
    [Crossref] [Google Scholar]
  25. Carone BR, Fauquier L, Habib N, Shea JM, Hart CE et al. 2010. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143:1084–96. https://doi.org/10.1016/j.cell.2010.12.008
    [Crossref] [Google Scholar]
  26. Ciabrelli F, Comoglio F, Fellous S, Bonev B, Ninova M et al. 2017. Stable Polycomb-dependent transgenerational inheritance of chromatin states in Drosophila. Nat. Genet. 49:876–86. https://doi.org/10.1038/ng.3848
    [Crossref] [Google Scholar]
  27. Colbert HA, Bargmann CI. 1995. Odorant-specific adaptation pathways generate olfactory plasticity in C. elegans. Neuron 14:803–12. https://doi.org/10.1016/0896-6273(95)90224-4
    [Crossref] [Google Scholar]
  28. Conine CC, Moresco JJ, Gu W, Shirayama M, Conte D et al. 2013. Argonautes promote male fertility and provide a paternal memory of germline gene expression in C. elegans. Cell 155:1532–44. https://doi.org/10.1016/j.cell.2013.11.032
    [Crossref] [Google Scholar]
  29. Conine CC, Sun F, Song L, Rivera-Pérez JA, Rando OJ. 2018. Small RNAs gained during epididymal transit of sperm are essential for embryonic development in mice. Dev. Cell 46:470–80.e3. https://doi.org/10.1016/j.devcel.2018.06.024
    [Crossref] [Google Scholar]
  30. Cubas P, Vincent C, Coen E. 1999. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401:157–61. https://doi.org/10.1038/43657
    [Crossref] [Google Scholar]
  31. Curzon P, Rustay NR, Browman KE. 2009. Cued and contextual fear conditioning for rodents. Methods of Behavior Analysis in Neuroscience JJ Buccafusco 19–37. Boca Raton, FL: CRC Press/Taylor & Francis
    [Google Scholar]
  32. Dantzer B, Newman AEM, Boonstra R, Palme R, Boutin S et al. 2013. Density triggers maternal hormones that increase adaptive offspring growth in a wild mammal. Science 340:1215–17. https://doi.org/10.1126/science.1235765
    [Crossref] [Google Scholar]
  33. Devanapally S, Ravikumar S, Jose AM. 2015. Double-stranded RNA made in C. elegans neurons can enter the germline and cause transgenerational gene silencing. PNAS 112:2133–38. https://doi.org/10.1073/pnas.1423333112
    [Crossref] [Google Scholar]
  34. Dias BG, Ressler KJ. 2014. Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat. Neurosci. 17:89–96. https://doi.org/10.1038/nn.3594
    [Crossref] [Google Scholar]
  35. Dion E, Pui LX, Weber K, Monteiro A. 2020. Early-exposure to new sex pheromone blends alters mate preference in female butterflies and in their offspring. Nat. Commun. 11:53 https://doi.org/10.1038/s41467-019-13801-2
    [Crossref] [Google Scholar]
  36. Dowen RH, Ahmed S. 2019. Maternal inheritance: Longevity programs nourish progeny via yolk. Curr. Biol. 29:R748–51. https://doi.org/10.1016/j.cub.2019.06.050
    [Crossref] [Google Scholar]
  37. Ehlers CL, Gizer IR, Gilder DA, Ellingson JM, Yehuda R. 2013. Measuring historical trauma in an American Indian community sample: contributions of substance dependence, affective disorder, conduct disorder and PTSD. Drug Alcohol Depend. 133:180–87. https://doi.org/10.1016/j.drugalcdep.2013.05.011
    [Crossref] [Google Scholar]
  38. Eliezer Y, Deshe N, Hoch L, Iwanir S, Pritz CO, Zaslaver A. 2019. A memory circuit for coping with impending adversity. Curr. Biol. 29:1573–83.e4. https://doi.org/10.1016/j.cub.2019.03.059
    [Crossref] [Google Scholar]
  39. Fields BD, Kennedy S. 2019. Chromatin compaction by small RNAs and the nuclear RNAi machinery in C. elegans. Sci. Rep. 9:9030 https://doi.org/10.1038/s41598-019-45052-y
    [Crossref] [Google Scholar]
  40. Fitz-James MH, Cavalli G. 2022. Molecular mechanisms of transgenerational epigenetic inheritance. Nat. Rev. Genet. 23:325–41. https://doi.org/10.1038/s41576-021-00438-5
    [Crossref] [Google Scholar]
  41. Frakes AE, Metcalf MG, Tronnes SU, Bar-Ziv R, Durieux J et al. 2020. Four glial cells regulate ER stress resistance and longevity via neuropeptide signaling in C. elegans. Science 367:436–40. https://doi.org/10.1126/science.aaz6896
    [Crossref] [Google Scholar]
  42. Franklin TB, Russig H, Weiss IC, Gräff J, Linder N et al. 2010. Epigenetic transmission of the impact of early stress across generations. Biol. Psychiatry 68:408–15. https://doi.org/10.1016/j.biopsych.2010.05.036
    [Crossref] [Google Scholar]
  43. Frézal L, Félix M-A. 2015. C. elegans outside the Petri dish. eLife 4:e05849 https://doi.org/10.7554/eLife.05849
    [Crossref] [Google Scholar]
  44. Gammon DB, Ishidate T, Li L, Gu W, Silverman N, Mello CC. 2017. The antiviral RNA interference response provides resistance to lethal arbovirus infection and vertical transmission in Caenorhabditis elegans. Curr. Biol. 27:795–806. https://doi.org/10.1016/j.cub.2017.02.004
    [Crossref] [Google Scholar]
  45. Garrity PA, Goodman MB, Samuel AD, Sengupta P. 2010. Running hot and cold: behavioral strategies, neural circuits, and the molecular machinery for thermotaxis in C. elegans and Drosophila. Genes Dev. 24:2365–82. https://doi.org/10.1101/gad.1953710
    [Crossref] [Google Scholar]
  46. Gluckman PD, Hanson MA, Cooper C, Thornburg KL. 2008. Effect of in utero and early-life conditions on adult health and disease. N. Engl. J. Med. 359:61–73. https://doi.org/10.1056/NEJMra0708473
    [Crossref] [Google Scholar]
  47. Gowri V, Dion E, Viswanath A, Piel FM, Monteiro A. 2019. Transgenerational inheritance of learned preferences for novel host plant odors in Bicyclus anynana butterflies. Evolution 73:2401–14. https://doi.org/10.1111/evo.13861
    [Crossref] [Google Scholar]
  48. Greer EL, Maures TJ, Hauswirth AG, Green EM, Leeman DS et al. 2010. Members of the H3K4 trimethylation complex regulate lifespan in a germline-dependent manner in C. elegans. Nature 466:383–87. https://doi.org/10.1038/nature09195
    [Crossref] [Google Scholar]
  49. Guzman DM, Chakka K, Shi T, Marron A, Fiorito AE et al. 2022. Transgenerational effects of alcohol on behavioral sensitivity to alcohol in Caenorhabditis elegans. PLOS ONE 17:e0271849 https://doi.org/10.1371/journal.pone.0271849
    [Crossref] [Google Scholar]
  50. Hasegawa K. 1957. The diapause hormone of the silkworm, Bombyx mori. Nature 179:1300–1. https://doi.org/10.1038/1791300b0
    [Crossref] [Google Scholar]
  51. Heestand B, Simon M, Frenk S, Titov D, Ahmed S. 2018. Transgenerational sterility of Piwi mutants represents a dynamic form of adult reproductive diapause. Cell Rep. 23:1156–71. https://doi.org/10.1016/j.celrep.2018.03.015
    [Crossref] [Google Scholar]
  52. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ et al. 2008. Persistent epigenetic differences associated with prenatal exposure to famine in humans. PNAS 105:17046–49. https://doi.org/10.1073/pnas.0806560105
    [Crossref] [Google Scholar]
  53. 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 https://doi.org/10.1371/journal.pgen.1006396
    [Crossref] [Google Scholar]
  54. Hiyoshi A, Berg L, Grotta A, Almquist Y, Rostila M. 2021. Parental death in childhood and pathways to increased mortality across the life course in Stockholm, Sweden: a cohort study. PLOS Med. 18:e1003549 https://doi.org/10.1371/journal.pmed.1003549
    [Crossref] [Google Scholar]
  55. Hong C, Lalsiamthara J, Ren J, Sang Y, Aballay A. 2021. Microbial colonization induces histone acetylation critical for inherited gut-germline-neural signaling. PLOS Biol. 19:e3001169 https://doi.org/10.1371/journal.pbio.3001169
    [Crossref] [Google Scholar]
  56. Jobson MA, Jordan JM, Sandrof MA, Hibshman JD, Lennox AL, Baugh LR. 2015. Transgenerational effects of early life starvation on growth, reproduction, and stress resistance in Caenorhabditis elegans. Genetics 201:201–12. https://doi.org/10.1534/genetics.115.178699
    [Crossref] [Google Scholar]
  57. Juang B-T, Gu C, Starnes L, Palladino F, Goga A et al. 2013. Endogenous nuclear RNAi mediates behavioral adaptation to odor. Cell 154:1010–22. https://doi.org/10.1016/j.cell.2013.08.006
    [Crossref] [Google Scholar]
  58. Kaletsky R, Moore RS, Vrla GD, Parsons LR, Gitai Z, Murphy CT. 2020. C. elegans interprets bacterial non-coding RNAs to learn pathogenic avoidance. Nature 586:445–51. https://doi.org/10.1038/s41586-020-2699-5
    [Crossref] [Google Scholar]
  59. Kauffman AL, Ashraf JM, Corces-Zimmerman MR, Landis JN, Murphy CT. 2010. Insulin signaling and dietary restriction differentially influence the decline of learning and memory with age. PLOS Biol. 8:e1000372 https://doi.org/10.1371/journal.pbio.1000372
    [Crossref] [Google Scholar]
  60. Kelley JL, Tobler M, Beck D, Sadler-Riggleman I, Quackenbush CR et al. 2021. Epigenetic inheritance of DNA methylation changes in fish living in hydrogen sulfide–rich springs. PNAS 118:e2014929118 https://doi.org/10.1073/pnas.2014929118
    [Crossref] [Google Scholar]
  61. Klosin A, Casas E, Hidalgo-Carcedo C, Vavouri T, Lehner B. 2017. Transgenerational transmission of environmental information in C. elegans. Science 356:320–23. https://doi.org/10.1126/science.aah6412
    [Crossref] [Google Scholar]
  62. Laforsch C, Tollrian R. 2004. Extreme helmet formation in Daphnia cucullata induced by small-scale turbulence. J. Plankton Res. 26:81–87. https://doi.org/10.1093/plankt/fbg114
    [Crossref] [Google Scholar]
  63. Lakhina V, Arey RN, Kaletsky R, Kauffman A, Stein G et al. 2015. Genome-wide functional analysis of CREB/long-term memory-dependent transcription reveals distinct basal and memory gene expression programs. Neuron 85:330–45. https://doi.org/10.1016/j.neuron.2014.12.029
    [Crossref] [Google Scholar]
  64. Lang-Mladek C, Popova O, Kiok K, Berlinger M, Rakic B et al. 2010. Transgenerational inheritance and resetting of stress-induced loss of epigenetic gene silencing in Arabidopsis. Mol. Plant 3:594–602. https://doi.org/10.1093/mp/ssq014
    [Crossref] [Google Scholar]
  65. Lee TW, David HS, Engstrom AK, Carpenter BS, Katz DJ. 2019. Repressive H3K9me2 protects lifespan against the transgenerational burden of COMPASS activity in C. elegans. eLife 8:e48498 https://doi.org/10.7554/eLife.48498
    [Crossref] [Google Scholar]
  66. Legüe M, Caneo M, Aguila B, Pollak B, Calixto A. 2022. Interspecies effectors of a transgenerational memory of bacterial infection in Caenorhabditis elegans. iScience 25:104627 https://doi.org/10.1016/j.isci.2022.104627
    [Crossref] [Google Scholar]
  67. Liberman N, Wang SY, Greer EL. 2019. Transgenerational epigenetic inheritance: from phenomena to molecular mechanisms. Curr. Opin. Neurobiol. 59:189–206. https://doi.org/10.1016/j.conb.2019.09.012
    [Crossref] [Google Scholar]
  68. Lim AI, McFadden T, Link VM, Han S-J, Karlsson R-M et al. 2021. Prenatal maternal infection promotes tissue-specific immunity and inflammation in offspring. Science 373:eabf3002 https://doi.org/10.1126/science.abf3002
    [Crossref] [Google Scholar]
  69. Lockwood BL, Julick CR, Montooth KL. 2017. Maternal loading of a small heat shock protein increases embryo thermal tolerance in Drosophila melanogaster. J. Exp. Biol. 220:4492–501. https://doi.org/10.1242/jeb.164848
    [Crossref] [Google Scholar]
  70. Ma C, Niu R, Huang T, Shao L-W, Peng Y et al. 2019. N6-methyldeoxyadenine is a transgenerational epigenetic signal for mitochondrial stress adaptation. Nat. Cell Biol. 21:319–27. https://doi.org/10.1038/s41556-018-0238-5
    [Crossref] [Google Scholar]
  71. Manikkam M, Tracey R, Guerrero-Bosagna C, Skinner MK. 2012. Pesticide and insect repellent mixture (permethrin and DEET) induces epigenetic transgenerational inheritance of disease and sperm epimutations. Reprod. Toxicol. 34:708–19. https://doi.org/10.1016/j.reprotox.2012.08.010
    [Crossref] [Google Scholar]
  72. Manikkam M, Tracey R, Guerrero-Bosagna C, Skinner MK. 2013. Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. PLOS ONE 8:e55387 https://doi.org/10.1371/journal.pone.0055387
    [Crossref] [Google Scholar]
  73. Miryeganeh M, Saze H. 2020. Epigenetic inheritance and plant evolution. Popul. Ecol. 62:17–27. https://doi.org/10.1002/1438-390X.12018
    [Crossref] [Google Scholar]
  74. Mitchell K. 2013. The trouble with epigenetics (part 2). Wiring the Brain Blog Jan. 14. http://www.wiringthebrain.com/2013/01/the-trouble-with-epigenetics-part-2.html
    [Google Scholar]
  75. Mondotte JA, Gausson V, Frangeul L, Suzuki Y, Vazeille M et al. 2020. Evidence for long-lasting transgenerational antiviral immunity in insects. Cell Rep. 33:108506 https://doi.org/10.1016/j.celrep.2020.108506
    [Crossref] [Google Scholar]
  76. Moore RS, Kaletsky R, Lesnik C, Cota V, Blackman E et al. 2021a. The role of the Cer1 transposon in horizontal transfer of transgenerational memory. Cell 184:4697–712.e18. https://doi.org/10.1016/j.cell.2021.07.022
    [Crossref] [Google Scholar]
  77. Moore RS, Kaletsky R, Murphy CT. 2019. Piwi/PRG-1 argonaute and TGF-β mediate transgenerational learned pathogenic avoidance. Cell 177:1827–41.e12. https://doi.org/10.1016/j.cell.2019.05.024
    [Crossref] [Google Scholar]
  78. Moore RS, Kaletsky R, Murphy CT. 2021b. Protocol for transgenerational learned pathogen avoidance behavior assays in Caenorhabditis elegans. STAR Protoc. 2:100384 https://doi.org/10.1016/j.xpro.2021.100384
    [Crossref] [Google Scholar]
  79. Ouyang JPT, Seydoux G. 2022. Nuage condensates: accelerators or circuit breakers for sRNA silencing pathways?. RNA 28:58–66. https://doi.org/10.1261/rna.079003.121
    [Crossref] [Google Scholar]
  80. Ouyang JPT, Zhang WL, Seydoux G. 2022. The conserved helicase ZNFX-1 memorializes silenced RNAs in perinuclear condensates. Nat. Cell Biol. 24:1129–40. https://doi.org/10.1038/s41556-022-00940-w
    [Crossref] [Google Scholar]
  81. Ow MC, Nichitean AM, Hall SE. 2021. Somatic aging pathways regulate reproductive plasticity in Caenorhabditis elegans. eLife 10:e61459 https://doi.org/10.7554/eLife.61459
    [Crossref] [Google Scholar]
  82. Palominos MF, Verdugo L, Gabaldon C, Pollak B, Ortíz-Severín J et al. 2017. Transgenerational diapause as an avoidance strategy against bacterial pathogens in Caenorhabditis elegans. mBio 8:e01234-17. https://doi.org/10.1128/mBio.01234-17
    [Crossref] [Google Scholar]
  83. Pereira AG, Gracida X, Kagias K, Zhang Y. 2020. C. elegans aversive olfactory learning generates diverse intergenerational effects. J. Neurogenet. 34:378–88. https://doi.org/10.1080/01677063.2020.1819265
    [Crossref] [Google Scholar]
  84. Perez MF, Francesconi M, Hidalgo-Carcedo C, Lehner B. 2017. Maternal age generates phenotypic variation in Caenorhabditis elegans. Nature 552:106–9. https://doi.org/10.1038/nature25012
    [Crossref] [Google Scholar]
  85. Perez MF, Lehner B. 2019. Intergenerational and transgenerational epigenetic inheritance in animals. Nat. Cell Biol. 21:143–51. https://doi.org/10.1038/s41556-018-0242-9
    [Crossref] [Google Scholar]
  86. Perez MF, Shamalnasab M, Mata-Cabana A, Valle SD, Olmedo M et al. 2021. Neuronal perception of the social environment generates an inherited memory that controls the development and generation time of C. elegans. Curr. Biol. 31:4256–68.e7. https://doi.org/10.1016/j.cub.2021.07.031
    [Crossref] [Google Scholar]
  87. Phillips CM, Updike DL. 2022. Germ granules and gene regulation in the Caenorhabditis elegans germline. Genetics 220:iyab195 https://doi.org/10.1093/genetics/iyab195
    [Crossref] [Google Scholar]
  88. Plesnar-Bielak A, Labocha MK, Kosztyła P, Woch KR, Banot WM et al. 2017. Fitness effects of thermal stress differ between outcrossing and selfing populations in Caenorhabditis elegans. Evol. Biol. 44:356–64. https://doi.org/10.1007/s11692-017-9413-z
    [Crossref] [Google Scholar]
  89. Posner R, Toker IA, Antonova O, Star E, Anava S et al. 2019. Neuronal small RNAs control behavior transgenerationally. Cell 177:1814–26.e15. https://doi.org/10.1016/j.cell.2019.04.029
    [Crossref] [Google Scholar]
  90. Qi B, Kniazeva M, Han M. 2017. A vitamin-B2-sensing mechanism that regulates gut protease activity to impact animal's food behavior and growth. eLife 6e26243 https://doi.org/10.7554/eLife.26243
    [Crossref] [Google Scholar]
  91. Quarato P, Singh M, Bourdon L, Cecere G. 2022. Inheritance and maintenance of small RNA-mediated epigenetic effects. BioEssays 44:2100284 https://doi.org/10.1002/bies.202100284
    [Crossref] [Google Scholar]
  92. Ramachandran S, Banerjee N, Bhattacharya R, Lemons ML, Florman J et al. 2021. A conserved neuropeptide system links head and body motor circuits to enable adaptive behavior. eLife 10:e71747 https://doi.org/10.7554/eLife.71747
    [Crossref] [Google Scholar]
  93. Rasmann S, De Vos M, Casteel CL, Tian D, Halitschke R et al. 2012. Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol. 158:854–63. https://doi.org/10.1104/pp.111.187831
    [Crossref] [Google Scholar]
  94. Rechavi O, Houri-Ze'evi L, Anava S, Goh WSS, Kerk SY et al. 2014. Starvation-induced transgenerational inheritance of small RNAs in C. elegans. Cell 158:277–87. https://doi.org/10.1016/j.cell.2014.06.020
    [Crossref] [Google Scholar]
  95. Remy J-J. 2010. Stable inheritance of an acquired behavior in Caenorhabditis elegans. Curr. Biol. 20:R877–78. https://doi.org/10.1016/j.cub.2010.08.013
    [Crossref] [Google Scholar]
  96. Rendina González AP, Preite V, Verhoeven KJF, Latzel V 2018. Transgenerational effects and epigenetic memory in the clonal plant Trifolium repens. Front. Plant Sci. 9:1677 https://doi.org/10.3389/fpls.2018.01677
    [Crossref] [Google Scholar]
  97. Ripoll-Sánchez L, Watteyne J, Sun H, Fernandez R, Taylor S et al. 2022. The neuropeptidergic connectome of C. elegans. bioRxiv 514396. https://doi.org/10.1101/2022.10.30.514396
    [Crossref]
  98. S. AE 1893. Das Keimplasma Eine Theorie der Vererbung. Nature 47:265–66. https://doi.org/10.1038/047265a0
    [Crossref] [Google Scholar]
  99. Saavedra-Rodríguez L, Feig LA 2013. Chronic social instability induces anxiety and defective social interactions across generations. Biol. Psychiatry 73:44–53 https://doi.org/10.1016/j.biopsych.2012.06.035
    [Crossref] [Google Scholar]
  100. Samuel BS, Rowedder H, Braendle C, Félix M-A, Ruvkun G. 2016. Caenorhabditis elegans responses to bacteria from its natural habitats. PNAS 113:E3941–49. https://doi.org/10.1073/pnas.1607183113
    [Crossref] [Google Scholar]
  101. Sanes JR, Zipursky SL. 2010. Design principles of insect and vertebrate visual systems. Neuron 66:15–36. https://doi.org/10.1016/j.neuron.2010.01.018
    [Crossref] [Google Scholar]
  102. Sarkies P. 2020. Molecular mechanisms of epigenetic inheritance: possible evolutionary implications. Semin. Cell Dev. Biol. 97:106–15. https://doi.org/10.1016/j.semcdb.2019.06.005
    [Crossref] [Google Scholar]
  103. Sato M, Sato K. 2012. Maternal inheritance of mitochondrial DNA: degradation of paternal mitochondria by allogeneic organelle autophagy, allophagy. Autophagy 8:424–25. https://doi.org/10.4161/auto.19243
    [Crossref] [Google Scholar]
  104. Schulenburg H, Félix M-A. 2017. The natural biotic environment of Caenorhabditis elegans. Genetics 206:55–86. https://doi.org/10.1534/genetics.116.195511
    [Crossref] [Google Scholar]
  105. Schwartz-Orbach L, Zhang C, Sidoli S, Amin R, Kaur D et al. 2020. Caenorhabditis elegans nuclear RNAi factor SET-32 deposits the transgenerational histone modification, H3K23me3. eLife 9:e54309 https://doi.org/10.7554/eLife.54309
    [Crossref] [Google Scholar]
  106. Seong K-H, Li D, Shimizu H, Nakamura R, Ishii S. 2011. Inheritance of stress-induced, ATF-2-dependent epigenetic change. Cell 145:1049–61. https://doi.org/10.1016/j.cell.2011.05.029
    [Crossref] [Google Scholar]
  107. Seroussi U, Li C, Sundby AE, Lee TL, Claycomb JM, Saltzman AL. 2022. Mechanisms of epigenetic regulation by C. elegans nuclear RNA interference pathways. Semin. Cell Dev. Biol. 127:142–54. https://doi.org/10.1016/j.semcdb.2021.11.018
    [Crossref] [Google Scholar]
  108. Stassen JHM, López A, Jain R, Pascual-Pardo D, Luna E et al. 2018. The relationship between transgenerational acquired resistance and global DNA methylation in Arabidopsis. Sci. Rep. 8:14761 https://doi.org/10.1038/s41598-018-32448-5
    [Crossref] [Google Scholar]
  109. Stern S, Fridmann-Sirkis Y, Braun E, Soen Y. 2012. Epigenetically heritable alteration of fly development in response to toxic challenge. Cell Rep. 1:528–42. https://doi.org/10.1016/j.celrep.2012.03.012
    [Crossref] [Google Scholar]
  110. Tan M-W, Mahajan-Miklos S, Ausubel FM. 1999. Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. PNAS 96:715–20. https://doi.org/10.1073/pnas.96.2.715
    [Crossref] [Google Scholar]
  111. Toker IA, Lev I, Mor Y, Gurevich Y, Fisher D et al. 2022. Transgenerational inheritance of sexual attractiveness via small RNAs enhances evolvability in C. elegans. Dev. Cell 57:298–309.e9. https://doi.org/10.1016/j.devcel.2022.01.005
    [Crossref] [Google Scholar]
  112. Trerotola M, Relli V, Simeone P, Alberti S. 2015. Epigenetic inheritance and the missing heritability. Hum. Genom. 9:17 https://doi.org/10.1186/s40246-015-0041-3
    [Crossref] [Google Scholar]
  113. Vågerö D, Pinger PR, Aronsson V, van den Berg GJ. 2018. Paternal grandfather's access to food predicts all-cause and cancer mortality in grandsons. Nat. Commun. 9:5124 https://doi.org/10.1038/s41467-018-07617-9
    [Crossref] [Google Scholar]
  114. van den Pol AN 2012. Neuropeptide transmission in brain circuits. Neuron 76:98–115. https://doi.org/10.1016/j.neuron.2012.09.014
    [Crossref] [Google Scholar]
  115. Vogt MC, Hobert O. 2023. Starvation-induced changes in somatic insulin/IGF-1R signaling drive metabolic programming across generations. Sci. Adv. 9:eade1817 https://doi.org/10.1126/sciadv.ade1817
    [Crossref] [Google Scholar]
  116. Wan Q-L, Meng X, Wang C, Dai W, Luo Z et al. 2022. Histone H3K4me3 modification is a transgenerational epigenetic signal for lipid metabolism in Caenorhabditis elegans. Nat. Commun. 13:768 https://doi.org/10.1038/s41467-022-28469-4
    [Crossref] [Google Scholar]
  117. Wang SY, Kim K, O'Brown ZK, Levan A, Dodson AE et al. 2022. Hypoxia induces transgenerational epigenetic inheritance of small RNAs. Cell Rep. 41:111800 https://doi.org/10.1016/j.celrep.2022.111800
    [Crossref] [Google Scholar]
  118. Webster AK, Jordan JM, Hibshman JD, Chitrakar R, Baugh LR. 2018. Transgenerational effects of extended dauer diapause on starvation survival and gene expression plasticity in Caenorhabditis elegans. Genetics 210:263–74. https://doi.org/10.1534/genetics.118.301250
    [Crossref] [Google Scholar]
  119. Weigel D, Colot V. 2012. Epialleles in plant evolution. Genome Biol. 13:249 https://doi.org/10.1186/gb-2012-13-10-249
    [Crossref] [Google Scholar]
  120. Willis AR, Zhao W, Sukhdeo R, Wadi L, El Jarkass HT et al. 2021. A parental transcriptional response to microsporidia infection induces inherited immunity in offspring. Sci. Adv. 7:eabf3114 https://doi.org/10.1126/sciadv.abf3114
    [Crossref] [Google Scholar]
  121. Wilson RI. 2013. Early olfactory processing in Drosophila: mechanisms and principles. Annu. Rev. Neurosci. 36:217–41. https://doi.org/10.1146/annurev-neuro-062111-150533
    [Crossref] [Google Scholar]
  122. Wu T, Ge M, Wu M, Duan F, Liang J et al. 2023. Pathogenic bacteria modulate pheromone response to promote mating. Nature 613:324–31. https://doi.org/10.1038/s41586-022-05561-9
    [Crossref] [Google Scholar]
  123. Xue B, Leibler S. 2018. Benefits of phenotypic plasticity for population growth in varying environments. PNAS 115:12745–50. https://doi.org/10.1073/pnas.1813447115
    [Crossref] [Google Scholar]
  124. Yehuda R, Daskalakis NP, Bierer LM, Bader HN, Klengel T et al. 2016. Holocaust exposure induced intergenerational effects on FKBP5 methylation. Biol. Psychiatry 80:372–80. https://doi.org/10.1016/j.biopsych.2015.08.005
    [Crossref] [Google Scholar]
  125. Zhang H, Lang Z, Zhu J-K. 2018. Dynamics and function of DNA methylation in plants. Nat. Rev. Mol. Cell Biol. 19:489–506. https://doi.org/10.1038/s41580-018-0016-z
    [Crossref] [Google Scholar]
  126. Zhang Y, Lu H, Bargmann CI. 2005. Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438:179–84. https://doi.org/10.1038/nature04216
    [Crossref] [Google Scholar]
  127. Zirkle C. 1935. The inheritance of acquired characters and the provisional hypothesis of pangenesis. Am. Nat. 69:417–45. https://doi.org/10.1086/280617
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-cellbio-020923-114620
Loading
/content/journals/10.1146/annurev-cellbio-020923-114620
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