Predator-induced transgenerational plasticity of parental care behaviour in male three-spined stickleback fish across two generations

Abstract

Parental care is a critical determinant of offspring fitness, and parents adjust their care in response to ecological challenges, including predation risk. The experiences of both mothers and fathers can influence phenotypes of future generations (transgenerational plasticity). If it is adaptive for parents to alter parental care in response to predation risk, then we expect F₁ and F₂ offspring who receive transgenerational cues of predation risk to shift their parental care behaviour if these ancestral cues reliably predict a similarly risky environment as their F₀ parents. Here, we used three-spined sticklebacks (Gasterosteus aculeatus) to understand how paternal exposure to predation risk prior to mating alters reproductive traits and parental care behaviour in unexposed F₁ sons and F₂ grandsons. Sons of predator-exposed fathers took more attempts to mate than sons of control fathers. F₁ sons and F₂ grandsons with two (maternal and paternal) predator-exposed grandfathers shifted their paternal care (fanning) behaviour in strikingly similar ways: they fanned less initially, but fanned more near egg hatching. This shift in fanning behaviour matches shifts observed in response to direct exposure to predation risk, suggesting a highly conserved response to pre-fertilization predator exposure that persists from the F₀ to the F₁ and F₂ generations.

Keywords: Gasterosteus aculeatus; epigenetics; paternal care; paternal effect; plasticity; transgenerational plasticity.

Figure 1.

Overview. The pedigrees track the pattern of predation exposure in parents or grandparents of all treatment groups (1–6). Squares indicate males and circles indicate females. There were two treatment groups for sons: (1) males whose fathers had not been exposed to predators or (2) males whose fathers had been exposed to predators prior to fertilization. There were four treatment groups for grandsons: (3) neither grandfather exposed, (4) maternal grandfather exposed, (5) paternal grandfather exposed, and (6) both grandfathers exposed. Shading represents generational time since the initial experiment involving predator exposure, i.e. most dark for experienced by the individual and most light for experienced by the grandfather(s). Black signifies control and orange signifies predation exposure. The outline of the sons and grandsons corresponds to the colours used in the data figures.

Figure 2.

Transgenerational effects of predator exposure on fanning. Fish with predator-exposed fathers (b) start out with less fanning (indicated by the marginal treatment term and the significant and negative treatment × day² term) but then have a steeper increase in fanning and end up with a peak that is higher (indicated by the significant and positive treatment × day term). This is a similar shift in care that is found in directly exposed F₀ males (a; figure produced from data from Hellmann et al. [30]). F₂ males (c) with two predator-exposed grandfathers (pale blue) had different fanning curves than those with two control grandfathers (grey); their fanning curves were very similar to that of fish with predator-exposed fathers and directly predator-exposed males. Fish with just one predator-exposed grandfather did not differ from those with two control grandfathers. Mean ± s.e. plotted for each day, curves are those predicted by the linear model, averaged for each treatment.