Skip to main content
SpringerLink
Log in

Pitfalls in ecological research – transgenerational effects

  • Published:
Folia Geobotanica Aims and scope Submit manuscript

Abstract

The phenotype of an individual can be affected by the environment of its predecessors, a phenomenon commonly referred to as transgenerational effects. These effects, if not properly acknowledged and/or controlled, can impede proper interpretation of ecological studies. Using examples from more than 40 recently published studies, I discuss the most frequently used methodological approaches to deal with unwanted transgenerational effects in ecological research. In this literature, growing one generation in a common environment before the experiment or fitting seed and/or seedling size as a covariate were the most prevalent tools used to account for or even out transgenerational effects. Although these methods can efficiently control for transgenerational effects of limited generational persistence, usually just one generation of offspring, they cannot sufficiently control for effects across multiple generations. I propose that, whenever possible in ecological experiments, two generations of plants be grown in a common environment prior to the main experiment and that extreme caution should be exercised in interpreting results if the degree of transgenerational effects is not known. I also suggest that in addition to controlling for transgenerational effects in ecological research, we should actively investigate transgenerational effects as a source of plant variation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agrawal A (2001) Transgenerational consequences of plant responses to herbivory: an adaptive maternal effect? Am Nat 157:555–569

    Article  CAS  PubMed  Google Scholar 

  • Agrawal A (2002) Herbivory and maternal effects: mechanisms and consequences of transgenerational induced plant resistance. Ecology 83:3408–3415

    Article  Google Scholar 

  • Ågren J, Schemske DW (2012) Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range. New Phytol 194:1112–1122

    Article  PubMed  Google Scholar 

  • Andalo C, Raquin C, Machon N, Godelle B, Mousseau M (1998) Direct and maternal effects of elevated CO2 on early root growth of germinating Arabidopsis thaliana seedlings. Ann Bot 81:405–411

    Article  Google Scholar 

  • Ariza C, Tielbörger K (2011) An evolutionary approach to studying the relative importance of plant-plant interactions along environmental gradients. Funct Ecol 25:932–942

    Article  Google Scholar 

  • Barski A, Cuddapah S, Cui KR, Roh TY, Schones DE, Wang ZB, Wei G, Chepelev I, Zhao KJ (2007) High-resolution profiling of histone methylations in the human genome. Cell 129:823–837

    Article  CAS  PubMed  Google Scholar 

  • Bennington CC, Fetcher N, Vavrek MC, Shaver GR, Cummings KJ, McGraw JB (2012) Home site advantage in two long-lived arctic plant species: results from two 30-year reciprocal transplant studies. J Ecol 100:841–851

    Article  Google Scholar 

  • Bird A (2007) Perceptions of epigenetics. Nature 447:396–398

    Article  CAS  PubMed  Google Scholar 

  • Bischoff A, Müller-Schärer H (2010) Testing population differentiation in plant species—how important are environmental maternal effects. Oikos 119:445–454

    Article  Google Scholar 

  • Bischoff A, Hurault B (2013) Scales and drivers of local adaptation in Brassica nigra (Brassicaceae) populations. Am J Bot 100:1162–1170

    Article  PubMed  Google Scholar 

  • Bischoff A, Trémulot S (2011) Differentiation and adaptation in Brassica nigra populations: interactions with related herbivores. Oecologia 165:971–81

    Article  PubMed  Google Scholar 

  • Bockelmann AC, Wels T, Bakker JP (2011) Seed origin determines the range expansion of the clonal grass Elymus athericus. Basic Appl Ecol 12:496–504

    Article  Google Scholar 

  • Bossdorf O, Shuja Z, Banta JA (2009) Genotype and maternal environment affect belowground interactions between Arabidopsis thaliana and its competitors. Oikos 118:1541–1551

    Article  Google Scholar 

  • Boyko A, Blevins T, Yao Y, Golubov A, Bilichak A, Ilnytskyy Y, Hollander J, Meins F, Kovalchuk I (2010) Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of dicer–like proteins. PLoS ONE 5:e9514

    Article  PubMed Central  PubMed  Google Scholar 

  • Bradshaw AD (2006) Unravelling phenotypic plasticity – why should we bother? New Phytol 170:644–648

    Article  PubMed  Google Scholar 

  • Breen AN, Richards JH (2008) Irrigation and fertilization effects on seed number, size, germination and seedling growth: implications for desert shrub establishment. Oecologia 157:13–19

    Article  CAS  PubMed  Google Scholar 

  • Colomé-Tatché M, Cortijo S, Wardenaar R, Morgado L, Lahouze B, Sarazin A, Etcheverry M, Martin A, Feng S, Duvernois-Berthet E, Labadie K, Wincker P, Jacobsem SE, Jansen RC, Colot V, Johannes F (2012) Features of the Arabidopsis recombination landscape resulting from combined loss of sequence variation and DNA methylation. Proc Natl Acad Sci USA 109:16240–16245

    Article  PubMed Central  PubMed  Google Scholar 

  • Cortijo S, Wardenaar R, Colomé-Tatché M, Gilly A, Etcheverry M, Labadie K, Caillieux E, Hospital F, Aury J, Wincker P, Roudier F, Jansen RC, Colot V, Johannes F (2014) Mapping the Epigenetic Basis of Complex Traits. Science 343:1145–1148

    Article  CAS  PubMed  Google Scholar 

  • Dias BG, Ressler K (2014) Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat Neurosci 17:89–96

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Doubková P, Suda J, Sudová R (2012) The symbiosis with arbuscular mycorrhizal fungi contributes to plant tolerance to serpentine edaphic stress. Soil Biol Biochem 44:56–64

    Article  Google Scholar 

  • Ebeling SK, Stöcklin J, Hensen I, Auge H (2011) Multiple common garden experiments suggest lack of local adaptation in an invasive ornamental plant. J Plant Ecol 4:209–220

    Article  Google Scholar 

  • Emery NC, Rice KJ, Stanton ML (2011) Fitness variation and local distribution limits in an annual plant population. Evolution 65:1011–1020

    Article  PubMed  Google Scholar 

  • Erfmeier A, Böhnke M, Bruelheide H (2011) Secondary invasion of Acer negundo: the role of phenotypic responses versus local adaptation. Biol Invas 13:1599–1614

    Article  Google Scholar 

  • De Frenne P, Brunet J, Shevtsova A, Kolb A, Graae BJ, Chabrerie O, Cousin SAO, Decocq G, DeSchrijver A, Diekmann M, Gruwez R, Heinken T, Hermy M, Nilsson C, Stanton S, Tack W, Willaert J, Verheyen K (2011) Temperature effects on forest herbs assessed by warming and transplant experiments along a latitudinal gradient. Glob Chang Biol 17:3240–3253

    Article  Google Scholar 

  • De Frenne P, Graae BJ, Brunet J, Shevtsova A, De Schrijver A, Chabrerie O, Cousin SAO, Decocq G, DeSchrijver A, Diekmann M, Gruwez R, Heinken, Kolb A, Nilsson C, Stanton S, Verheyen K (2012) The response of forest plant regeneration to temperature variation along a latitudinal gradient. Ann Bot 109:1037–1046

    Article  PubMed Central  PubMed  Google Scholar 

  • Galloway LF (2001) The effect of maternal and paternal environments on seed characters in the herbaceous plant Campanula americana (Campanulaceae). Am J Bot 88:832–840

    Article  CAS  PubMed  Google Scholar 

  • Galloway LF, Etterson JR (2007) Transgenerational plasticity is adaptive in the wild. Science 318:1134–1136

    Article  CAS  PubMed  Google Scholar 

  • Godoy O, Saldaña A, Fuentes N, Valladares F, Gianoli E. (2011) Forests are not immune to plant invasions: phenotypic plasticity and local adaptation allow Prunella vulgaris to colonize a temperate evergreen rainforest. Biol Invas 13:1615–1625

    Article  Google Scholar 

  • Gormally CL, Donovan LA (2011) No Evidence of Local Adaptation in Uniola paniculata L. (Poaceae), a Coastal Dune Grass. Southeast Nat 10:751–760

    Article  Google Scholar 

  • Grady KC, Ferrier SM, Kolb TE, Hart SC, Allan GJ, Whitham TG (2011) Genetic variation in productivity of foundation riparian species at the edge of their distribution: implications for restoration and assisted migration in a warming climate. Glob Chang Biol 17:3724–3735

    Article  Google Scholar 

  • Grady KC, Laughlin DC, Ferrier SM, Kolb TE, Hart SC, Allan GJ, Whitham TG (2013) Conservative leaf economic traits correlate with fast growth of genotypes of a foundation riparian species near the thermal maximum extent of its geographic range. Funct Ecol 27:428–438

    Article  Google Scholar 

  • Grierson CS, Barnes SR, Chase MW, Clarke M, Grierson D, Edwards KJ, Jellis GJ, Jones JD, Knapp S, Oldroyd G, Poppy G, Temple P, Williams R, Bastow R (2011) One hundred important questions facing plant science research. New Phytol 192:6–12

    Article  CAS  PubMed  Google Scholar 

  • Haggerty BP, Galloway LF (2011) Response of individual components of reproductive phenology to growing season length in a monocarpic herb. J Ecol 99:242–253

    Article  Google Scholar 

  • Halpern SL (2005) Sources and consequences of seed size variation in Lupinus perennis (Fabaceae): adaptive and non-adaptive hypotheses. Am J Bot 92:205–213

    Article  PubMed  Google Scholar 

  • Hufford KM, Mazer SJ (2012) Local Adaptation and the Effects of Grazing on the Performance of Nassella pulchra: Implications for Seed Sourcing in Restoration. Restor Ecol 20:688–695

    Article  Google Scholar 

  • Ishizuka W, Goto S (2012) Modeling intraspecific adaptation of Abies sachalinensis to local altitude and responses to global warming, based on a 36-year reciprocal transplant experiment. Evol Appl 5:229–244

    Article  PubMed Central  PubMed  Google Scholar 

  • Jablonka E, Lamb MJ (1995) Epigenetic inheritance and evolution: The Lamarckian dimension. Oxford University Press, Oxford

    Google Scholar 

  • Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, et al. (2009) Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet 5:e1000530

    Article  PubMed Central  PubMed  Google Scholar 

  • Kaati, G, Bygren LO, Edvinsson S (2002) Cardiovascular and diabetes mortality determined by nutrition during parents’ and grandparents’ slow growth period. Europ J Hum Genet 10:682–688

    Article  CAS  PubMed  Google Scholar 

  • Kalske A, Muola A, Laukkanen L, Mutikainen P, Leimu R (2012) Variation and constraints of local adaptation of a long-lived plant, its pollinators and specialist herbivores. J Ecol 100:1359–1372

    Article  Google Scholar 

  • Kawai Y, Kudo G (2011) Local differentiation of flowering phenology in an alpine-snowbed herb Gentiana nipponica. Botany 89:361–367

    Article  Google Scholar 

  • Kim E, Donohue K (2013) Local adaptation and plasticity of Erysimum capitatum to altitude: its implications for responses to climate change. J Ecol 101:796–805

    Article  Google Scholar 

  • Knapp EE, Rice KJ (2011) Effects of competition and temporal variation on the evolutionary potential of two native bunchgrass species. Restor Ecol 19:407–417

    Article  Google Scholar 

  • Koutecká E, Lepš J (2013) The growth and survival of three closely related Myosotis species in a 3-year transplant experiment. Botany 91:209–217

    Article  Google Scholar 

  • Krannitz PG (1997) Seed weight variability of antelope bitterbrush (Purshia tridentata: Rosaceae). Am Mid Nat 138:306–321

    Article  Google Scholar 

  • Lande R (2009) Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J Evol Biol 22:1435–1446

    Article  PubMed  Google Scholar 

  • Latzel V, Allan E, Bortolini Silveira A, Colot V, Fischer M, Bossdorf O (2013) Epigenetic diversity increases the productivity and stability of plant populations. Nat Commun 4:2875

    Article  PubMed  Google Scholar 

  • Latzel V, Hájek T, Klimešová J, Gómez S (2009) Nutrients and disturbance history in two Plantago species: maternal effects as a clue for observed dichotomy between resprouting and seeding strategies. Oikos 118:1669–1678

    Article  Google Scholar 

  • Latzel V, Janeček Š, Doležal J, Klimešová J, Bossdorf O (2014) Adaptive transgenerational plasticity in the perennial Plantago lanceolata. Oikos 123:41–46

    Article  Google Scholar 

  • Latzel V, Klimešová J (2010) Year-to-year changes in expression of maternal effects in perennial plants. Basic Appl Ecol 11:702–708

    Article  Google Scholar 

  • Latzel V, Klimešová J, Hájek T, Gómez S, Šmilauer P (2010) Maternal effects alter progeny’s response to disturbance and nutrients in two Plantago species. Oikos 119:1700–1710

    Article  Google Scholar 

  • Leinonen PH, Remington DL, Savolainen O (2011) Local adaptation, phenotypic differentiation, and hybrid fitness in diverged natural populations of Arabidopsis lyrata. Evolution 65:90–107

    Article  PubMed  Google Scholar 

  • Leinonen PH, Remington DL, Leppälä J, Savolainen O (2013) Genetic basis of local adaptation and flowering time variation in Arabidopsis lyrata. Mol Ecol 22:709–23

    Article  CAS  PubMed  Google Scholar 

  • Liancourt P, Tielbörger K (2011) Ecotypic differentiation determines the outcome of positive interactions in a dryland annual plant species. Perspect Plant Ecol Evol Syst 13:259–264

    Article  Google Scholar 

  • Lipowsky A, Schmid B, Roscher C (2011) Selection for monoculture and mixture genotypes in a biodiversity experiment. Basic Appl Ecol 12:360–371

    Article  Google Scholar 

  • Martin SL, Husband BC (2013) Adaptation of diploid and tetraploid Chamerion angustifolium to elevation but not local environment. Evolution 67:1780–91

    Article  PubMed  Google Scholar 

  • Meineri E, Spindelböck J, Vandvik V (2013) Seedling emergence responds to both seed source and recruitment site climates: a climate change experiment combining transplant and gradient approaches. Plant Ecol 214:607–619

    Article  Google Scholar 

  • Miao SL, Bazzaz FA, Primack RB (1991) Persistence of maternal nutrient effects in Plantago major: The third generation. Ecology 72:1634–1642

    Article  Google Scholar 

  • Mousseau TA, Fox CW (1998) Maternal Effects as Adaptations. Oxford University Press, New York

    Google Scholar 

  • Muhamed H, Touzard B, Le Bagousse-Pinguet Y, Michalet R (2013) The role of biotic interactions for the early establishment of oak seedlings in coastal dune forest communities. For Ecol Manage 297:67–74

    Article  Google Scholar 

  • Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladeres F, van Kleunen M (2010) Plant phenotypic plasticity in a changing climate. Trends Plant Sci 15:684–692

    Article  CAS  PubMed  Google Scholar 

  • O’Farrill G, Chapman CA, Gonzalez A (2011) Origin and deposition sites influence seed germination and seedling survival of Manilkara zapota: implications for long-distance, animal-mediated seed dispersal. Seed Sci Res 21:305–313

    Article  Google Scholar 

  • Ortegón-Campos I, Abdala-Roberts L, Parra-Tabla V, Cervera CJ, Marrufo-Zapata D, Herrera CM (2012) Influence of multiple factors on plant local adaptation: soil type and folivore effects in Ruellia nudiflora (Acanthaceae). Evol Ecol 26:545–558

    Article  Google Scholar 

  • Palm E, Brady K, Van Volkenburgh E (2012) Serpentine tolerance in Mimulus guttatus does not rely on exclusion of magnesium. Funct Plant Biol 39:679–688

    Article  CAS  Google Scholar 

  • Plaistow SJ, Benton TG (2009) The influence of context-dependent maternal effects on population dynamics: an experimental test. Philos Trans R Soc Lond B Biol Sci 364:1049–1058

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Raj S, Bräutigam K, Hamanishi ET, Wilkins O, Schroeder W, Mansfield SD, Plant AL, Campbell M (2011) Clone history shapes Populus drought responses. Proc Natl Acad Sci USA 108:12521–12526

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rice KJ, Gerlach JD, Dyer AR, McKay JK (2013) Evolutionary ecology along invasion fronts of the annual grass Aegilops triuncialis. Biol Invasions 15:2531–2545

    Article  Google Scholar 

  • Richards EJ (2006) Inherited epigenetic variation – revisiting soft inheritance. Nat Rev Genet 7:395–401

    Article  CAS  PubMed  Google Scholar 

  • Riginos C, Heschel MS, Schmitt J (2007) Maternal effects of drought stress and inbreeding in Impatiens capensis (Balsaminaceae). Am J Bot 94:1984–1991

    Article  PubMed  Google Scholar 

  • Roach DA, Wulff RD (1987) Maternal effects in plants. Annu Rev Ecol Syst 18:209–235

    Article  Google Scholar 

  • Rossiter MC (1996) Incidence and consequences of inherited environmental effects. Annu Rev Ecol Syst 27:451–476

    Article  Google Scholar 

  • Scheepens JF, Stöcklin J (2013) Flowering phenology and reproductive fitness along a mountain slope: maladaptive responses to transplantation to a warmer climate in Campanula thyrsoides. Oecologia 171:679–691

    Article  CAS  PubMed  Google Scholar 

  • Schreiber SG, Ding C, Hamann A, Hacke UG, Thomas BR, Brouard JS (2013) Frost hardiness vs. growth performance in trembling aspen: an experimental test of assisted migration. J Appl Ecol 50:939–949

    Article  Google Scholar 

  • Smith DS, Schweitzer JA, Turk P, Bailey JK, Hart SC, Shuster SM, Whitham TG (2012) Soil-mediated local adaptation alters seedling survival and performance. Plant Soil 352:243–251

    Article  CAS  Google Scholar 

  • Souther S, Lechowicz MJ, McGraw JB (2012) Experimental test for adaptive differentiation of ginseng populations reveals complex response to temperature. Ann Bot 110:829–837

    Article  PubMed Central  PubMed  Google Scholar 

  • Sõber V, Ramula S (2013) Seed number and environmental conditions do not explain seed size variability for the invasive herb Lupinus polyphyllus. Plant Ecol 214:883–892

    Article  Google Scholar 

  • Stanton-Geddes J, Shaw RG, Tiffin P (2012) Interactions between soil habitat and geographic range location affect plant fitness. PLoS ONE 7:e36015

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sultan SE, Barton K, Wilczek AM (2009) Contrasting patterns of transgenerational plasticity in ecologically distinct congeners. Ecology 90:1831–1839

    Article  PubMed  Google Scholar 

  • Van Steensel B, Henikoff S (2003) Epigenomic profiling using microarrays. Biotechniques 35:346–357

    PubMed  Google Scholar 

  • Volis S (2011) Adaptive genetic differentiation in a predominantly self-pollinating species analyzed by transplanting into natural environment, crossbreeding and Q ST – F ST test. New Phytol 192:237–248

    Article  CAS  PubMed  Google Scholar 

  • Wagner D (2003) Chromatin regulation of plant development. Curr Opin Plant Biol 6:20–28

    Article  CAS  PubMed  Google Scholar 

  • Whittle C, Otto SP, Johnston MO, Krochko JE (2009) Adaptive epigenetic memory of ancestral temperature regime in Arabidopsis thaliana. Botany 87:650–657

    Article  CAS  Google Scholar 

  • Woods EC, Hastings AP, Turley NE, Heard SB, Agrawal AA (2012) Adaptive geographical clines in the growth and defense of a native plant. Ecol Monograph 82:149–168

    Article  Google Scholar 

  • Yost JM, Barry T, Kay KM, Rajakaruna N (2012) Edaphic adaptation maintains the coexistence of two cryptic species on serpentine soils. Am J Bot 99:890–897

    Article  CAS  PubMed  Google Scholar 

  • Zhou W, Wang Z, Davy AJ, Liu G (2013) Geographic variation and local adaptation in Oryza rufipogon across its climatic range in China. J Ecol 101:1498–1508

    Article  Google Scholar 

Download references

Acknowledgements

I thank Zuzana Münzbergová, Hana Skálová, Věroslava Hadincová, Veronika Dumalasová and Jitka Klimešová for critical discussions during the preparation of the manuscript. I am also grateful to Jonathan Rosenthal for improving the English and his valuable comments. Very helpful and inspiring were also the comments of two anonymous reviewers. This study was financially supported by the Czech Science Foundation (grant GA14–06802S) and by institutional long-term research development project RVO 67985939.

Author information

Authors and Affiliations

  1. Institute of Botany, Czech Academy of Sciences, Zámek 1, CZ-252 43, Průhonice, Czech Republic

    Vít Latzel

Authors
  1. Vít Latzel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vít Latzel.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Latzel, V. Pitfalls in ecological research – transgenerational effects. Folia Geobot 50, 75–85 (2015). https://doi.org/10.1007/s12224-015-9208-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12224-015-9208-x

Keywords

Search

Navigation