Opinion
Transgenerational Plasticity in Human-Altered Environments

https://doi.org/10.1016/j.tree.2019.09.003Get rights and content

Highlights

  • Human activities are dramatically altering ecological communities. While many organisms are threatened by human-induced rapid environmental change (HIREC), others are thriving. This variability is often attributed to differences in genetic variation and/or within-generational plasticity, but transgenerational plasticity (TGP) may be another key (often overlooked) process that contributes to this variation.

  • We develop a framework that explores how TGP can affect organisms’ responses to HIREC. We highlight three sequential processes in the detection and transmission of parental cues to offspring that are critical for TGP to be beneficial in a given environment.

  • Because many hypotheses regarding TGP in human-altered environments have yet to be tested, our framework summarizes potential positive and negative outcomes and outlines key areas for future study.

Our ability to predict how species will respond to human-induced rapid environmental change (HIREC) may depend upon our understanding of transgenerational plasticity (TGP), which occurs when environments experienced by previous generations influence phenotypes of subsequent generations. TGP evolved to help organisms cope with environmental stressors when parental environments are highly predictive of offspring environments. HIREC can alter conditions that favored TGP in historical environments by reducing parents’ ability to detect environmental conditions, disrupting previous correlations between parental and offspring environments, and interfering with the transmission of parental cues to offspring. Because of the propensity to produce errors in these processes, TGP will likely generate negative fitness outcomes in response to HIREC, though beneficial fitness outcomes may occur in some cases.

Section snippets

Considering Transgenerational Plasticity in the Context of Human-Induced Rapid Environmental Change

Humans are profoundly affecting the global abundance and distribution of organisms by facilitating habitat loss and fragmentation [1], introducing exotic species [2], overharvesting wild populations [3], increasing pollutant exposure [4], and altering the global climate [5]. While some species (e.g., invasive species, commensal pests) have been successful [6] under human-induced rapid environmental change (HIREC) (see Glossary) [7], other species exhibit maladaptive responses that contribute to

How HIREC Alters Environments in Ways That May Influence the Benefits of TGP

TGP is likely to be beneficial if: (i) parents can detect and identify current environmental conditions, (ii) parental environments accurately predict offspring environments, and (iii) parents can accurately transmit information to offspring so that it can be integrated into offspring phenotypes [17]. Here, we outline a framework that highlights how HIREC is likely to produce errors in one or more of these processes if HIREC produces a mismatch between current environmental conditions and

Overall Fitness Consequences of HIREC-Induced TGP

HIREC will likely reduce parents’ ability to detect and assess their own environment, alter historical relationships in the degree of autocorrelation between parental and offspring environments, and limit the accuracy of information transmission and reception between parents and offspring. Because errors can occur at each stage, we argue that TGP is especially prone to errors compared with WGP, which may have severe consequences for offspring fitness in human-altered environments.

If parents

Concluding Remarks

HIREC is likely to make TGP maladaptive if it alters one or more of the conditions that made TGP adaptive in historical environments. As environments become more variable and unpredictable, TGP may facilitate species declines, at least until parents can evolve mechanisms to better detect novel environmental conditions or evolve novel TGP pathways to more accurately convey information about novel environmental conditions to offspring (see Outstanding Questions). However, TGP may also allow rapid

Acknowledgments

We thank M. Bensky for creating the images for Figure 1 and S. Gignoux-Wolfsohn, R. Fletcher, and three anonymous reviewers for providing helpful comments that improved the manuscript. While writing the manuscript, J.K.H. was supported by a National Institutes of Health NRSA fellowship (award #F32GM121033), S.C.D. was supported by a Smithsonian Institutional Postdoctoral Fellowship, A.M.B. was supported by NSF IOS-1121980 and 191100 and NIH 2R01GM082937-06A1, B.L. was supported by NSF

Glossary

Autocorrelation
similarity between environmental conditions in a temporal or spatial series.
Cue reliability
how well environmental cues reflect environmental conditions.
Diversified bet hedging (DBH)
when parents increase phenotypic variance in their offspring to lower the variance in genotypic fitness; can be a type of TGP if the parents’ environment modifies offspring phenotypic variation.
Ecological trap
a type of evolutionary trap; when organisms choose a suboptimal habitat, even though there is

References (82)

  • J.J. Gilroy et al.

    Beyond ecological traps: perceptual errors and undervalued resources

    Trends Ecol Evol

    (2007)
  • B. Barrett

    Counter-culture: does social learning help or hinder adaptive response to human-induced rapid environmental change?

    Front Ecol Evol

    (2019)
  • J.A. Stamps et al.

    Bayesian models of development

    Trends Ecol Evol

    (2016)
  • D. Legrand

    Eco-evolutionary dynamics in fragmented landscapes

    Ecography

    (2017)
  • A. Kuparinen et al.

    Harvest-induced evolution: insights from aquatic and terrestrial systems

    Philos. Trans. R. Soc. Lond. B Biol. Sci.

    (2017)
  • M. Saaristo

    Direct and indirect effects of chemical contaminants on the behaviour, ecology and evolution of wildlife

    Proc. Biol. Sci.

    (2018)
  • E.A. Beever

    Behavioral flexibility as a mechanism for coping with climate change

    Front. Ecol. Environ.

    (2017)
  • E.M. Wolkovich

    Temperature-dependent shifts in phenology contribute to the success of exotic species with climate change

    Am. J. Bot.

    (2013)
  • A. Sih

    Evolution and behavioural responses to human-induced rapid environmental change

    Evol. Appl.

    (2011)
  • T.P. Hughes

    Global warming and recurrent mass bleaching of corals

    Nature

    (2017)
  • S. Bonamour

    Phenotypic plasticity in response to climate change: the importance of cue variation

    Philos. Trans. R. Soc. Lond. B Biol. Sci.

    (2019)
  • C. Parmesan et al.

    Plants and climate change: complexities and surprises

    Ann. Bot.

    (2015)
  • A.M. Davidson

    Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis

    Ecol. Lett.

    (2011)
  • B. Wong et al.

    Behavioral responses to changing environments

    Behav. Ecol.

    (2015)
  • E. Jablonka

    The adaptive advantage of phenotypic memory in changing environments

    Philos. Trans. R. Soc. Lond. B Biol. Sci.

    (1995)
  • J.M. Donelson

    Transgenerational plasticity and climate change experiments: where do we go from here?

    Glob. Chang. Biol.

    (2018)
  • R.J. Fletcher

    How the type of anthropogenic change alters the consequences of ecological traps

    Proc. Biol. Sci.

    (2012)
  • A.M. Bell et al.

    An integrative framework for understanding the mechanisms and multigenerational consequences of transgenerational plasticity

    Annu. Rev. Ecol. Evol. Syst. Published online July

    (2019)
  • J. Herman et al.

    Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations

    Front. Plant Sci.

    (2011)
  • T.A. Mousseau et al.

    Maternal Effects as Adaptations

    (1998)
  • M.J. Sheriff

    Integrating ecological and evolutionary context in the study of maternal stress

    Integr. Comp. Biol.

    (2017)
  • T.G. Groothuis

    Revisiting mechanisms and functions of prenatal hormone-mediated maternal effects using avian species as a model

    Philos. Trans. R. Soc. Lond. B Biol. Sci.

    (2019)
  • K. McJunkin

    Maternal effects of microRNAs in early embryogenesis

    RNA Biol

    (2018)
  • O. Leimar et al.

    The evolution of transgenerational integration of information in heterogeneous environments

    Am Nat

    (2015)
  • J.M. McNamara

    Detection vs. selection: integration of genetic, epigenetic and environmental cues in fluctuating environments

    Ecol Lett

    (2016)
  • B. Kuijper et al.

    When to rely on maternal effects and when on phenotypic plasticity?

    Evolution

    (2015)
  • T. Uller

    Weak evidence for anticipatory parental effects in plants and animals

    J Evol Biol

    (2013)
  • S.C. Burgess et al.

    Adaptive parental effects: the importance of estimating environmental predictability and offspring fitness appropriately

    Oikos

    (2014)
  • A. Bošković et al.

    Transgenerational epigenetic inheritance

    Annu Rev Genet

    (2018)
  • J.L. Pick

    The more you get, the more you give: positive cascading effects shape the evolutionary potential of prenatal maternal investment

    Evol Lett

    (2019)
  • J.W. McGlothlin et al.

    The contribution of maternal effects to selection response: an empirical test of competing models

    Evolution

    (2014)
  • Cited by (0)

    7

    These authors contributed equally to this work

    View full text