Personal and transgenerational cues are nonadditive at the phenotypic and molecular level

Abstract

Organisms can gain information about their environment from their ancestors, their parents or their own personal experience. 'Cue integration' models often start with the simplifying assumption that information from different sources is additive. Here, we test key assumptions and predictions of cue integration theory at both the phenotypic and molecular level in threespined sticklebacks (Gasterosteus aculeatus). We show that regardless of whether cues about predation risk were provided by their father or acquired through personal experience, sticklebacks produced the same set of predator-adapted phenotypes. Moreover, there were nonadditive effects of personal and paternal experience: animals that received cues from both sources resembled animals that received cues from a single source. A similar pattern was detected at the molecular level: there was a core set of genes that were differentially expressed in the brains of offspring regardless of whether risk was experienced by their father, themselves or both. These results provide strong support for cue integration theory because they show that cues provided by parents and personal experience are comparable at both the phenotypic and molecular level, and draw attention to the importance of nonadditive responses to multiple cues.

The role of variation and plasticity in parental care during the adaptive radiation of three‐spine sticklebacks

“…Another intriguing possibility is that the reduction in fanning might provide a cue to offspring about predation risk in their environment, resulting in offspring with predator‐adapted phenotypes (Stein & Bell ; Stein et al. ). If sons learn from their fathers, then their male offspring will also reduce fanning.…”

“…Alternatively, if the variation among reaction norms results from nongenetic mechanisms, then when marine males move into freshwater, those males that reduce fanning in response to dragonfly naiad could have higher fitness in freshwater because males spend more time guarding their nests (Stein & Bell 2015), resulting in higher survival rates of offspring. Another intriguing possibility is that the reduction in fanning might provide a cue to offspring about predation risk in their environment, resulting in offspring with predator-adapted phenotypes (Stein & Bell 2014;Stein et al 2018). If sons learn from their fathers, then their male offspring will also reduce fanning.…”

The effects of embryonic experience with predation risk vary across a wave exposure gradient

“…, Stein et al. ), to inform their response to risk in heterogeneous environments. The embryonic phase of life can be particularly sensitive to environmental cues, including those from predators, which may influence an individual's current and future phenotype (Dufty et al.…”

“…In systems where predation risk is particularly variable, prey assess their risk of predation through immediate, direct experience with predator cues (Lima andDill 1990, Kats andDill 1998). However, prey are also likely to rely on their historical experiences with predators, whether their own or those of their parents or grandparents (Sheriff et al 2010, Stein et al 2018, to inform their response to risk in heterogeneous environments. The embryonic phase of life can be particularly sensitive to environmental cues, including those from predators, which may influence an individual's current and future phenotype (Dufty et al 2002, English et al 2016.…”

Naturally clonal vertebrates are an untapped resource in ecology and evolution research

“…Recent work has shown the potential of these theoretical-conceptual models in explaining and predicting development in labile traits. Stein and colleagues used threespined sticklebacks, Gasterosteus aculeatus, to manipulate two sources of cues: parental and personal experience with predator cues 56 . They found that sticklebacks adjust their behavior and gene expression in response to these cues non-additively with the presentation of cues as either parental or personal information generating similar phenotypic responses in the offspring 56 .…”