TY - JOUR
T1 - Sex-specific plasticity across generations I
T2 - Maternal and paternal effects on sons and daughters
AU - Hellmann, Jennifer K.
AU - Bukhari, Syed Abbas
AU - Deno, Jack
AU - Bell, Alison M.
N1 - Funding Information:
Thank you to Eunice Chen, Erin Hsiao, Yangxue Ma, Liam Masse and Christian Zielinksi for help with data collection and to Sarah Donelan and the Bell lab for comments on previous versions of this manuscript. This work was supported by the National Institutes of Health award number 2R01GM082937‐06A1 to A.M.B. and National Institutes of Health NRSA Fellowship F32GM121033 to J.K.H. The authors have no conflicts of interest.
Publisher Copyright:
© 2020 British Ecological Society
PY - 2020/12
Y1 - 2020/12
N2 - Intergenerational plasticity or parental effects—when parental environments alter the phenotype of future generations—can influence how organisms cope with environmental change. An intriguing, underexplored possibility is that sex—of both the parent and the offspring—plays an important role in driving the evolution of intergenerational plasticity in both adaptive and non-adaptive ways. Here, we evaluate the potential for sex-specific parental effects in a freshwater population of three-spined sticklebacks Gasterosteus aculeatus by independently and jointly manipulating maternal and paternal experiences and separately evaluating their phenotypic effects in sons versus daughters. We tested the adaptive hypothesis that daughters are more responsive to cues from their mother, whereas sons are more responsive to cues from their father. We exposed mothers, fathers or both parents to visual cues of predation risk and measured offspring antipredator traits and brain gene expression. Predator-exposed fathers produced sons that were more risk-prone, whereas predator-exposed mothers produced more anxious sons and daughters. Furthermore, maternal and paternal effects on offspring survival were non-additive: offspring with a predator-exposed father, but not two predator-exposed parents, had lower survival against live predators. There were also strong sex-specific effects on brain gene expression: exposing mothers versus fathers to predation risk activated different transcriptional profiles in their offspring, and sons and daughters strongly differed in the ways in which their brain gene expression profiles were influenced by parental experience. We found little evidence to support the hypothesis that offspring prioritize their same-sex parent's experience. Parental effects varied with both the sex of the parent and the offspring in complicated and non-additive ways. Failing to account for these sex-specific patterns (e.g. by pooling sons and daughters) would have underestimated the magnitude of parental effects. Altogether, these results draw attention to the potential for sex to influence patterns of intergenerational plasticity and raise new questions about the interface between intergenerational plasticity and sex-specific selective pressures, sexual conflict and sexual selection.
AB - Intergenerational plasticity or parental effects—when parental environments alter the phenotype of future generations—can influence how organisms cope with environmental change. An intriguing, underexplored possibility is that sex—of both the parent and the offspring—plays an important role in driving the evolution of intergenerational plasticity in both adaptive and non-adaptive ways. Here, we evaluate the potential for sex-specific parental effects in a freshwater population of three-spined sticklebacks Gasterosteus aculeatus by independently and jointly manipulating maternal and paternal experiences and separately evaluating their phenotypic effects in sons versus daughters. We tested the adaptive hypothesis that daughters are more responsive to cues from their mother, whereas sons are more responsive to cues from their father. We exposed mothers, fathers or both parents to visual cues of predation risk and measured offspring antipredator traits and brain gene expression. Predator-exposed fathers produced sons that were more risk-prone, whereas predator-exposed mothers produced more anxious sons and daughters. Furthermore, maternal and paternal effects on offspring survival were non-additive: offspring with a predator-exposed father, but not two predator-exposed parents, had lower survival against live predators. There were also strong sex-specific effects on brain gene expression: exposing mothers versus fathers to predation risk activated different transcriptional profiles in their offspring, and sons and daughters strongly differed in the ways in which their brain gene expression profiles were influenced by parental experience. We found little evidence to support the hypothesis that offspring prioritize their same-sex parent's experience. Parental effects varied with both the sex of the parent and the offspring in complicated and non-additive ways. Failing to account for these sex-specific patterns (e.g. by pooling sons and daughters) would have underestimated the magnitude of parental effects. Altogether, these results draw attention to the potential for sex to influence patterns of intergenerational plasticity and raise new questions about the interface between intergenerational plasticity and sex-specific selective pressures, sexual conflict and sexual selection.
KW - Gasterosteus aculeatus
KW - intergenerational plasticity
KW - maternal effect
KW - non-genetic inheritance
KW - phenotypic plasticity
KW - predation
KW - stress
KW - transgenerational plasticity
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UR - http://www.scopus.com/inward/citedby.url?scp=85096701824&partnerID=8YFLogxK
U2 - 10.1111/1365-2656.13364
DO - 10.1111/1365-2656.13364
M3 - Article
C2 - 33191518
AN - SCOPUS:85096701824
SN - 0021-8790
VL - 89
SP - 2788
EP - 2799
JO - Journal of Animal Ecology
JF - Journal of Animal Ecology
IS - 12
ER -