Sex‐specific plasticity across generations II: Grandpaternal effects are lineage specific and sex specific

Abstract

1. Transgenerational plasticity (TGP) occurs when the environment encountered by one generation (F0) alters the phenotypes of one or more future generations (e.g. F1 and F2). Sex selective TGP, via specific lineages or to only male or female descendants, has been underexplored in natural systems, and may be adaptive if it allows past generations to fine-tune the phenotypes of future generations in response to sex-specific life-history strategies. 2. We sought to understand if exposing males to predation risk can influence grandoffspring via sperm in three-spined stickleback Gasterosteus aculeatus. We specifically tested the hypothesis that grandparental effects are transmitted in a sex-specific way down the male lineage, from paternal grandfathers to F2 males. 3. We reared F1 offspring of unexposed and predator-exposed F0 males under 'control' conditions and used them to generate F2s with control grandfathers, a predator-exposed maternal grandfather (i.e. predator-exposed F0 males to F1 daughters to F2s), a predator-exposed paternal grandfather (i.e. predator-exposed F0 males to F1 sons to F2s) or two predator-exposed grandfathers. We then assayed male and female F2s for a variety of traits related to antipredator defence. 4. We found little evidence that transgenerational effects were mediated to only male descendants via the paternal lineage. Instead, grandpaternal effects depended on lineage and were mediated largely across sexes, from F1 males to F2 females and from F1 females to F2 males. When their paternal grandfather was exposed to predation risk, female F2s were heavier and showed a reduced change in behaviour in response to a simulated predator attack relative to grandoffspring of control, unexposed grandparents. In contrast, male F2s showed reduced antipredator behaviour when their maternal grandfather was exposed to predation risk. However, these patterns were only evident when one grandfather, but not both grandfathers, was exposed to predation risk, suggesting the potential for non-additive interactions across lineages. 5. If sex-specific and lineage effects are common, then grandparental effects are likely underestimated in the literature. These results draw attention to the importance of sex-selective inheritance of environmental effects and raise new questions about the proximate and ultimate causes of selective transmission across generations.

Sex‐specific plasticity across generations I: Maternal and paternal effects on sons and daughters

“…Consequently, theoretical and empirical work seeking to understand the evolution of transgenerational plasticity would benefit from considering the conditions which influence sex‐specific patterns of transgenerational plasticity in both adaptive and non‐adaptive ways. Furthermore, given broad interest in understanding the consequences of transgenerational plasticity for future generations and its potential to influence adaptive evolution, future work should consider how sex‐specific effects in the first generation may alter the ways in which intergenerational effects persist for multiple generations in lineage‐specific and/or sex‐specific ways (Hellmann, Carlson, & Bell, 2020).…”

Sex-specific transgenerational effects of diet on offspring life history and physiology

“…Studies investigating sex-specificity of transgenerational effects across a range of taxa have observed instances in which environmental modification such as dietary challenges, presence of predators, or behaviour-modifying drugs of the grandparental environment triggered sex-specific effects on grandoffspring phenotype. Intriguingly, in these cases, transgenerational effects tend to manifest in the opposite sex to that subjected to the grandparental treatment; that is, modification of the grandmaternal environment may enhance or inhibit trait expression among grandsons, or conversely, modification to the grandpaternal environment may enhance or inhibit trait expression among granddaughters 10,25,30,32,33 . Our findings are consistent with previous research, revealing opposing directions of sucrose-mediated grandmaternal effects in each of the sexes.…”

“…predation risk and levels of sexual conflict, among parents may catalyse transgenerational effects that differ in magnitude or direction across sexes, and which may also be lineage (genotype) specific 10 . Notwithstanding, currently it remains unclear whether such transgenerational effects are consistently instigated across diverse environmental stresses, whether they generally act to enhance or depress offspring performance, and whether they are transferred primarily through maternal or paternal lineages or hinge on interactions between both.…”

Paternal exposure to a common pharmaceutical (Ritalin) has transgenerational effects on the behaviour of Trinidadian guppies

“…While MPH treatment caused a significant effect in G 1 males but not G 1 females, this sex-specific effect was reversed in their progeny for one behavioural metric (CA1), with only female offspring and great-grandoffspring differing in behaviour based on their father’s/great-grandfather’s treatment. Other studies have observed transgenerational effects expressed in the sex opposite to the one originally affected by an environmental stimulus 33 – 37 . This result further emphasizes the importance of studying transgenerational effects in both sexes.…”

“…First, many of these studies do not report potentially confounding effects of differences in survival or reproductive success between control and treatment lines. Second, some studies only investigate the effects in progeny of one sex, despite evidence that parental effects are sometimes sex-specific 33 – 37 . Third, most examples come from rodents (but see 5 , 14 , 27 , 37 ), which makes it unclear if these results can be generalized to other taxa.…”