Evolutionary Biology

Sensitive windows for within- and trans-generational plasticity of anti-predator defences

10.24072/pcjournal.304 - Peer Community Journal, Volume 3 (2023), article no. e71.

Get full text PDF Peer reviewed and recommended by PCI

Transgenerational plasticity could be an important mechanism for adaptation to variable environments in addition to within-generational plasticity. But its potential for adaptation may be restricted to specific developmental windows that are highly sensitive and responsive to environmental cues. Determining these sensitive windows is essential to understand the temporal dynamic of environmental cue detection, phenotype induction and selection. We examined the sensitive windows of both within- and trans-generational plasticity of anti-predator defences in the freshwater snail Physa acuta. Parental snails were exposed to olfactory cues of their crayfish predator at different exposure windows: embryonic development, early, mid or late post-embryonic development. Behavioural and morphological defences were then assessed in adult parents and offspring. The sensitive window of within-generational plasticity was the embryonic development, the whole post-embryonic development, or a combination of early-life and late development depending on the defence. This showed that early-life periods of development (embryonic and early post-embryonic) are sensitive windows of within-generational plasticity. However, the sensitive window also persisted until late developmental stages for some defences, providing evidence that the early-life is not the only sensitive window as empirical and theoretical studies often state. There were less sensitive windows for transgenerational plasticity: embryonic and/or mid post-embryonic development. Interestingly, the embryonic period was a sensitive window of transgenerational plasticity for a defence only when it was also a sensitive window of within-generational plasticity for that defence. On the opposite, the mid post-embryonic development was a sensitive window specific to transgenerational plasticity. This suggests that transgenerational plasticity, although linked to within-generational plasticity by the embryonic sensitive window, may also be induced via a specific channel, independent of within-generational plasticity induction and expression. Finally, the late developmental window was never a sensitive window of transgenerational plasticity as it was theoretically expected. This result may be explained by the potential long-term reliability of parental cues in our system. It is worth noting that we did not find any sensitive window for some defences, either because none of them induced the defence or all exposure windows induced the defence in a similar magnitude. Overall, the developmental window of cue exposure shapes within- and trans-generational responses and thus brings complexity to the study of phenotypic plasticity, notably when it comes to determining its adaptive potential.

Published online:
DOI: 10.24072/pcjournal.304
Keywords: timing of exposure; sensitive windows; critical windows; predator-prey interactions; Physa acuta; phenotypic plasticity; transgenerational effects; inducible defences
Tariel-Adam, Juliette 1, 2; Luquet, Émilien 1; Plénet, Sandrine 1

1 Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, F-69622, Villeurbanne, France
2 Fish Lab, Department of Biological Sciences, Macquarie University, Sydney, NSW, Australia
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Tariel-Adam, Juliette and Luquet, \'Emilien and Pl\'enet, Sandrine},
     title = {Sensitive windows for within- and trans-generational plasticity of anti-predator defences},
     journal = {Peer Community Journal},
     eid = {e71},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.304},
     language = {en},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.304/}
AU  - Tariel-Adam, Juliette
AU  - Luquet, Émilien
AU  - Plénet, Sandrine
TI  - Sensitive windows for within- and trans-generational plasticity of anti-predator defences
JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.304/
DO  - 10.24072/pcjournal.304
LA  - en
ID  - 10_24072_pcjournal_304
ER  - 
%0 Journal Article
%A Tariel-Adam, Juliette
%A Luquet, Émilien
%A Plénet, Sandrine
%T Sensitive windows for within- and trans-generational plasticity of anti-predator defences
%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.304/
%R 10.24072/pcjournal.304
%G en
%F 10_24072_pcjournal_304
Tariel-Adam, Juliette; Luquet, Émilien; Plénet, Sandrine. Sensitive windows for within- and trans-generational plasticity of anti-predator defences. Peer Community Journal, Volume 3 (2023), article  no. e71. doi : 10.24072/pcjournal.304. https://peercommunityjournal.org/articles/10.24072/pcjournal.304/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100639

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Agrawal, A. A.; Laforsch, C.; Tollrian, R. Transgenerational induction of defences in animals and plants, Nature, Volume 401 (1999) no. 6748, pp. 60-63 | DOI

[2] Ahlgren, J.; Chapman, B. B.; Nilsson, P. A.; Brönmark, C. Individual boldness is linked to protective shell shape in aquatic snails, Biology Letters, Volume 11 (2015) no. 4 | DOI

[3] Alexander, J. E.; Covich, A. P. Predation Risk and Avoidance Behavior in Two Freshwater Snails, The Biological Bulletin, Volume 180 (1991) no. 3, pp. 387-393 | DOI

[4] Alexander, J. E.; Covich, A. P. Predator avoidance by the freshwater snail Physella virgata in response to the crayfishProcambarus simulans, Oecologia, Volume 87 (1991) no. 3, pp. 435-442 | DOI

[5] Auld, J. R.; Relyea, R. A. Are there interactive effects of mate availability and predation risk on life history and defence in a simultaneous hermaphrodite?, Journal of Evolutionary Biology, Volume 21 (2008) no. 5, pp. 1371-1378 | DOI

[6] Auld, J. R.; Relyea, R. A. Life-history plasticity and inbreeding depression under mate limitation and predation risk: cumulative lifetime fitness dissected with a life table response experiment, Evolutionary Ecology, Volume 24 (2010) no. 5, pp. 1171-1185 | DOI

[7] Auld, J. R.; Relyea, R. A. Adaptive plasticity in predator-induced defenses in a common freshwater snail: altered selection and mode of predation due to prey phenotype, Evolutionary Ecology, Volume 25 (2010) no. 1, pp. 189-202 | DOI

[8] Bates, D.; Mächler, M.; Bolker, B.; Walker, S. Fitting Linear Mixed-Effects Models Using lme4, Journal of Statistical Software, Volume 67 (2015) no. 1 | DOI

[9] Beaty, L. E.; Wormington, J. D.; Kensinger, B. J.; Bayley, K. N.; Goeppner, S. R.; Gustafson, K. D.; Luttbeg, B. Shaped by the past, acting in the present: transgenerational plasticity of anti‐predatory traits, Oikos, Volume 125 (2016) no. 11, pp. 1570-1576 | DOI

[10] Bell, A. M.; Hellmann, J. K. An Integrative Framework for Understanding the Mechanisms and Multigenerational Consequences of Transgenerational Plasticity, Annual Review of Ecology, Evolution, and Systematics, Volume 50 (2019) no. 1, pp. 97-118 | DOI

[11] Ben-Shachar, M.; Lüdecke, D.; Makowski, D. effectsize: Estimation of Effect Size Indices and Standardized Parameters, Journal of Open Source Software, Volume 5 (2020) no. 56 | DOI

[12] Blumstein, D. T.; Daniel, J. C. Quantifying Behavior the JWatcher Way, Sinauer Associates, Sunderland, 2007

[13] Bonamour, S.; Chevin, L.-M.; Charmantier, A.; Teplitsky, C. Phenotypic plasticity in response to climate change: the importance of cue variation, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 374 (2019) no. 1768 | DOI

[14] Bonduriansky, R.; Crean, A. J. What are parental condition‐transfer effects and how can they be detected?, Methods in Ecology and Evolution, Volume 9 (2017) no. 3, pp. 450-456 | DOI

[15] Bradshaw, A. Evolutionary Significance of Phenotypic Plasticity in Plants, Advances in Genetics, Elsevier, 1965, pp. 115-155 | DOI

[16] Bukowski, S. J.; Auld, J. R. The effects of calcium in mediating the inducible morphological defenses of a freshwater snail, Physa acuta, Aquatic Ecology, Volume 48 (2014) no. 1, pp. 85-90 | DOI

[17] Burton, T.; Metcalfe, N. B. Can environmental conditions experienced in early life influence future generations?, Proceedings of the Royal Society B: Biological Sciences, Volume 281 (2014) no. 1785 | DOI

[18] Covich, A. P.; Crowl, T. A.; Alexander,, J. E.; Vaughn, C. C. Predator-Avoidance Responses in Freshwater Decapod-Gastropod Interactions Mediated by Chemical Stimuli, Journal of the North American Benthological Society, Volume 13 (1994) no. 2, pp. 283-290 | DOI

[19] Crowl, T. A.; Covich, A. P. Predator-Induced Life-History Shifts in a Freshwater Snail, Science, Volume 247 (1990) no. 4945, pp. 949-951 | DOI

[20] Deng, Y.; Bossdorf, O.; Scheepens, J. F. Transgenerational effects of temperature fluctuations in Arabidopsis thaliana, AoB PLANTS, Volume 13 (2021) no. 6 | DOI

[21] DeWitt, T. J.; Robinson, B. W.; Wilson, D. S. Functional Diversity among Predators of a Freshwater Snail Imposes an Adaptive Trade-off for Shell Morphology, Evolutionary Ecology Research, Volume 2 no. 2, pp. 129-148

[22] Donelan, S. C.; Hellmann, J. K.; Bell, A. M.; Luttbeg, B.; Orrock, J. L.; Sheriff, M. J.; Sih, A. Transgenerational Plasticity in Human-Altered Environments, Trends in Ecology & Evolution, Volume 35 (2020) no. 2, pp. 115-124 | DOI

[23] English, S.; Barreaux, A. M. The evolution of sensitive periods in development: insights from insects, Current Opinion in Behavioral Sciences, Volume 36 (2020), pp. 71-78 | DOI

[24] English, S.; Fawcett, T. W.; Higginson, A. D.; Trimmer, P. C.; Uller, T. Adaptive use of information during growth can explain long-term effects of early life experiences, The American Naturalist, Volume 187 (2016) no. 5, pp. 620-632 | DOI

[25] Fallet, M.; Luquet, E.; David, P.; Cosseau, C. Epigenetic inheritance and intergenerational effects in mollusks, Gene, Volume 729 (2020) | DOI

[26] Faulk, C.; Dolinoy, D. C. Timing is everything, Epigenetics, Volume 6 (2011) no. 7, pp. 791-797 | DOI

[27] Fawcett, T. W.; Frankenhuis, W. E. Adaptive explanations for sensitive windows in development, Frontiers in Zoology, Volume 12 (2015) no. Suppl 1 | DOI

[28] Feil, R.; Fraga, M. F. Epigenetics and the environment: emerging patterns and implications, Nature Reviews Genetics, Volume 13 (2012) no. 2, pp. 97-109 | DOI

[29] Galloway, L. F.; Etterson, J. R. Transgenerational Plasticity Is Adaptive in the Wild, Science, Volume 318 (2007) no. 5853, pp. 1134-1136 | DOI

[30] Groothuis, T. G. G.; Taborsky, B. Introducing biological realism into the study of developmental plasticity in behaviour, Frontiers in Zoology, Volume 12 (2015) no. Suppl 1 | DOI

[31] Hales, N. R.; Schield, D. R.; Andrew, A. L.; Card, D. C.; Walsh, M. R.; Castoe, T. A. Contrasting gene expression programs correspond with predator-induced phenotypic plasticity within and across generations inDaphnia, Molecular Ecology, Volume 26 (2017) no. 19, pp. 5003-5015 | DOI

[32] Henry, P.-Y.; Bousset, L.; Sourrouille, P.; Jarne, P. Partial selfing, ecological disturbance and reproductive assurance in an invasive freshwater snail, Heredity, Volume 95 (2005) no. 6, pp. 428-436 | DOI

[33] Henry, P.-Y.; Jarne, P. Marking hard-shelled gastropods: tag loss, impact on life-history traits, and perspectives in biology, Invertebrate Biology, Volume 126 (2007) no. 2, pp. 138-153 | DOI

[34] Hoverman, J. T.; Relyea, R. A. How flexible is phenotypic plasticity? Developmental windows for trait induction and reversal, Ecology, Volume 88 (2007) no. 3, pp. 693-705 | DOI

[35] Jablonka, E.; Oborny, B.; Molnar, I.; Kisdi, E.; Hofbauer, J.; Czaran, T. The adaptive advantage of phenotypic memory in changing environments, Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Volume 350 (1995) no. 1332, pp. 133-141 | DOI

[36] Jonsson, B.; Jonsson, N. Early environment influences later performance in fishes, Journal of Fish Biology, Volume 85 (2014) no. 2, pp. 151-188 | DOI

[37] Josse, J.; Husson, F. missMDA: A Package for Handling Missing Values in Multivariate Data Analysis, Journal of Statistical Software, Volume 70 (2016) no. 1 | DOI

[38] Kassambara, A. Ggpubr: 'ggplot2' Based Publication Ready Plots, Manual

[39] Keiser, C. N.; Mondor, E. B. Transgenerational Behavioral Plasticity in a Parthenogenetic Insect in Response to Increased Predation Risk, Journal of Insect Behavior, Volume 26 (2013) no. 4, pp. 603-613 | DOI

[40] Kuznetsova, A.; Brockhoff, P. B.; Christensen, R. H. B. lmerTest Package: Tests in Linear Mixed Effects Models, Journal of Statistical Software, Volume 82 (2017) no. 13, pp. 1-26 | DOI

[41] Lê, S.; Josse, J.; Husson, F. FactoMineR: An R Package for Multivariate Analysis, Journal of Statistical Software, Volume 25 (2008) no. 1, pp. 1-18 | DOI

[42] Leimar, O.; McNamara, J. M. The Evolution of Transgenerational Integration of Information in Heterogeneous Environments, The American Naturalist, Volume 185 (2015) no. 3 | DOI

[43] Lenth, R. Emmeans: Estimated Marginal Means, Aka Least-Squares Means

[44] Luquet, E.; Tariel, J. Offspring reaction norms shaped by parental environment: interaction between within- and trans-generational plasticity of inducible defenses, BMC Evolutionary Biology, Volume 16 (2016) no. 1 | DOI

[45] McCarthy, T.; Dickey, B. Chemically mediated effects of injured prey on behavior of both prey and predators, Behaviour, Volume 139 (2002) no. 5, pp. 585-602 | DOI

[46] McNamara, J. M.; Dall, S. R. X.; Hammerstein, P.; Leimar, O. Detection vs. selection: integration of genetic, epigenetic and environmental cues in fluctuating environments, Ecology Letters, Volume 19 (2016) no. 10, pp. 1267-1276 | DOI

[47] Mikulski, A.; Czernik, M.; Pijanowska, J. Induction time and reversibility of changes in Daphnia life history caused by the presence of fish, Journal of Plankton Research, Volume 27 (2005) no. 8, pp. 757-762 | DOI

[48] Mikulski, A.; Pijanowska, J. When and how can Daphnia prepare their offspring for the threat of predation?, Hydrobiologia, Volume 643 (2010) no. 1, pp. 21-26 | DOI

[49] Mousseau, T. The adaptive significance of maternal effects, Trends in Ecology & Evolution, Volume 13 (1998) no. 10, pp. 403-407 | DOI

[50] Panchanathan, K.; Frankenhuis, W. E. The evolution of sensitive periods in a model of incremental development, Proceedings of the Royal Society B: Biological Sciences, Volume 283 (2016) no. 1823 | DOI

[51] Pigliucci, M. Phenotypic Plasticity: Beyond Nature and Nurture, JHU Press, 2001

[52] Price, T. D.; Qvarnström, A.; Irwin, D. E. The role of phenotypic plasticity in driving genetic evolution, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 270 (2003) no. 1523, pp. 1433-1440 | DOI

[53] Pujol, B. Sensitive windows for phenotypic plasticity within and across generations; where empirical results do not meet the theory but open a world of possibilities, Peer Community in Evolutionary Biology (2023) | DOI

[54] R Development Core Team R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Boston, MA, 2022

[55] Radersma, R.; Hegg, A.; Noble, D. W. A.; Uller, T. Timing of maternal exposure to toxic cyanobacteria and offspring fitness in Daphnia magna : Implications for the evolution of anticipatory maternal effects, Ecology and Evolution, Volume 8 (2018) no. 24, pp. 12727-12736 | DOI

[56] Relyea, R. A. Predators come and predators go: The reversibility of predator-induced traits, Ecology, Volume 84 (2003) no. 7, pp. 1840-1848 | DOI

[57] RStudio Team RStudio: Integrated Development Environment for R, RStudio, 2022

[58] Rundle, S. D.; Brönmark, C. Inter– and intraspecific trait compensation of defence mechanisms in freshwater snails, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 268 (2001) no. 1475, pp. 1463-1468 | DOI

[59] Salice, C. J.; Plautz, S. C. Predator-Induced Defences in Offspring of Laboratory and Wild-Caught Snails: Prey History Impacts Prey Response, Evolutionary Ecology Research, Volume 13 (2011) no. 4, pp. 373-386

[60] Snell-Rood, E. C.; Swanson, E. M.; Young, R. L. Life history as a constraint on plasticity: developmental timing is correlated with phenotypic variation in birds, Heredity, Volume 115 (2015) no. 4, pp. 379-388 | DOI

[61] Stamps, J. A.; Krishnan, V. V. Combining Information from Ancestors and Personal Experiences to Predict Individual Differences in Developmental Trajectories, The American Naturalist, Volume 184 (2014) no. 5, pp. 647-657 | DOI

[62] Stamps, J. A.; Krishnan, V. Age-dependent changes in behavioural plasticity: insights from Bayesian models of development, Animal Behaviour, Volume 126 (2017), pp. 53-67 | DOI

[63] Stamps, J. A.; Luttbeg, B. Sensitive Period Diversity: Insights From Evolutionary Models, The Quarterly Review of Biology, Volume 97 (2022) no. 4, pp. 243-295 | DOI

[64] Stein, L. R.; Bukhari, S. A.; Bell, A. M. Personal and transgenerational cues are nonadditive at the phenotypic and molecular level, Nature Ecology & Evolution, Volume 2 (2018) no. 8, pp. 1306-1311 | DOI

[65] Steiner, U. K.; Van Buskirk, J. Environmental stress and the costs of whole-organism phenotypic plasticity in tadpoles, Journal of Evolutionary Biology, Volume 21 (2007) no. 1, pp. 97-103 | DOI

[66] Stevison, B.; Kensinger, B.; Luttbeg, B. Different morphological traits influence predator defense and space use in Physa acuta, American Malacological Bulletin, Volume 34 (2016) no. 2, pp. 79-84 | DOI

[67] Tariel, J.; Luquet, É.; Plénet, S. Interactions Between Maternal, Paternal, Developmental, and Immediate Environmental Effects on Anti-predator Behavior of the Snail Physa acuta, Frontiers in Ecology and Evolution, Volume 8 (2020) | DOI

[68] Tariel, J.; Plénet, S.; Luquet, É. Transgenerational Plasticity in the Context of Predator-Prey Interactions, Frontiers in Ecology and Evolution, Volume 8 (2020) | DOI

[69] Tariel, J.; Plénet, S.; Luquet, É. Transgenerational plasticity of inducible defences: Combined effects of grand‐parental, parental and current environments, Ecology and Evolution, Volume 10 (2020) no. 5, pp. 2367-2376 | DOI

[70] Tollrian, R.; Harvell, C. The Ecology and Evolution of Inducible Defenses, Princeton University Press, Princeton, New Jersey, 1999

[71] Turner, A. M.; Fetterolf, S. A.; Bernot, R. J. Predator identity and consumer behavior: differential effects of fish and crayfish on the habitat use of a freshwater snail, Oecologia, Volume 118 (1999) no. 2, pp. 242-247 | DOI

[72] Walasek, N.; Frankenhuis, W. E.; Panchanathan, K. An evolutionary model of sensitive periods when the reliability of cues varies across ontogeny, Behavioral Ecology, Volume 33 (2021) no. 1, pp. 101-114 | DOI

[73] Weiss, L. C.; Heilgenberg, E.; Deussen, L.; Becker, S. M.; Kruppert, S.; Tollrian, R. Onset of kairomone sensitivity and the development of inducible morphological defenses in Daphnia pulex, Hydrobiologia, Volume 779 (2016) no. 1, pp. 135-145 | DOI

[74] Wickham, H. Ggplot2: Elegant Graphics for Data Analysis, Springer, Verlag New York

[75] Wickham, H.; François, R.; Henry, L.; Müller, K. Dplyr: A Grammar of Data Manipulation

[76] Yin, J.; Zhou, M.; Lin, Z.; Li, Q. Q.; Zhang, Y. Transgenerational effects benefit offspring across diverse environments: a meta‐analysis in plants and animals, Ecology Letters, Volume 22 (2019) no. 11, pp. 1976-1986 | DOI

[77] Zhang, Y.; Yin, J.; Zhou, M.; Lin, Z.; Li, Q. Q. Adaptive transgenerational effects remain significant, Ecology Letters, Volume 23 (2020) no. 11, pp. 1719-1720 | DOI

Cited by Sources: