Abstract
Maternal effects directly and indirectly modify an offspring’s phenotype during development, preparing the offspring for an environment similar to an environment experienced by the mother. Evolutionarily, this could be adaptive if organisms did not experience a large amount of environmental variation across generations. We argue increased anthropogenic changes have led maternal effects to be maladaptive in plants. Similar problems in humans have been proposed, where metabolic diseases may be increased by a mismatch between the in utero environment and the adult environment; often referred to as the Barker Hypothesis. Plants may experience similar metabolic and functional disorders, caused by maternal effects generated from unreliable environmental cues. In the last 200 years, human activities have increased habitat fragmentation, changed patterns of nutrient deposition, and increased climatic variation within and among years. In this manuscript, we suggest that ecologists should consider the increased negative influence of maternal effects on plant growth and reproduction in spatially fragmented and temporally stochastic landscapes. Several implications for conservation and research arise from this discussion: (1) researchers should focus on evolutionarily relevant measures of spatial and temporal heterogeneity, (2) the maternal history of seeds used for population restoration should be considered, and (3) contiguous habitats should be constructed to reduce the impact of evolutionary traps.
Similar content being viewed by others
References
Barker DJP (1997) Maternal nutrition, fetal nutrition, and disease in later life. Nutrition 13:807–813
Battin J (2004) When good animals love bad habitats: ecological traps and the conservation of animal populations. Conserv Biol 18:1482–1491
Bischoff A, Muller-Scharer H (2010) Testing population differentiation in plant species - how important are environmental maternal effects. Oikos 119:445–454
Comstock JP, Ehleringer JR (1992) Plant adaptation in the Great-Basin and Colorado Plateau. Great Basin Nat 52:195–215
Cordeiro NJ, Ndangalasi HJ, McEntee JP, Howe HF (2009) Disperser limitation and recruitment of an endemic African tree in a fragmented landscape. Ecology 90:1030–1041
Donohue K, Schmitt J (1998) Maternal environmental effects in plants: adaptive plasticity? In: Mousseau TA, Fox CW (eds) Maternal effects as adaptations?. Oxford University Press, New York, pp 137–158
Donohue K, Dorn L, Griffith C, Kim E, Aguilera A, Polisetty CR, Schmitt J (2005) The evolutionary ecology of seed germination of Arabidopsis thaliana: variable natural selection on germination timing. Evolution 59:758–770
Dyer AR, Brown CS, Espeland EK, McKay JK, Meimberg H, Rice KJ (2010) The role of adaptive trans-generational plasticity in biological invasions of plants. Evol Appl 3:179–192
Ehrlen J, Eriksson O (2000) Dispersal limitation and patch occupancy in forest herbs. Ecology 81:1667–1674
Gabriel W (2006) Selective advantage of irreversible and reversible phenotypic plasticity. Arch Hydrobiol 167:1–20
Galloway LF, Etterson JR (2007) Transgenerational plasticity is adaptive in the wild. Science 318:1134–1136
Galloway LF, Etterson JR, McGlothlin JW (2009) Contribution of direct and maternal genetic effects to life-history evolution. New Phytol 183:826–838
Garcia M, Litago J, Palacios-Orueta A, Pinzon JE, Ustin SL (2010) Short-term propagation of rainfall perturbations on terrestrial ecosystems in central California. Appl Veg Sci 13:146–162
Godfrey KM, Barker DJP (2000) Fetal nutrition and adult disease. Am J Clin Nutr 71:1344S–1352S
Guzman A, Stevenson PR (2008) Seed dispersal, habitat selection and movement patterns in the Amazonian tortoise, Geochelone denticulata. Amphib-reptil 29:463–472
Helenurm K, Schaal BA (1996) Genetic and maternal effects on offspring fitness in Lupinus texensis (Fabaceae). Am J Bot 83:1596–1608
Hoegh-Guldberg O, Hughes L, McIntyre S, Lindenmayer DB, Parmesan C, Possingham HP, Thomas CD (2008) Assisted colonization and rapid climate change. Science 321:345–346
Hooftman DAP, van Kleunen M, Diemer M (2003) Effects of habitat fragmentation on the fitness of two common wetland species, Carex davalliana and Succisa pratensis. Oecologia 134:350–359
Hufford KM, Mazer SJ (2003) Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends Ecol Evol 18:147–155
Kaplan RH (1992) Greater maternal investment can decrease offspring survival in the frog Bombina orientalis. Ecology 73:280–288
Khurana E, Singh JS (2001) Ecology of tree seed and seedlings: implications for tropical forest conservation and restoration. Curr Sci 80:748–757
Kjaersgaard A, Faurby S, Andersen DH, Pertoldi C, David JR, Loeschcke V (2007) Effects of temperature and maternal and grandmaternal age on wing shape in parthenogenetic Drosophila mercatorum. J Therm Biol 32:59–65
Kleb HR, Wilson SD (1999) Scales of heterogeneity in prairie and forest. Can J Bot-Revue Canadienne De Botanique 77:370–376
Kolesnichenko AV, Pobezhimova TP, Grabelnych OI, Tourchaninova VV, Korzun AM, Koroleva NA, Zykova VV, Voinikov VK (2003) Difference between the temperature of non-hardened and hardened winter wheat seedling shoots during cold stress. J Therm Biol 28:235–244
Kueffer C, Kronauer L, Edwards PJ (2009) Wider spectrum of fruit traits in invasive than native floras may increase the vulnerability of oceanic islands to plant invasions. Oikos 118:1327–1334
Kyneb A, Toft S (2006) Effects of maternal diet quality on offspring performance in the rove beetle Tachyporus hypnorum. Ecol Entomol 31:322–330
Lucas RW, Forseth IN, Casper BB (2008) Using rainout shelters to evaluate climate change effects on the demography of Cryptantha flava. J Ecol 96:514–522
Major KM, Davison IR (1998) Influence of temperature and light on growth and photosynthetic physiology of Fucus evanescens (Phaeophyta) embryos. Eur J Phycol 33:129–138
Marshall DJ, Allen RM, Crean AJ (2008) The ecological and evolutionary importance of maternal effects in the sea. In: Gibson RN, Atkinson RJA, Gordon JDM (eds) Oceanography and marine biology: an annual review, vol 46. CRC Press-Taylor and Francis Group, Boca Raton, pp 203–250
Marshall DJ, Heppell SS, Munch SB, Warner RR (2010) The relationship between maternal phenotype and offspring quality: do older mothers really produce the best offspring? Ecology 91:2862–2873
Matejek B, Huber C, Dannenmann M, Kohlpaintner M, Gasche R, Papen H (2010) Microbial N turnover processes in three forest soil layers following clear cutting of an N saturated mature spruce stand. Plant Soil 337:93–110
McLachlan JS, Hellmann JJ, Schwartz MW (2007) A framework for debate of assisted migration in an era of climate change. Conserv Biol 21:297–302
Mech LD, Nelson ME, McRoberts RE (1991) Effects of maternal and grandmaternal nutrition on deer mass and vulnterability to wolf predation. J Mammal 72:146–151
Molinier J, Ries G, Zipfel C, Hohn B (2006) Transgeneration memory of stress in plants. Nature 442:1046–1049
Moron V, Robertson AW, Ward MN (2006) Seasonal predictability and spatial coherence of rainfall characteristics in the tropical setting of Senegal. Mon Weather Rev 134:3248–3262
Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol and Evol 13:403–407
Nathan R, Muller-Landau HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol 15:278–285
Newman D, Pilson D (1997) Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution 51:354–362
Ouborg NJ, Vergeer P, Mix C (2006) The rough edges of the conservation genetics paradigm for plants. J Ecol 94:1233–1248
Quintana-Ascencio PF, Weekley CW, Menges ES (2007) Comparative demography of a rare species in Florida scrub and road habitats. Biol Conserv 137:263–270
Ravelli ACJ, van der Meulen JHP, Michels RPJ, Osmond C, Barker DJP, Hales CN, Bleker OP (1998) Glucose tolerance in adults after prenatal exposure to famine. Lancet 351:173–177
Ricciardi A, Simberloff D (2009) Assisted colonization is not a viable conservation strategy. Trends Ecol Evol 24:248–253
Roach DA, Wulff RD (1987) Maternal effects in plants. Annu Rev Ecol Syst 18:209–235
Rodrigo J (2000) Spring frosts in deciduous fruit trees - morphological damage and flower hardiness. Sci Hortic 85:155–173
Rohde A, Junttila O (2008) Remembrances of an embryo: long-term effects on phenology traits in spruce. New Phytol 177:2–5
Roseboom TJ, van der Meulen JHP, Ravelli ACJ, van Montfrans GA, Osmond C (1998) Blood pressure in adults after prenatal exposure to the Dutch famine. J Hypertens 16:P3604
Ruager-Martin R, Hyde MJ, Modi N (2010) Maternal obesity and infant outcomes. Early Hum Dev 86:715–722
Schlaepfer MA, Runge MC, Sherman PW (2002) Ecological and evolutionary traps. Trends Ecol Evol 17:474–480
Schmid B, Dolt C (1994) Effects of maternal and paternal environment and genotype on offspring phenotype in Solidago altissima l. Evolution 48:1525–1549
Strong DT, Sale PWG, Helyar KR (1998) The influence of the soil matrix on nitrogen mineralisation and nitrification. I. Spatial variation and a hierarchy of soil properties. Aust J Soil Res 36:429–447
Thompson JD (1991) Phenotypic plasticity as a component of evolutionary change. Trends Ecol Evol 6:246–249
Uller T (2008) Developmental plasticity and the evolution of parental effects. Trends Ecol Evol 23:432–438
Wolf JB, Wade MJ (2009) What are maternal effects (and what are they not)? Philos Trans R Soc B-Biol Sci 364:1107–1115
Wolfe LM, Mazer SJ (2005) Patterns of phenotypic plasticity and their fitness consequences in wild radish (Raphanus sativus : Brassicaceae). Int J Plant Sci 166:631–640
Wulff RD, Causin HF, Benitez O, Bacalini PA (1999) Intraspecific variability and maternal effects in the response to nutrient addition in Chenopodium album. Can J Bot-Revue Canadienne De Botanique 77:1150–1158
Acknowledgments
We would like to thank Rob Fletcher at The University of Florida, Brian Allan, the Chase lab, and James Cheverud at Washington University for helpful comments and reviews. Also, the comments from two anonymous reviewers greatly improved this manuscript. This work was partly supported by an EPA Science to Achieve Results Fellowship awarded to M.S.S.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Schuler, M.S., Orrock, J.L. The maladaptive significance of maternal effects for plants in anthropogenically modified environments. Evol Ecol 26, 475–481 (2012). https://doi.org/10.1007/s10682-011-9499-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10682-011-9499-1