The transgenerational consequences of paternal social isolation and predation exposure in threespined sticklebacks.

Gasterosteus aculeatus intergenerational paternal effects phenotypic plasticity predation risk social buffering stress

Journal

The Journal of animal ecology

ISSN: 1365-2656

Titre abrégé: J Anim Ecol

Pays: England

ID NLM: 0376574

Informations de publication

Date de publication:
25 Jul 2024

Historique:

received: 30 12 2023

accepted: 22 04 2024

medline: 26 7 2024

pubmed: 26 7 2024

entrez: 25 7 2024

Statut: aheadofprint

Résumé

Parents routinely encounter stress in the ecological environment that can affect offspring development (transgenerational plasticity: TGP); however, parents' interactions with conspecifics may alter how parents respond to ecological stressors. During social buffering, the presence of conspecifics can reduce the response to or increase the speed of recovery from a stressor. This may have cascading effects on offspring if conspecifics can mitigate parental responses to ecological stress in ways that blunt the transmission of stress-induced transgenerational effects. Here, we simultaneously manipulated both paternal social isolation and experience with predation risk prior to fertilisation in threespined stickleback (Gasterosteus aculeatus). We generated offspring via in-vitro fertilisation to allow us to isolate paternal effects mediated via sperm alone (i.e. in the absence of paternal care). If social buffering mitigates TGP induced by paternal exposure to predation risk, then we expect the transgenerational effects of predation exposure to be weaker when a conspecific is present compared to when the father is isolated. Offspring of predator-exposed fathers showed reduced anxiety-like behaviour and tended to be captured faster by the predator. Fathers who were socially isolated also had offspring that were captured faster by a live predator, suggesting that paternal social isolation may have maladaptive effects on how offspring respond to ecological stressors. Despite additive effects of paternal social isolation and paternal predation risk, we found no evidence of an interaction between these paternal treatments, suggesting that the presence of a conspecific did not buffer fathers and/or offspring from the effects of predation risk. Our results suggest that socially induced stress is an important, yet underappreciated, mediator of TGP and can elicit transgenerational effects even in species that do not form permanent social groups. Future studies should therefore consider how the parental social environment can affect both within and trans-generational responses to ecological stressors.

Identifiants

DOI: 10.1111/1365-2656.14151 PMID: 39049666

pubmed: 39049666

doi: 10.1111/1365-2656.14151

doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

Informations de copyright

Références

Afseth, C., Shim, A., Anderson, S., Bell, A., & Hellmann, J. K. (2022). Vertical transmission of horizontally‐acquired social information in sticklebacks: Implications for transgenerational plasticity. Proceedings of the Royal Society B: Biological Sciences, 289, 20220571.

Akkerman, K. C., Sattarin, A., Kelly, J. K., & Scoville, A. G. (2016). Transgenerational plasticity is sex‐dependent and persistent in yellow monkeyflower (Mimulus guttatus). Environmental Epigenetics, 2, dvw003.

Bartolomucci, A., Palanza, P., Sacerdote, P., Ceresini, G., Chirieleison, A., Panerai, A. E., & Parmigiani, S. (2003). Individual housing induces altered immuno‐endocrine responses to psychological stress in male mice. Psychoneuroendocrinology, 28, 540–558.

Batchelor, V., & Pang, T. Y. (2019). HPA axis regulation and stress response is subject to intergenerational modification by paternal trauma and stress. General and Comparative Endocrinology, 280, 47–53.

Beemelmanns, A., & Roth, O. (2016). Biparental immune priming in the pipefish Syngnathus typhle. Zoology, 119, 262–272.

Bell, A. M., & Hellmann, J. K. (2019). An integrative framework for understanding the mechanisms and multigenerational consequences of transgenerational plasticity. Annual Review of Ecology, Evolution, and Systematics, 50, 97–118.

Ben‐Shachar, M. S., Lüdecke, D., & Makowski, D. (2020). effectsize: Estimation of effect size indices and standardized parameters. Journal of Open Software, 5, 2815.

Bonduriansky, R., & Head, M. (2007). Maternal and paternal condition effects on offspring phenotype in Telostylinus angusticollis (Diptera: Neriidae). Journal of Evolutionary Biology, 20, 2379–2388.

Bonduriansky, R., Runagall‐McNaull, A., & Crean, A. J. (2016). The nutritional geometry of parental effects: Maternal and paternal macronutrient consumption and offspring phenotype in a neriid fly. Functional Ecology, 30, 1675–1686.

Bouwhuis, S., Vedder, O., & Becker, P. H. (2015). Sex‐specific pathways of parental age effects on offspring lifetime reproductive success in a long‐lived seabird. Evolution, 69, 1760–1771.

Brandl, H. B., Pruessner, J. C., & Farine, D. R. (2022). The social transmission of stress in animal collectives. Proceedings of the Royal Society B: Biological Sciences, 289, 20212158.

Brass, K. E., Herndon, N., Gardner, S. A., Grindstaff, J. L., & Campbell, P. (2020). Intergenerational effects of paternal predator cue exposure on behavior, stress reactivity, and neural gene expression. Hormones and Behavior, 124, 104806.

Bygren, L. O., Tinghög, P., Carstensen, J., Edvinsson, S., Kaati, G., Pembrey, M. E., & Sjöström, M. (2014). Change in paternal grandmothers' early food supply influenced cardiovascular mortality of the female grandchildren. BMC Genetics, 15, 12.

Chen, E., Zielinski, C., Deno, J., Singh, R., Bell, A. M., & Hellmann, J. K. (2021). The specificity of sperm‐mediated paternal effects in threespine sticklebacks. Behavioral Ecology and Sociobiology, 75, 68.

Cockrem, J. F. (2013). Individual variation in glucocorticoid stress responses in animals. General and Comparative Endocrinology, 181, 45–58.

Crane, A. L., & Ferrari, M. C. O. (2015). Minnows trust conspecifics more than themselves when faced with conflicting information about predation risk. Animal Behaviour, 100, 184–190.

Culbert, B. M., Gilmour, K. M., & Balshine, S. (2019). Social buffering of stress in a group‐living fish. Proceedings of the Royal Society B: Biological Sciences, 286, 20191626.

da Costa, A. P., Leigh, A. E., Man, M.‐S., & Kendrick, K. M. (2004). Face pictures reduce behavioural, autonomic, endocrine and neural indices of stress and fear in sheep. Proceedings of the Royal Society B: Biological Sciences, 271, 2077–2084.

Dellinger, M., Zhang, W., Bell, A. M., & Hellmann, J. K. (2018). Do male sticklebacks use visual and/or olfactory cues to assess a potential mate's history with predation risk? Animal Behaviour, 145, 151–159.

DeVries, A. C., Glasper, E. R., & Detillion, C. E. (2003). Social modulation of stress responses. Physiology & Behavior, 79, 399–407.

Dietz, D. M., LaPlant, Q., Watts, E. L., Hodes, G. E., Russo, S. J., Feng, J., Oosting, R. S., Vialou, V., & Nestler, E. J. (2011). Paternal transmission of stress‐induced pathologies. Biological Psychiatry, 70, 408–414.

Donelson, J. M., Wong, M., Booth, D. J., & Munday, P. L. (2016). Transgenerational plasticity of reproduction depends on rate of warming across generations. Evolutionary Applications, 9, 1072–1081.

Dronjak, S., Gavrilović, L., Filipović, D., & Radojčić, M. B. (2004). Immobilization and cold stress affect sympatho–adrenomedullary system and pituitary–adrenocortical axis of rats exposed to long‐term isolation and crowding. Physiology & Behavior, 81, 409–415.

Faraji, J., Soltanpour, N., Lotfi, H., Moeeini, R., Moharreri, A.‐R., Roudaki, S., Hosseini, S. A., Olson, D. M., Abdollahi, A.‐A., Soltanpour, N., Mohajerani, M. H., & Metz, G. A. S. (2017). Lack of social support raises stress vulnerability in rats with a history of ancestral stress. Scientific Reports, 7, 5277.

Faustino, A. I., Tacão‐Monteiro, A., & Oliveira, R. F. (2017). Mechanisms of social buffering of fear in zebrafish. Scientific Reports, 7, 44329.

Fisher, D. N., Haines, J. A., Boutin, S., Dantzer, B., Lane, J. E., Coltman, D. W., & McAdam, A. G. (2019). Indirect effects on fitness between individuals that have never met via an extended phenotype. Ecology Letters, 22, 697–706.

Fisher, D. N., & McAdam, A. G. (2017). Social traits, social networks and evolutionary biology. Journal of Evolutionary Biology, 30, 2088–2103.

Friard, O., & Gamba, M. (2016). BORIS: A free, versatile open‐source event‐logging software for video/audio coding and live observations. Methods in Ecology and Evolution, 7, 1325–1330.

Fürtbauer, I., & Heistermann, M. (2016). Cortisol coregulation in fish. Scientific Reports, 6, 30334.

Gapp, K., Jawaid, A., Sarkies, P., Bohacek, J., Pelczar, P., Prados, J., Farinelli, L., Miska, E., & Mansuy, I. M. (2014). Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nature Neuroscience, 17, 667–669.

Gilad, T., & Scharf, I. (2019). Separation between maternal and paternal effects on offspring following exposure of adult red flour beetles to two stressors. Ecological Entomology, 44, 494–501.

Gilmour, K. M., & Bard, B. (2022). Social buffering of the stress response: Insights from fishes. Biology Letters, 18, 20220332.

Hagmayer, A., Lankheet, M. J., Bijsterbosch, J., van Leeuwen, J. L., & Pollux, B. J. A. (2022). Maternal food restriction during pregnancy affects offspring development and swimming performance in a placental live‐bearing fish. Journal of Experimental Biology, 225, jeb242850.

He, N., Kong, Q.‐Q., Wang, J.‐Z., Ning, S.‐F., Miao, Y.‐L., Yuan, H.‐J., Gong, S., Cui, X.‐Z., Li, C.‐Y., & Tan, J.‐H. (2016). Parental life events cause behavioral difference among offspring: Adult pre‐gestational restraint stress reduces anxiety across generations. Scientific Reports, 6, 39497.

Hellmann, J. K., Bukhari, S. A., Deno, J., & Bell, A. M. (2020). Sex‐specific plasticity across generations I: Maternal and paternal effects on sons and daughters. Journal of Animal Ecology, 89, 2788–2799.

Hellmann, J. K., Carlson, E. R., & Bell, A. M. (2020). Sex‐specific plasticity across generations II: Grandpaternal effects are lineage‐ and sex‐specific. Journal of Animal Ecology, 89, 2800–2812.

Hellmann, J. K., Carlson, E. R., & Bell, A. M. (2021). The interplay between sperm‐mediated and care‐mediated paternal effects in threespined sticklebacks. Animal Behaviour, 179, 267–277.

Hellmann, J. K., Keagy, J., Carlson, E. R., Kempfer, S., & Bell, A. M. (2024). Predator‐induced transgenerational plasticity of parental care behaviour in male three‐spined stickleback fish across two generations. Proceedings of the Royal Society B: Biological Sciences, 291, 20232582.

Hellmann, J. K., & Rogers, M. R. (2024). Data from: The transgenerational consequences of paternal social isolation and predation exposure in threespined sticklebacks. bioRxiv, https://doi.org/10.1101/2024.01.16.575739

Hennessy, M. B., Kaiser, S., & Sachser, N. (2009). Social buffering of the stress response: Diversity, mechanisms, and functions. Frontiers in Neuroendocrinology, 30, 470–482.

Immler, S. (2018). The sperm factor: Paternal impact beyond genes. Heredity, 121, 239–247.

Kassambara, A., & Mundt, M. (2017). factoextra: Extract and visualize the results of multivariate data analyses. R package version 1.0.5. https://CRAN.R‐project.org/package=factoextra

Kikusui, T., Winslow, J. T., & Mori, Y. (2006). Social buffering: Relief from stress and anxiety. Philosophical Transactions of the Royal Society B, 361, 2215–2228.

Kiyokawa, Y., Kikusui, T., Takeuchi, Y., & Mori, Y. (2004). Partner's stress status influences social buffering effects in rats. Behavioral Neurosceince, 118, 798–804.

Kong, Q.‐Q., Tian, X.‐D., Wang, J., Yuan, H.‐J., Ning, S.‐F., Luo, M.‐J., & Tan, J.‐H. (2021). A next‐generation sequencing study on mechanisms by which restraint and social instability stresses of male mice alter offspring anxiety‐like behavior. Scientific Reports, 11, 7952.

Koolhaas, J. M., Korte, S. M., De Boer, S. F., Van Der Vegt, B. J., Van Reenen, C. G., Hopster, H., De Jong, I. C., Ruis, M. A. W., & Blokhuis, H. J. (1999). Coping styles in animals: Current status in behavior and stress‐physiology. Neuroscience & Biobehavioral Reviews, 23, 925–935.

Ludwig, S. C., Kapetanopoulos, K., Kotrschal, K., & Wascher, C. A. F. (2017). Effects of mate separation in female and social isolation in male free‐living Greylag geese on behavioural and physiological measures. Behavioural Processes, 138, 134–141.

MacLeod, K. J., English, S., Ruuskanen, S. K., & Taborsky, B. (2023). Stress in the social context: A behavioural and eco‐evolutionary perspective. Journal of Experimental Biology, 226, jeb245829.

MacLeod, K. J., Monestier, C., Ferrari, M. C. O., McGhee, K. E., Sheriff, M. J., & Bell, A. M. (2022). Predator‐induced transgenerational plasticity in animals: A meta‐analysis. Oecologia, 200, 371–383.

Mashoodh, R., Franks, B., Curley, J. P., & Champagne, F. A. (2012). Paternal social enrichment effects on maternal behavior and offspring growth. Proceedings of the National Academy of Sciences, 109, 17232–17238.

Maximino, C., Marques de Brito, T., Dias, C. A. G.d. M., Gouveia, A., Jr., & Morato, S. (2010). Scototaxis as anxiety‐like behavior in fish. Nature Protocols, 5, 209–216.

McDonald, R. J., Hong, N. S., Trow, J. S., Kaupp, C., Balog, R. J., Gokarn, L., Falkenberg, E. A., McCreary, K. J., Soltanpour, N., Witbeck, C., McKenna, A., & Metz, G. A. S. (2023). Effects of maternal social isolation on adult rodent offspring cognition. Scientific Reports, 13, 7748.

McGhee, K. E., Feng, S., Leasure, S., & Bell, A. M. (2015). A female's past experience with predators affects male courtship and the care her offspring will receive from their father. Proceedings of the Royal Society B: Biological Sciences, 282, 20151840.

McQuaid, R. J., McInnis, O. A., Paric, A., Al‐Yawer, F., Matheson, K., & Anisman, H. (2016). Relations between plasma oxytocin and cortisol: The stress buffering role of social support. Neurobiology of Stress, 3, 52–60.

Mommer, B. C., & Bell, A. M. (2013). A test of maternal programming of offspring stress response to predation risk in threespine sticklebacks. Physiology and Behavior, 122, 222–227.

Moore, R. S., Kaletsky, R., & Murphy, C. T. (2019). Piwi/PRG‐1 argonaute and TGF‐α mediate transgenerational learned pathogenic avoidance. Cell, 177, 1827–1841.e1812.

Nylen, K. J., O'Hara, M. W., & Engeldinger, J. (2013). Perceived social support interacts with prenatal depression to predict birth outcomes. Journal of Behavioral Medicine, 36, 427–440.

Ozbay, F., Johnson, D. C., Dimoulas, E., Morgan, C. A., Charney, D., & Southwick, S. (2007). Social support and resilience to stress: From neurobiology to clinical practice. Psychiatry (Edgmont), 4, 35–40.

Pessato, A., McKechnie, A. E., & Mariette, M. M. (2022). A prenatal acoustic signal of heat affects thermoregulation capacities at adulthood in an arid‐adapted bird. Scientific Reports, 12, 5842.

Potticary, A. L., & Duckworth, R. A. (2020). Multiple environmental stressors induce an adaptive maternal effect. The American Naturalist, 196, 487–500.

Rodgers, A. B., Morgan, C. P., Bronson, S. L., Revello, S., & Bale, T. L. (2013). Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. Journal of Neuroscience, 33, 9003–9012.

Romero, L. M., Dickens, M. J., & Cyr, N. E. (2009). The reactive scope model—A new model integrating homeostasis, allostasis, and stress. Hormones and Behavior, 55, 375–389.

Sanchez, M. M., McCormack, K. M., & Howell, B. R. (2015). Social buffering of stress responses in nonhuman primates: Maternal regulation of the development of emotional regulatory brain circuits. Social Neuroscience, 10, 512–526.

Schumann, S., Mozzi, G., Piva, E., Devigili, A., Negrato, E., Marion, A., Bertotto, D., & Santovito, G. (2023). Social buffering of oxidative stress and cortisol in an endemic cyprinid fish. Scientific Reports, 13, 20579.

Sheriff, M. J., Krebs, C. J., & Boonstra, R. (2010). The ghosts of predators past: Population cycles and the role of maternal programming under fluctuating predation risk. Ecology, 91, 2983–2994.

Stanton, M. E., Patterson, J. M., & Levine, S. (1985). Social influences on conditioned cortisol secretion in the squirrel monkey. Psychoneuroendocrinology, 10, 125–134.

Stein, L. R., & Bell, A. M. (2014). Paternal programming in sticklebacks. Animal Behaviour, 95, 165–171.

Tariel, J., Plénet, S., & Luquet, É. (2020). Transgenerational plasticity in the context of predator‐prey interactions. Frontiers in Ecology and Evolution, 8, 319.

Walsh, K., McCormack, C. A., Webster, R., Pinto, A., Lee, S., Feng, T., Krakovsky, H. S., O'Grady, S. M., Tycko, B., Champagne, F. A., Werner, E. A., Liu, G., & Monk, C. (2019). Maternal prenatal stress phenotypes associate with fetal neurodevelopment and birth outcomes. Proceedings of the National Academy of Sciences, 116, 23996–24005.

Yehuda, R., Bell, A., Bierer, L. M., & Schmeidler, J. (2008). Maternal, not paternal, PTSD is related to increased risk for PTSD in offspring of holocaust survivors. Journal of Psychiatric Research, 42, 1104–1111.

Yusishen, M. E., Yoon, G. R., Bugg, W., Jeffries, K. M., Currie, S., & Anderson, W. G. (2020). Love thy neighbor: Social buffering following exposure to an acute thermal stressor in a gregarious fish, the lake sturgeon (Acipenser fulvescens). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 243, 110686.