Transgenerational plasticity (TGP) occurs when the environment experienced by a parent influences the development of their offspring. In this article, we develop a framework for understanding the ...mechanisms and multigenerational consequences of TGP. First, we conceptualize the mechanisms of TGP in the context of communication between parents (senders) and offspring (receivers) by dissecting the steps between an environmental cue received by a parent and its resulting effects on the phenotype of one or more future generations. Breaking down the problem in this way highlights the diversity of mechanisms likely to be involved in the process. Second, we review the literature on multigenerational effects and find that the documented patterns across generations are diverse. We categorize different multigenerational patterns and explore the proximate and ultimate mechanisms that can generate them. Throughout, we highlight opportunities for future work in this dynamic and integrative area of study.
Our ability to predict how species will respond to human-induced rapid environmental change (HIREC) may depend upon our understanding of transgenerational plasticity (TGP), which occurs when ...environments experienced by previous generations influence phenotypes of subsequent generations. TGP evolved to help organisms cope with environmental stressors when parental environments are highly predictive of offspring environments. HIREC can alter conditions that favored TGP in historical environments by reducing parents’ ability to detect environmental conditions, disrupting previous correlations between parental and offspring environments, and interfering with the transmission of parental cues to offspring. Because of the propensity to produce errors in these processes, TGP will likely generate negative fitness outcomes in response to HIREC, though beneficial fitness outcomes may occur in some cases.
Human activities are dramatically altering ecological communities. While many organisms are threatened by human-induced rapid environmental change (HIREC), others are thriving. This variability is often attributed to differences in genetic variation and/or within-generational plasticity, but transgenerational plasticity (TGP) may be another key (often overlooked) process that contributes to this variation.We develop a framework that explores how TGP can affect organisms’ responses to HIREC. We highlight three sequential processes in the detection and transmission of parental cues to offspring that are critical for TGP to be beneficial in a given environment.Because many hypotheses regarding TGP in human-altered environments have yet to be tested, our framework summarizes potential positive and negative outcomes and outlines key areas for future study.
Aims
Phyllosphere bacteria play critical roles in plant growth promotion, disease suppression and global nutrient cycling but remain understudied.
Methods
In this project, we examined the bacterial ...community on the phyllosphere of eight diverse lines of
Brassica napus
for ten weeks in Saskatoon, Saskatchewan Canada.
Results
The bacterial community was shaped largely by plant growth stage with distinct communities present before and after flowering. Bacterial diversity before flowering had 111 core members with high functional potential, with the peak of diversity being reached during flowering. After flowering, bacterial diversity dropped quickly and sharply to 16 members of the core community, suggesting that the plant did not support the same functional potential anymore.
B. napus
line had little effect on the larger community, but appeared to have more of an effect on the rare bacteria.
Conclusions
Our work suggests that the dominant bacterial community is driven by plant growth stage, whereas differences in plant line seemed to affect rare bacteria. The role of these rare bacteria in plant health remains unresolved.
Edge effects resulting from adjacent land uses are poorly understood in agroecosystems yet understanding above and belowground edge effects is crucial for maintaining ecosystem function. The aim of ...our study was to examine impacts of land management on aboveground and belowground edge effects, measured by changes in plant community, soil properties, and soil microbial communities across agroecosystem edges. We measured plant composition and biomass, soil properties (total carbon, total nitrogen, pH, nitrate, and ammonium), and soil fungal and bacterial community composition across perennial grassland-annual cropland edges. Edge effects due to land management were detected both aboveground and belowground. The plant community at the edge was distinct from the adjacent land uses, where annual, non-native, plant species were abundant. Soil total nitrogen and carbon significantly decreased across the edge (P < 0.001), with the highest values in the perennial grasslands. Both bacterial and fungal communities were different across the edge with clear changes in fungal communities driven directly and indirectly by land management. A higher abundance of pathogens in the more heavily managed land uses (i.e. crop and edge) was detected. Changes in plant community composition, along with soil carbon and nitrogen also influenced the soil fungal community across these agroecosystems edges. Characterizing edge effects in agroecosystem, especially those associated with soil microbial communities, is an important first step in ensuring soil health and resilience in these managed landscapes.
Holobiont bacterial community assembly processes are an essential element to understanding the plant microbiome. To elucidate these processes, leaf, root, and rhizosphere samples were collected from ...eight lines of Brassica napus in Saskatchewan over the course of 10 weeks. We then used ecological null modeling to disentangle the community assembly processes over the growing season in each plant part. The root was primarily dominated by stochastic community assembly processes, which is inconsistent with previous studies that suggest of a highly selective root environment. Leaf assembly processes were primarily stochastic as well. In contrast, the rhizosphere was a highly selective environment. The dominant rhizosphere selection process leads to more similar communities. Assembly processes in all plant compartments were dependent on plant growth stage with little line effect on community assembly. The foundations of assembly in the leaf were due to the harsh environment, leading to dominance of stochastic effects, whereas the stochastic effects in the root interior likely arise due to competitive exclusion or priority effects. Engineering canola microbiomes should occur during periods of strong selection assuming strong selection could promote beneficial bacteria. For example, engineering the microbiome to resist pathogens, which are typically aerially born, should focus on the flowering period, whereas microbiomes to enhance yield should likely be engineered postflowering as the rhizosphere is undergoing strong selection.
In order to harness the microbiome for more sustainable crop production, we must first have a better understanding of microbial community assembly processes that occurring during plant development. This study examines the bacterial community assembly processes of the leaf, root, and rhizosphere of eight different lines of Brassica napus over the growing season. The influence of growth stage and B. napus line were examined in conjunction with the assembly processes. Understanding what influences the assembly processes of crops might allow for more targeted breeding efforts by working with the plant to manipulate the microbiome when it is undergoing the strongest selection pressure.
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.
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.
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.
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.
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.
This study demonstrates that sperm‐mediated paternal effects can be inherited selectively across generations in a lineage and sex‐specific fashion. In threespined sticklebacks, the phenotypes of male and female F2s varied when predation risk was experienced by maternal versus paternal grandfathers, with non‐additive interactions when one versus two grandfathers were predator‐exposed.
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.
In three‐spined sticklebacks, maternal and paternal exposure to predation risk had largely distinct effects in offspring and parental experiences produced different phenotypes in sons versus daughters. Further, non‐additive interactions between maternal and paternal effects suggest offspring phenotypes are influenced by the interplay between environmentally‐induced epigenetic changes in eggs versus sperm.
There is growing evidence that offspring receive information about their environment vertically, i.e. from their parents (environmental parental effects or transgenerational plasticity). For example, ...parents exposed to predation risk may produce offspring with heightened antipredator defences. At the same time, organisms can gain information about the environment horizontally, from conspecifics. In this study, we provide some of the first evidence that horizontally acquired social information can be transmitted vertically across generations. Three-spined stickleback (
) fathers produced larval offspring with altered antipredator behaviour when fathers received visual and olfactory cues from predator-chased neighbours. Although fathers did not personally witness their neighbours being chased (i.e. they never saw the predator), changes in offspring traits were similar to those induced by direct paternal exposure to predation risk. These findings suggest that two different non-genetic pathways (horizontal transfer of social information, vertical transfer via sperm-mediated paternal effects) can combine to affect offspring phenotypes. The implications of simultaneous horizontal and vertical transmission are widely appreciated in the context of disease and culture; our results suggest that they could be equally important for the maintenance of phenotypic variation and could have profound consequences for the rate at which information flows within and across generations.
The environment experienced by one generation can influence the phenotypes of future generations. Because parental cues can be conveyed to offspring at multiple points in time, ranging from ...fertilization to posthatching/parturition, offspring can potentially receive multiple cues from their parents via different mechanisms. We have relatively little information regarding how different mechanisms operate in isolation and in tandem, but it is possible, for example, that offspring phenotypes induced by nongenetic changes to gametes may be amplified by, mitigated by, or depend upon parental care. Here, we manipulated paternal experience with predation risk prior to fertilization in threespine stickleback, Gasterosteus aculeatus, and then examined the potential of paternal care to mitigate and/or amplify sperm-mediated paternal effects. Specifically, we compared (1) offspring of predator-exposed fathers who were reared without paternal care, (2) offspring of predator-exposed fathers who were reared with paternal care, (3) offspring of control (unexposed) fathers who were reared without paternal care and (4) offspring of control fathers who were reared with paternal care. We found that offspring of predator-exposed fathers were less active and had higher cortisol following a simulated predator attack. Although predator-exposed males shifted their paternal care behaviours – reduced fanning early in egg development and increased fanning right before egg hatching compared to control males – this shift in paternal behavior did not appear to affect offspring traits. This suggests that paternal care neither amplifies nor compensates for these phenotypic effects induced by sperm and that nongenetic changes induced by sperm may occur independently of nongenetic changes induced by paternal care. Overall, these results underscore the importance of considering how parents may have multiple nongenetic mechanisms by which they can influence offspring.
•We studied how nongenetic changes to sperm and paternal care influence offspring.•Predator-exposed fathers delayed paternal care until later in offspring development.•Paternal predation exposure reduced activity and increased cortisol in offspring.•Predator-induced changes were similar in orphaned and parented offspring.•Paternal care did not appear to influence sperm-mediated paternal effects.
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 F
and F
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 F
parents. Here, we used three-spined sticklebacks (
) to understand how paternal exposure to predation risk prior to mating alters reproductive traits and parental care behaviour in unexposed F
sons and F
grandsons. Sons of predator-exposed fathers took more attempts to mate than sons of control fathers. F
sons and F
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 F
to the F
and F
generations.
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