Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Non-Genetic Inheritance

1 Issue per year


Emerging Science

Open Access
Online
ISSN
2084-8846
See all formats and pricing
More options …

Non-genetic inheritance and changing environments

Santiago Salinas / Simon C. Brown
  • Dept. of Ecology and Evolutionary Biology, University of California Santa Cruz, Santa Cruz, CA, 95060, USA
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Marc Mangel
  • Center for Stock Assessment Research, University of California Santa Cruz, Santa Cruz, CA 95060, USA
  • Dept. of Biology, University of Bergen, Bergen, 5020, Norway
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Stephan B. Munch
Published Online: 2013-10-22 | DOI: https://doi.org/10.2478/ngi-2013-0005

Abstract

Climate change continues to impact species worldwide. Understanding and predicting how populations will respond is of clear importance. Here, we review a mechanism by which populations may respond rapidly to these changes: Trans-Generational Plasticity (TGP). TGP exists when the environment experienced by the parents affects the shape of the reaction norm in their offspring; that is, the parental and offspring environments interact to determine the offspring phenotype. We survey 80 empirical studies from 63 species (32 orders, 9 phyla) that demonstrate TGP. Overall, TGP is taxonomically widespread and present in response to environmental drivers likely to be impacted by climate change. Although many examples now exist, we also identify areas of research that could greatly improve our understanding of TGP. We conclude that TGP is sufficiently established both theoretically and empirically to merit study as a potential coping tactic against rapid environmental changes.

Keywords: Transgenerational plasticity; Maternal effect; Inter-generational; Cross-generational; Acclimation

  • [1] Intergovernmental Panel on Climate Change I., Synthesis report. Contribution of working groups I, II and III to the fourth assessment report of the Intergovernmental Panel on Climate Change, IPCC, Geneva, Switzerland, 2007. Available from: http://www.ipcc.ch/pdf/assessment-report/ar4/syr/ar4_syr.pdf Google Scholar

  • [2] Perry A.L., Low P.J., Ellis J.R., Reynolds J.D., Climate change and distribution shifts in marine fishes, Science, 2005, 308, 1912–1915, DOI: 10.1126/science.1111322 CrossrefGoogle Scholar

  • [3] Thompson R.M., Beardall J., Beringer J., Grace M., Sardina P., Means and extremes: building variability into communitylevel climate change experiments, Ecology Letters, 2013, 16, 799–806, DOI: 10.1111/ele.12095 CrossrefGoogle Scholar

  • [4] Raffel T.R., Romansic J.M., Halstead N.T., McMahon T.A., Venesky M.D., Rohr J.R., Disease and thermal acclimation in a more variable and unpredictable climate, Nature Climate Change, 2013, 3, 146–151, DOI: 10.1038/nclimate1659 CrossrefGoogle Scholar

  • [5] Dore M.H.I., Climate change and changes in global precipitation patterns: What do we know? Environment International, 2005, 31, 1167–1181, DOI: 10.1016/j. envint.2005.03.004 CrossrefGoogle Scholar

  • [6] Doney S.C., Fabry V.J., Feely R.A., Kleypas J.A., Ocean acidification: the other CO2 problem, Annual Review of Marine Science, 2009, 1, 169–192, DOI: 10.1146/annurev. marine.010908.163834 CrossrefGoogle Scholar

  • [7] Binzer A., Guill C., Brose U., Rall B.C., The dynamics of food chains under climate change and nutrient enrichment, Philosophical Transactions of the Royal Society B, 2012, 367, 2935–2944, DOI: 10.1890/10-0260.1 CrossrefGoogle Scholar

  • [8] Dukes J.S., Mooney H.A., Does global change increase the success of biological invaders? Trends in Ecology & Evolution, 1999, 14, 135–139, DOI: 10.1016/S0169-5347(98)01554-7 CrossrefGoogle Scholar

  • [9] Rohr J.R., Dobson A.P., Johnson P.T.J., Kilpatrick A.M., Paull S.H., Raffel T.R., et al., Frontiers in climate change-disease research, Trends in Ecology & Evolution, 2011, 26, 270–277, DOI: 10.1016/j.tree.2011.03.002 CrossrefGoogle Scholar

  • [10] Parmesan C., Ecological and evolutionary responses to recent climate change, Annual Review of Ecology Evolution and Systematics, 2006, 37, 637–669, DOI: 10.1146/annurev. ecolsys.37.091305.110100 CrossrefGoogle Scholar

  • [11] Nicotra A.B., Atkin O.K., Bonser S.P., Davidson A.M., Finnegan E.J., Mathesius U., et al., Plant phenotypic plasticity in a changing climate, Trends in Plant Science, 2010, 15, 684–692, DOI: 10.1016/j.tplants.2010.09.008 CrossrefGoogle Scholar

  • [12] Bradshaw W.E., Evolutionary response to rapid climate change, Science, 2006, 312, 1477–1478, DOI: 10.1126/ science.1127000 CrossrefGoogle Scholar

  • [13] Donohue K., Schmitt J., Maternal environmental effects in plants: adaptive plasticity? In: Mousseau T.A., Fox C.W. (Eds.), Maternal effects as adaptations, Oxford University Press, New York, 1998 Google Scholar

  • [14] Plaistow S.J., Lapsley C.T., Benton T.G., Context-dependent intergenerational effects: the interaction between past and present environments and its effect on population dynamics, The American Naturalist, 2006, 167, 206–215, DOI: 10.1086/499380 CrossrefGoogle Scholar

  • [15] Parker L.M., Ross P.M., O’Connor W.A., Borysko L., Raftos D.A., Pörtner H.-O., Adult exposure influences offspring response to ocean acidification in oysters, Global Change Biology, 2012, 18, 82–92, DOI: 10.1111/j.1365-2486.2011.02520.x CrossrefGoogle Scholar

  • [16] Sultan S.E., Phenotypic plasticity in plants: a case study in ecological development, Evolution & Development, 2003, 5, 25–33, DOI: 10.1046/j.1525-142X.2003.03005.x CrossrefGoogle Scholar

  • [17] Donelson J.M., Munday P.L., McCormick M.I., Pitcher C.R., Rapid transgenerational acclimation of a tropical reef fish to climate change, Nature Climate Change, 2012, 2, 30–32, DOI: 10.1038/nclimate1323 CrossrefGoogle Scholar

  • [18] Salinas S., Munch S.B., Thermal legacies: transgenerational effects of temperature on growth in a vertebrate, Ecology Letters, 2012, 15, 159–163, DOI: 10.1111/j.1461- 0248.2011.01721.x CrossrefGoogle Scholar

  • [19] Finstad A.G., Jonsson B., Effect of incubation temperature on growth performance in Atlantic salmon, Marine Ecology Progress Series, 2012, 454, 75–82, DOI: 10.3354/ meps09643 CrossrefGoogle Scholar

  • [20] Reed T.E., Waples R.S., Schindler D.E., Hard J.J., Kinnison M.T., Phenotypic plasticity and population viability: the importance of environmental predictability, Proceedings of the Royal Society B, 2010, 277, 3391–3400, DOI: 10.1098/ rspb.2010.0771 CrossrefGoogle Scholar

  • [21] Jirtle R.L., Skinner M.K., Environmental epigenomics and disease susceptibility, Nature Reviews Genetics, 2007, 8, 253–262, DOI: 10.1038/nrg2045 CrossrefGoogle Scholar

  • [22] Bonduriansky R., Crean A.J., Day T., The implications of nongenetic inheritance for evolution in changing environments, Evolutionary Applications, 2012, 5, 192–201, DOI: 10.1111/j.1752-4571.2011.00213.x CrossrefGoogle Scholar

  • [23] Hurst T.P., Munch S.B., Lavelle K.A., Thermal reaction norms for growth vary among cohorts of Pacific cod (Gadus macrocephalus), Marine Biology, 2012, 159, 2173–2183, DOI: 10.1007/s00227-012-2003-9 CrossrefGoogle Scholar

  • [24] Donelson J.M., Munday P.L., McCormick M.I., Nilsson G.E., Acclimation to predicted ocean warming through developmental plasticity in a tropical reef fish, Global Change Biology, 2010, 17, 1712–1719, DOI: 10.1111/j.1365- 2486.2010.02339.x CrossrefGoogle Scholar

  • [25] Scott G.R., Johnston I.A., Temperature during embryonic development has persistent effects on thermal acclimation capacity in zebrafish, Proceedings of the National Academy of Sciences USA, 2012, 109, 14247–14252, DOI: 10.1073/ pnas.1205012109/-/DCSupplemental/pnas.201205012SI.pdf CrossrefGoogle Scholar

  • [26] Burton T., McKelvey S., Stewart D.C., Armstrong J.D., Metcalfe N.B., Early maternal experience shapes offspring performance in the wild, Ecology, 2013, 94, 618–626, DOI: 10.1890/12-0462.1 CrossrefGoogle Scholar

  • [27] Grindstaff J.L., Hasselquist D., Nilsson J.A., Sandell M., Smith H.G., Stjernman M., Transgenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity, Proceedings of the Royal Society B, 2006, 273, 2551–2557, DOI: 10.1098/rspb.2006.3608 CrossrefGoogle Scholar

  • [28] Madden R.A., A simple approximation for the variance of meterological time averages, Journal of Applied Meteorology, 1979, 18, 703–705, DOI: 10.1175/1520-0450(1979)018<0703:ASAFTV>2.0.CO;2 CrossrefGoogle Scholar

  • [29] Burgess S.C., Marshall D.J., Temperature-induced maternal effects and environmental predictability, Journal of Experimental Biology, 2011, 214, 2329–2336, DOI: 10.1242/ jeb.054718 CrossrefGoogle Scholar

  • [30] Walther G.-R., Post E., Convey P., Menzel A., Parmesan C., Beebee T.J.C., et al., Ecological responses to recent climate change, Nature, 2002, 416, 389–395, DOI: 10.1038/416389a CrossrefGoogle Scholar

  • [31] Inchausti P., Ginzburg L.R., Maternal effects mechanism of population cycling: a formidable competitor to the traditional predator-prey view, Philosophical Transactions of the Royal Society B, 2009, 364, 1117–1124, DOI: 10.1098/ rstb.2008.0292 CrossrefGoogle Scholar

  • [32] Van Allen B.G., Rudolf V.H.W., Ghosts of habitats past: environmental carry-over effects drive population dynamics in novel habitat, The American Naturalist, 2013, 181, 596– 608, DOI: 10.1086/670127 CrossrefGoogle Scholar

  • [33] Dyer A.R., Brown C.S., Espeland E.K., McKay J.K., Meimberg H., Rice K.J., The role of adaptive trans-generational plasticity in biological invasions of plants, Evolutionary Applications, 2010, 3, 179–192, DOI: 10.1111/j.1752-4571.2010.00118.x CrossrefGoogle Scholar

  • [34] Jacobs B.S., Lesmeister S.A., Maternal environmental effects on fitness, fruit morphology and ballistic seed dispersal distance in an annual forb, Functional Ecology, 2012, 26, 588–597, DOI: 10.1111/j.1365-2435.2012.01964.x CrossrefGoogle Scholar

  • [35] Vergeer P., Wagemaker N., Ouborg N.J., Evidence for an epigenetic role in inbreeding depression, Biology Letters, 2012, 8, 798–801, DOI: 10.1098/rsbl.2012.0494 CrossrefGoogle Scholar

  • [36] Bull C.D., Metcalfe N.B., Mangel M., Seasonal matching of foraging to anticipated energy requirements in anorexic juvenile salmon, Proceedings of the Royal Society B, 1996, 263, 13–18, DOI: 10.1098/rspb.1996.0003 CrossrefGoogle Scholar

  • [37] Tagkopoulos I., Liu Y.-C., Tavazoie S., Predictive behavior within microbial genetic networks, Science, 2008, 320, 1313–1317, DOI: 10.1126/science.1154456 CrossrefGoogle Scholar

  • [38] Mitchell A., Romano G.H., Groisman B., Yona A., Dekel E., Kupiec M., et al., Adaptive prediction of environmental changes by microorganisms, Nature, 2009, 460, 220–224, DOI: 10.1038/nature08112 CrossrefGoogle Scholar

  • [39] Richards E.J., Inherited epigenetic variation-revisiting soft inheritance, Nature Reviews Genetics, 2006, 7, 395–401, DOI: 10.1038/nrg1834 CrossrefGoogle Scholar

  • [40] Rando O.J., Verstrepen K.J., Timescales of genetic and epigenetic inheritance, Cell, 2007, 128, 655–668, DOI: 10.1016/j.cell.2007.01.023 CrossrefGoogle Scholar

  • [41] Jablonka E., Raz G., Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution, Quarterly Review of Biology, 2009, 84, 131–176, DOI: 10.1086/598822 CrossrefGoogle Scholar

  • [42] West-Eberhard M.J., Developmental plasticity and evolution, Oxford University Press, New York, 2003 Google Scholar

  • [43] Schwander T., Leimar O., Genes as leaders and followers in evolution, Trends in Ecology & Evolution, 2011, 26, 143–151, DOI: 10.1016/j.tree.2010.12.010 CrossrefGoogle Scholar

  • [44] Day T., Bonduriansky R., A unified approach to the evolutionary consequences of genetic and nongenetic inheritance, The American Naturalist, 2011, 178, E18–E36, DOI: 10.1086/660911 CrossrefGoogle Scholar

  • [45] Relyea R.A., Costs of phenotypic plasticity, The American Naturalist, 2002, 159, 272–282, DOI: 10.1086/338540 CrossrefGoogle Scholar

  • [46] van Buskirk J., Steiner U.K., The fitness costs of developmental canalization and plasticity, Journal of Evolutionary Biology, 2009, 22, 852–860, DOI: 10.1111/j.1420-9101.2009.01685.x CrossrefGoogle Scholar

  • [47] Uller T., Developmental plasticity and the evolution of parental effects, Trends in Ecology & Evolution, 2008, 23, 432–438, DOI: 10.1016/j.tree.2008.04.005 CrossrefGoogle Scholar

  • [48] Moran D.T., Dias G.M., Marshall D.J., Associated costs and benefits of a defended phenotype across multiple environments, Functional Ecology, 2010, 24, 1299–1305, DOI: 10.1111/j.1365-2435.2010.01741.x CrossrefGoogle Scholar

  • Table references Google Scholar

  • [1] Johnsen O., Daehlen O.G., Ostreng G., Skroppa T., Daylength and temperature during seed production interactively affect adaptive performance of Picea abies progenies, New Phytologist, 2005, 168, 589–596, DOI: 10.1111/j.1469- 8137.2005.01538.x CrossrefGoogle Scholar

  • [2] Blödner C., Goebel C., Feussner I., Gatz C., Polle A., Warm and cold parental reproductive environments affect seed properties, fitness, and cold responsiveness in Arabidopsis thaliana progenies, Plant Cell & Environment, 2007, 30, 165– 175, DOI: 10.1111/j.1365-3040.2006.01615.x CrossrefGoogle Scholar

  • [3] Whittle C.A., Otto S.P., Johnston M.O., Krochko J.E., Adaptive epigenetic memory of ancestral temperature regime in Arabidopsis thaliana, Botany, 2009, 87, 650–657, DOI: 10.1139/B09-030 CrossrefGoogle Scholar

  • [4] Suter L., Widmer A., Environmental heat and salt stress induce transgenerational phenotypic changes in Arabidopsis thaliana, PLoS ONE, 2013, 8, e60364, DOI: 10.1371/journal. pone.0060364.s006 CrossrefGoogle Scholar

  • [5] Went F.W., Effects of environment of parent and grandparent generations on tuber production by potatoes, American Journal of Botany, 1959, 277–282, CrossrefGoogle Scholar

  • [6] Lacey E.P., Parental effects in Plantago lanceolata L. I. A growth chamber experiment to examine pre- and postzygotic temperature effects, Evolution, 1996, 865–878, DOI: 10.2307/2410858 CrossrefGoogle Scholar

  • [7] Alexander H.M., Wulff R.D., Experimental ecological genetics in Plantago: X. The effects of maternal temperature on seed and seedling characters in P. lanceolata, Journal of Ecology, 1985, 73, 271–282, DOI: 10.2307/2259783 CrossrefGoogle Scholar

  • [8] Groeters F.R., Dingle H., Genetic and maternal influences on life history plasticity in milkweed bugs (Oncopeltus): response to temperature, Journal of Evolutionary Biology, 1988, 1, 317–333, DOI: 10.1046/j.1420-9101.1988.1040317.x CrossrefGoogle Scholar

  • [9] Crill W.D., Huey R.B., Gilchrist G.W., Within- and betweengeneration effects of temperature on the morphology and physiology of Drosophila melanogaster, Evolution, 1996, 1205–1218, DOI: 10.2307/2410661 CrossrefGoogle Scholar

  • [10] Blanckenhorn W.U., Temperature effects on egg size and their fitness consequences in the yellow dung fly Scathophaga stercoraria, Evol Ecol, 2000, 14, 627–643, DOI: 10.1023/A:1010911017700 CrossrefGoogle Scholar

  • [11] Steigenga M.J., Fischer K., Within- and between-generation effects of temperature on life-history traits in a butterfly, Journal of Thermal Biology, 2011, 32, 396–405, DOI: 10.1016/j.jtherbio.2007.06.001 CrossrefGoogle Scholar

  • [12] Geister T.L., Lorenz M.W., Hoffmann K.H., Fischer K., Energetics of embryonic development: effects of temperature on egg and hatchling composition in a butterfly, Journal of Comparative Physiology B, 2009, 179, 87–98, DOI: 10.1007/ s00360-008-0293-5 CrossrefGoogle Scholar

  • [13] Burgess S.C., Marshall D.J., Temperature-induced maternal effects and environmental predictability, Journal of Experimental Biology, 2011, 214, 2329–2336, DOI: 10.1242/ jeb.054718 CrossrefGoogle Scholar

  • [14] Swain D.P., Lindsey C.C., Meristic variation in a clone of the cyprinodont fish Rivulus marmoratus related to temperature history of the parents and of the embryos, Canadian Journal of Zoology, 1986, 64, 1444–1455, DOI: 10.1139/z86-216 CrossrefGoogle Scholar

  • [15] Travis J., McManus M.G., Baer C.F., Sources of variation in physiological phenotypes and their evolutionary significance, Integrative and Comparative Biology, 1999, 39, 422–433, DOI: 10.1093/icb/39.2.422 CrossrefGoogle Scholar

  • [16] Salinas S., Munch S.B., Thermal legacies: transgenerational effects of temperature on growth in a vertebrate, Ecology Letters, 2012, 15, 159–163, DOI: 10.1111/j.1461- 0248.2011.01721.x CrossrefGoogle Scholar

  • [17] Donelson J.M., Munday P.L., McCormick M.I., Pitcher C.R., Rapid transgenerational acclimation of a tropical reef fish to climate change, Nature Climate Change, 2012, 2, 30–32, DOI: 10.1038/nclimate1323 CrossrefGoogle Scholar

  • [18] Dentry W., Lindsey C.C., Vertebral variation in zebrafish (Brachydanio rerio) related to the prefertilization temperature history of their parents, Canadian Journal of Zoology, 1978, 56, 280–283, DOI: 10.1139/z78-037 CrossrefGoogle Scholar

  • [19] Riginos C., Heschel M.S., Schmitt J., Maternal effects of drought stress and inbreeding in Impatiens capensis (Balsaminaceae), American Journal of Botany, 2007, 94, 1984–1991, DOI: 10.3732/ajb.94.12.1984 CrossrefGoogle Scholar

  • [20] Sultan S.E., Barton K., Wilczek A.M., Contrasting patterns of transgenerational plasticity in ecologically distinct congeners, Ecology, 2009, 90, 1831–1839, DOI: 10.1890/08-1064.1 CrossrefGoogle Scholar

  • [21] Herman J.J., Sultan S.E., Horgan-Kobelski T., Riggs C., Adaptive transgenerational plasticity in an annual plant: grandparental and parental drought stress enhance performance of seedlings in dry soil, Integrative and Comparative Biology, 2012, 52, 77– 88, DOI: 10.1093/icb/ics041 CrossrefGoogle Scholar

  • [22] Yoder J.A., Tank J.L., Rellinger E.J., Evidence of a maternal effect that protects against water stress in larvae of the American dog tick, Dermacentor variabilis (Acari: Ixodidae), Journal of Insect Physiology, 2006, 52, 1034–1042, DOI: 10.1016/j.jinsphys.2006.07.002 CrossrefGoogle Scholar

  • [23] Lau J.A., Peiffer J., Reich P.B., Tiffin P., Transgenerational effects of global environmental change: long-term CO2 and nitrogen treatments influence offspring growth response to elevated CO2, Oecologia, 2008, 158, 141–150, DOI: 10.1007/s00442-008-1127-6 CrossrefGoogle Scholar

  • [24] Parker L.M., Ross P.M., O’Connor W.A., Borysko L., Raftos D.A., Pörtner H.-O., Adult exposure influences offspring response to ocean acidification in oysters, Global Change Biology, 2012, 18, 82–92, DOI: 10.1111/j.1365- 2486.2011.02520.x CrossrefGoogle Scholar

  • [25] Miller G.M., Watson S.-A., Donelson J.M., McCormick M.I., Munday P.L., Parental environment mediates impacts of increased carbon dioxide on a coral reef fish, Nature Climate Change, 2012, 2, 1–4, DOI: 10.1038/nclimate1599 CrossrefGoogle Scholar

  • [26] Molinier J., Ries G., Zipfel C., Hohn B., Transgeneration memory of stress in plants, Nature, 2006, 442, 1046–1049, DOI: 10.1038/nature05022 CrossrefGoogle Scholar

  • [27] Jacobs B.S., Lesmeister S.A., Maternal environmental effects on fitness, fruit morphology and ballistic seed dispersal distance in an annual forb, Functional Ecology, 2012, 26, 588–597, DOI: 10.1111/j.1365-2435.2012.01964.x CrossrefGoogle Scholar

  • [28] Etterson J.R., Galloway L.F., The influence of light on paternal plants in Campanula americana (Campanulaceae): pollen characteristics and offspring traits, American Journal of Botany, 2002, 89, 1899–1906, DOI: 10.3732/ajb.89.12.1899 CrossrefGoogle Scholar

  • [29] Galloway L.F., Etterson J.R., Transgenerational plasticity is adaptive in the wild, Science, 2007, 318, 1134–1136, DOI: 10.1126/science.1148766 CrossrefGoogle Scholar

  • [30] Galloway L.F., The effect of maternal and paternal environments on seed characters in the herbaceous plant Campanula Americana (Campanulaceae), American Journal of Botany, 2001, 88, 832–840, DOI: 10.2307/2657035 CrossrefGoogle Scholar

  • [31] Latzel V., Janeček Š., Doležal J., Klimešová J., Bossdorf O., Adaptive transgenerational plasticity in the perennial Plantago lanceolata, Oikos, 2013, (in press), DOI: 10.1111/j.1600- 0706.2013.00537.x CrossrefGoogle Scholar

  • [32] Miao S.L., Bazzaz F.A., Primack R.B., Effects of maternal nutrient pulse on reproduction of two colonizing Plantago species, Ecology, 1991, 72, 586–596, DOI: 10.2307/2937198 CrossrefGoogle Scholar

  • [33] Wulff R.D., Causin H.F., Benitez O., Bacalini P.A., Intraspecific variability and maternal effects in the response to nutrient addition in Chenopodium album, Canadian Journal of Botany, 1999, 77, 1150–1158, DOI: 10.1139/cjb-77-8-1150 CrossrefGoogle Scholar

  • [34] Sultan S.E., Phenotypic plasticity for offspring traits in Polygonum persicaria, Ecology, 1996, 77, 1791–1807, DOI: 10.2307/2265784 CrossrefGoogle Scholar

  • [35] Dyer A.R., Brown C.S., Espeland E.K., McKay J.K., Meimberg H., Rice K.J., The role of adaptive trans-generational plasticity in biological invasions of plants, Evolutionary Applications, 2010, 3, 179–192, DOI: 10.1111/j.1752-4571.2010.00118.x CrossrefGoogle Scholar

  • [36] Amzallag G.N., Influence of parental NaCl treatment on salinity tolerance of offspring in Sorghum bicolor (L.) Moench, New Phytologist, 1994, 128, 715–723, DOI: 10.1111/j.1469- 8137.1994.tb04035.x CrossrefGoogle Scholar

  • [37] Alekseev V., Lampert W., Maternal control of resting-egg production in Daphnia, Nature, 2001, 414, 899–901, DOI: 10.1038/414899a CrossrefGoogle Scholar

  • [38] Fernandez-Gonzalez M.A., Gonzalez-Barrientos J., Carter M.J., Ramos-Jiliberto R., Parent-to-offspring transfer of sublethal effects of copper exposure: metabolic rate and life-history traits of Daphnia, Revista Chilena de Historia Natural, 2011, 84, 195–201, DOI: 10.4067/S0716- 078X2011000200005 CrossrefGoogle Scholar

  • [39] Kwok K.W.H., Grist E.P.M., Leung K.M.Y., Acclimation effect and fitness cost of copper resistance in the marine copepod Tigriopus japonicus, Ecotoxicology and Environmental Safety, 2009, 72, 358–364, DOI: 10.1016/j.ecoenv.2008.03.014 CrossrefGoogle Scholar

  • [40] Marshall D.J., Transgenerational plasticity in the sea: contextdependent maternal effects across the life history, Ecology, 2008, 89, 418–427, DOI: 10.1890/07-0449.1 CrossrefGoogle Scholar

  • [41] Tait N.N., Atapattu D., Browne R., Effect of salinity change on early development in Galeolaria caespitosa (Polychaeta: Serpulidae), Marine and Freshwater Research, 1984, 35, 483–486, DOI: 10.1071/MF9840483 CrossrefGoogle Scholar

  • [42] Hintz J.L., Lawrence J.M., Acclimation of gametes to reduced salinity prior to spawning in Luidia clathrata (Echinodermata: Asteroidea), Marine Biology, 1994, 120, 443–446, DOI: 10.1007/BF00680219 CrossrefGoogle Scholar

  • [43] Nye J.A., Davis D.D., Miller T.J., The effect of maternal exposure to contaminated sediment on the growth and condition of larval Fundulus heteroclitus, Aquatic Toxicology, 2007, 82, 242–250, DOI: 10.1016/j.aquatox.2007.02.011 CrossrefGoogle Scholar

  • [44] Kinne O., Irreversible nongenetic adaptation, Comparative Biochemistry and Physiology, 1962, 5, 265–282, DOI: 10.1016/0010-406X(62)90056-7 CrossrefGoogle Scholar

  • [45] Lin H.C., Hsu S.C., Hwang P.P., Maternal transfer of cadmium tolerance in larval Oreochromis mossambicus, Journal of Fish Biology, 2000, 57, 239–249, DOI: 10.1006/jfbi.2000.1339 CrossrefGoogle Scholar

  • [46] Sellin M.K., Kolok A.S., Maternally derived Cu tolerance in larval fathead minnows: how long does it persist? Journal of Fish Biology, 2006, 69, 1570–1574, DOI: 10.1111/j.1095- 8649.2006.01210.x CrossrefGoogle Scholar

  • [47] Burggren W., Blank T., Physiological study of larval fishes: challenges and opportunities, Scientia Marina, 2009, 73, 99–110, DOI: 10.3989/scimar.2009.73s1099 CrossrefGoogle Scholar

  • [48] Ho D.H., Burggren W.W., Parental hypoxic exposure confers offspring hypoxia resistance in zebrafish (Danio rerio), Journal of Experimental Biology, 2012, 215, 4208–4216, DOI: 10.1242/jeb.074781 CrossrefGoogle Scholar

  • [49] Karadas F., Pappas A.C., Surai P.F., Speake B.K., Embryonic development within carotenoid-enriched eggs influences the post-hatch carotenoid status of the chicken, Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 2005, 141, 244–251, DOI: 10.1016/j. cbpc.2005.04.001 CrossrefGoogle Scholar

  • [50] Agrawal A.A., Herbivory and maternal effects: mechanisms and consequences of transgenerational induced plant resistance, Ecology, 2002, 83, 3408–3415, DOI: 10.1890/0012-9658(2002)083[3408:HAMEMA]2.0.CO;2 CrossrefGoogle Scholar

  • [51] Gianoli E., González-Teuber M., Effect of support availability, mother plant genotype and maternal support environment on the twining vine Ipomoea purpurea, Plant Ecology, 2005, 179, 231–235, DOI: 10.1007/s11258-005-0198-2 CrossrefGoogle Scholar

  • [52] Latzel V., Klimešová J., Hájek T., Gómez S., Šmilauer P., Maternal effects alter progeny’s response to disturbance and nutrients in two Plantago species, Oikos, 2010, 119, 1700– 1710, DOI: 10.1111/j.1600-0706.2010.18737.x CrossrefGoogle Scholar

  • [53] Plaistow S.J., Lapsley C.T., Benton T.G., Context-dependent intergenerational effects: the interaction between past and present environments and its effect on population dynamics, The American Naturalist, 2006, 167, 206–215, DOI: 10.1086/499380 CrossrefGoogle Scholar

  • [54] Mestre L., Bonte D., Food stress during juvenile and maternal development shapes natal and breeding dispersal in a spider, Behavioral Ecology, 2012, 23, 759–764, DOI: 10.1093/ beheco/ars024 CrossrefGoogle Scholar

  • [55] LaMontagne J.M., McCauley E., Maternal effects in Daphnia: what mothers are telling their offspring and do they listen? Ecology Letters, 2001, 4, 64–71, DOI: 10.1046/j.1461- 0248.2001.00197.x CrossrefGoogle Scholar

  • [56] Mitchell S.E., Read A.F., Poor maternal environment enhances offspring disease resistance in an invertebrate, Proceedings of the Royal Society B, 2005, 272, 2601–2607, DOI: 10.1038/ng1202-569 CrossrefGoogle Scholar

  • [57] Little T.J., O’Connor B., Colegrave N., Watt K., Read A.F., Maternal transfer of strain-specific immunity in an invertebrate, Curr. Biol, 2003, 13, 489–492, DOI: 10.1016/ S0960-9822(03)00163-5 CrossrefGoogle Scholar

  • [58] Gustafsson S., Rengefors K., Hansson L.-A., Increased consumer fitness following transfer of toxin tolerance to offspring via maternal effects, Ecology, 2005, 86, 2561– 2567, DOI: 10.1890/04-1710 CrossrefGoogle Scholar

  • [59] Agrawal A.A., Laforsch C., Tollrian R., Transgenerational induction of defences in animals and plants, Nature, 1999, 401, 60–63, DOI: 10.1038/43425 CrossrefGoogle Scholar

  • [60] Zadereev Y.S., Maternal effects, conspecific chemical cues, and switching from parthenogenesis to gametogenesis in the cladoceran Moina macrocopa, Aquatic Ecology, 2003, 37, 251–255, DOI: 10.1023/A:1025850417717 CrossrefGoogle Scholar

  • [61] Lopatina T.S., Zadereev E.S., The effect of food concentration on the juvenile somatic growth rate of body length, fecundity and the production of resting eggs by Moina brachiata (Crustacea: Cladocera) single females, Journal of Siberian Federal University - Biology, 2012, 4, 427–438 Google Scholar

  • [62] Hafer N., Ebil S., Uller T., Pike N., Transgenerational effects of food availability on age at maturity and reproductive output in an asexual collembolan species, Biology Letters, 2011, 7, 755–758, DOI: 10.1098/rsbl.2011.0139 CrossrefGoogle Scholar

  • [63] Storm J.J., Lima S.L., Mothers forewarn offspring about predators: a transgenerational maternal effect on behavior, The American Naturalist, 2010, 175, 382–390, DOI: 10.1086/650443 CrossrefGoogle Scholar

  • [64] Islam S.M., Roessingh P., Simpson S.J., McCaffery A.R., Parental effects on the behaviour and colouration of nymphs of the desert locust Schistocerca gregaria, Journal of Insect Physiology, 1994, 40, 173–181, DOI: 10.1016/0022- 1910(94)90089-2 CrossrefGoogle Scholar

  • [65] Via S., The genetic structure of host plant adaptation in a spatial patchwork: demographic variability among reciprocally transplanted pea aphid clones, Evolution, 1991, 827–852, DOI: 10.2307/2409692 CrossrefGoogle Scholar

  • [66] Zehnder C.B., Hunter M.D., A comparison of maternal effects and current environment on vital rates of Aphis nerii, the milkweed–oleander aphid, Ecological Entomology, 2007, 32, 172–180, DOI: 10.1111/j.1365-2311.2007.00853.x CrossrefGoogle Scholar

  • [67] Kyneb A., Toft S., Effects of maternal diet quality on offspring performance in the rove beetle Tachyporus hypnorum, Ecological Entomology, 2006, 31, 322–330, DOI: 10.1111/j.1365-2311.2006.00775.x CrossrefGoogle Scholar

  • [68] Moret Y., “Trans-generational immune priming”: specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor, Proceedings of the Royal Society B, 2006, 273, 1399–1405, DOI: 10.1098/ rspb.2006.3465 CrossrefGoogle Scholar

  • [69] Futuyma D.J., Herrmann C., Milstein S., Keese M.C., Apparent transgenerational effects of host plant in the leaf beetle Ophraella notulata (Coleoptera: Chrysomelidae), Oecologia, 1993, 96, 365–372, DOI: 10.1007/BF00317507 CrossrefGoogle Scholar

  • [70] Bonduriansky R., Head M., Maternal and paternal condition effects on offspring phenotype in Telostylinus angusticollis (Diptera: Neriidae), Journal of Evolutionary Biology, 2007, 20, 2379–2388, DOI: 10.1111/j.1420-9101.2007.01419.x CrossrefGoogle Scholar

  • [71] Vijendravarma R.K., Narasimha S., Kawecki T.J., Effects of parental larval diet on egg size and offspring traits in Drosophila, Biology Letters, 2010, 6, 238–241, DOI: 10.1098/rspb.1998.0366 CrossrefGoogle Scholar

  • [72] Grech K., Maung L., Read A.F., The effect of parental rearing conditions on offspring life history in Anopheles stephensi, Malaria Journal, 2007, 6, 130, DOI: 10.1186/1475-2875-6-130 CrossrefGoogle Scholar

  • [73] Triggs A.M., Knell R.J., Parental diet has strong transgenerational effects on offspring immunity, Functional Ecology, 2012, 1409–1417, DOI: 10.1111/j.1365- 2435.2012.02051.x CrossrefGoogle Scholar

  • [74] Cahenzli F., Erhardt A., Transgenerational acclimatization in an herbivore-host plant relationship, Proceedings of the Royal Society B, 2013, 280, 20122856, DOI: 10.1098/ rspb.2012.2856 CrossrefGoogle Scholar

  • [75] Rotem K., Agrawal A.A., Kott L., Parental effects in Pieris rapae in response to variation in food quality: adaptive plasticity across generations? Ecological Entomology, 2003, 28, 211–218, DOI: 10.1046/j.1365-2311.2003.00507.x CrossrefGoogle Scholar

  • [76] Harvey S.C., Orbidans H.E., All eggs are not equal: the maternal environment affects progeny reproduction and developmental fate in Caenorhabditis elegans, PLoS ONE, 2011, 6, e25840, DOI: 10.1371/journal.pone.0025840.t001 CrossrefGoogle Scholar

  • [77] Kaneko G., Yoshinaga T., Yanagawa Y., Ozaki Y., Tsukamoto K., Watabe S., Calorie restriction-induced maternal longevity is transmitted to their daughters in a rotifer, Functional Ecology, 2011, 25, 209–216, DOI: 10.1111/j.1365- 2435.2010.01773.x CrossrefGoogle Scholar

  • [78] Lin H.C., Dunson W.A., An explanation of the high strain diversity of a self-fertilizing hermaphroditic fish, Ecology, 1995, 593–605, DOI: 10.2307/1941216 CrossrefGoogle Scholar

  • [79] Bashey F., Cross-generational environmental effects and the evolution of offspring size in the Trinidadian guppy Poecilia reticulata, Evolution, 2006, 60, 348–361, DOI: 10.1111/ j.0014-3820.2006.tb01111.x CrossrefGoogle Scholar

  • [80] Cadby C.D., Jones S.M., Wapstra E., Potentially adaptive effects of maternal nutrition during gestation on offspring phenotype of a viviparous reptile, Journal of Experimental Biology, 2011, 214, 4234–4239, DOI: 10.1242/jeb.057349 CrossrefGoogle Scholar

About the article

Received: 2013-07-28

Accepted: 2013-08-31

Published Online: 2013-10-22


Citation Information: Non-Genetic Inheritance, ISSN (Online) 2084-8846, DOI: https://doi.org/10.2478/ngi-2013-0005.

Export Citation

©2013 Santiago Salinas et al., licensee Versita Sp. z o. o. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivs license (http://creativecommons.org/licenses/by-nc-nd/3.0/), which means that the text may be used for non-commercial purposes, provided credit is given to the author.. This content is open access.

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

[1]
Sonia E. Sultan
Interface Focus, 2017, Volume 7, Number 5, Page 20170009
[4]
Ø. N. Kielland, C. Bech, and S. Einum
Proceedings of the Royal Society B: Biological Sciences, 2017, Volume 284, Number 1846, Page 20162494
[5]
Philip L. Munday, Jennifer M. Donelson, and Jose A. Domingos
Global Change Biology, 2017, Volume 23, Number 1, Page 307
[7]
Lisa N.S. Shama, Felix C. Mark, Anneli Strobel, Ana Lokmer, Uwe John, and K. Mathias Wegner
Evolutionary Applications, 2016, Volume 9, Number 9, Page 1096
[8]
Araceli Rodríguez-Romero, Michael D. Jarrold, Gloria Massamba-N'Siala, John I. Spicer, and Piero Calosi
Evolutionary Applications, 2016, Volume 9, Number 9, Page 1082
[9]
Natalí J. Delorme and Mary A. Sewell
Marine Biology, 2016, Volume 163, Number 10
[10]
Jacob J. Herman and Sonia E. Sultan
Proceedings of the Royal Society B: Biological Sciences, 2016, Volume 283, Number 1838, Page 20160988
[11]
[12]
Mark S. Poesch, Louise Chavarie, Cindy Chu, Shubha N. Pandit, and William Tonn
Fisheries, 2016, Volume 41, Number 7, Page 385
[13]
Elise Mazé-Guilmo, Simon Blanchet, Olivier Rey, Nicolas Canto, and Géraldine Loot
Proceedings of the Royal Society B: Biological Sciences, 2016, Volume 283, Number 1830, Page 20160587
[14]
Benjamin G. Van Allen and Volker H. W. Rudolf
Proceedings of the National Academy of Sciences, 2016, Volume 113, Number 25, Page 6939
[15]
Jodie L Rummer and Philip L Munday
Fish and Fisheries, 2017, Volume 18, Number 1, Page 22
[16]
Mikko Vihtakari, Jon Havenhand, Paul E. Renaud, and Iris E. Hendriks
Frontiers in Marine Science, 2016, Volume 3
[17]
Pauline M. Ross, Laura Parker, and Maria Byrne
ICES Journal of Marine Science: Journal du Conseil, 2016, Volume 73, Number 3, Page 537
[19]
Santiago Salinas
Nature Climate Change, 2014, Volume 4, Number 12, Page 1054
[20]
Sushil Kumar, Renu Kumari, and Vishakha Sharma
Agricultural Research, 2015, Volume 4, Number 2, Page 109
[21]
Jennifer M. Donelson and Philip L. Munday
Global Change Biology, 2015, Volume 21, Number 8, Page 2954
[22]
E DePasquale, H Baumann, and CJ Gobler
Marine Ecology Progress Series, 2015, Volume 523, Page 145
[23]
Alex J. Malvezzi, Christopher S. Murray, Kevin A. Feldheim, Joseph D. DiBattista, Dany Garant, Christopher J. Gobler, Demian D. Chapman, and Hannes Baumann
Evolutionary Applications, 2015, Volume 8, Number 4, Page 352
[24]
Blair K. Adams, David Cote, and Jeffrey A. Hutchings
Ecology of Freshwater Fish, 2016, Volume 25, Number 2, Page 307
[25]
Catherine A. Pfister, Andrew J. Esbaugh, Christina A. Frieder, Hannes Baumann, Emily E. Bockmon, Meredith M. White, Brendan R. Carter, Heather M. Benway, Carol A. Blanchette, Emily Carrington, James B. McClintock, Daniel C. McCorkle, Wade R. McGillis, T. Aran Mooney, and Patrizia Ziveri
Environmental Science & Technology, 2014, Volume 48, Number 17, Page 9982
[26]
Franziska M. Schade, Catriona Clemmesen, and K. Mathias Wegner
Marine Biology, 2014, Volume 161, Number 7, Page 1667
[27]
CS Murray, A Malvezzi, CJ Gobler, and H Baumann
Marine Ecology Progress Series, 2014, Volume 504, Page 1
[28]
Lisa N. S. Shama, Anneli Strobel, Felix C. Mark, K. Mathias Wegner, and Dustin Marshall
Functional Ecology, 2014, Volume 28, Number 6, Page 1482

Comments (0)

Please log in or register to comment.
Log in