Thermal transgenerational effects remain after two generations

Lee, Who‐Seung; Salinas, Santiago; Lee, Young‐Rog; Siskidis, Jo Anne; Mangel, Marc; Munch, Stephan B.

doi:10.1002/ece3.6767

Cited by 10 publications

(13 citation statements)

References 49 publications

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“…Previous studies have found a significant interaction between parental treatment temperature and offspring rearing temperature on growth rate (Salinas and Munch, 2012;Lee et al, 2020;Munch et al, 2021). Here, we found that transgenerational effects on growth rate extend out to 63 days post-hatch, indicating that thermal TGP persists throughout the entire juvenile stage.…”

Section: Growth Rate 21 Daysmentioning

confidence: 91%

“…The fish were acclimated in aquaria held at 24 • C at the Southwest Fisheries Science Center, Santa Cruz, California. As sheepshead minnows exhibit grandparental effects (Lee et al, 2020) we maintained breeding populations in the lab under constant temperature (24 • C) for three generations, to reduce uncontrolled environmental effects and used F 3 fish as the parents in this experiment.…”

Section: Methodsmentioning

confidence: 99%

“…Therefore, we are reasonably confident that TGP in sheepshead minnows is not an experimental artifact. Moreover, the fact that sire-driven TGP is nearly equal to that contributed by dams after 3 weeks of growth and persists to grand-offspring (Lee et al, 2020), strongly suggest that thermal TGP in offspring growth is epigenetic, though further work is needed to elucidate a specific mechanism, e.g., methylation (Jiang et al, 2013;Skvortsova et al, 2019).…”

Section: Growth Rate 21 Daysmentioning

confidence: 99%

“…Moreover, they grow well in individual housings making it possible to eliminate competition for food and social stress as factors influencing growth. Critically, previous studies have found that sheepshead minnows exhibit thermal TGP across multiple generations (Salinas and Munch, 2012;Lee et al, 2020). After 30 days of parental exposure to different temperatures, the fastest growing offspring tend to be individuals whose parents were at the same temperature (Salinas and Munch, 2012;Munch et al, 2021).…”

Section: Introductionmentioning

confidence: 98%

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Separating Paternal and Maternal Contributions to Thermal Transgenerational Plasticity

2021

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Climate change is rapidly altering the thermal environment in terrestrial and aquatic systems. Transgenerational thermal plasticity (TGP) – which occurs when the temperatures experienced by the parental generation prior to the fertilization of gametes results in a change in offspring reaction norms – may mitigate the effects of climate change. Although “maternal effects” have been widely studied, relatively little is known about TGP effects in vertebrates, particularly paternal contributions. We used artificial fertilization to cross sheepshead minnow (Cyprinodon variegatus) parents exposed to either low (26°C) or high (32°C) temperatures and measured growth rates of the offspring over the first 8 weeks of life at both low and high temperatures. A linear mixed effects model was employed to quantify the effects of maternal, paternal, and offspring temperatures on offspring growth and fecundity. We found that the offspring growth rate up to 63 days post-hatch was affected by both the temperature they experienced directly and parental temperatures prior to fertilization. Growth was lowest when neither parents’ temperature matched the offspring temperature, indicating a strong transgenerational effect. Notably, offspring growth was highest when all three (offspring, sire, and dam) temperatures matched [although the three-way interaction was found to be marginally non-significant (P = 0.155)], suggesting that TGP effects were additive across significant sire-offspring (P < 0.001) and dam-offspring interactions (P < 0.001). Transgenerational effects on fecundity (GSI) were suggestive for both maternal and paternal effects, but not significant. The finding that thermal TGP is contributed by both parents strongly suggests that it has an epigenetic basis.

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Section: Growth Rate 21 Daysmentioning

confidence: 91%

Section: Methodsmentioning

confidence: 99%

Section: Growth Rate 21 Daysmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 98%

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Separating Paternal and Maternal Contributions to Thermal Transgenerational Plasticity

2021

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“…In general, transgenerational warm acclimation had a smaller effect on differential gene expression compared to the strength of within-generation warm acclimation and, for some genes, transgenerational acclimation had opposing effects on offspring gene expression (mothers vs. fathers, or parents vs. offspring). The influence of transgenerational acclimation on offspring responses to environmental changes is complex, may not always be apparent in the phenotype or may have weak effects (Uller et al 2013; Bautista and Burggren 2019; Lee et al 2020; Sánchez-Tójar et al 2020). However, the patterns of gene expression we observed here could present itself in the offspring’s phenotype and we have previously shown that transgenerational environmental mismatching can have maladaptive effects in lake trout (Penney et al 2021).…”

Section: Discussionmentioning

confidence: 99%

Transcriptomic responses to within- and transgenerational environmental warming in a cold-adapted salmonid

Penney

Burness

Wilson

2022

Preprint

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Cold-adapted species are particularly threatened by climate change as rates of environmental warming outpace the ability of many populations adapt. Recent evidence suggest that transgenerational thermal plasticity may play a role in the response of cold-adapted organisms to long-term changes in temperature. Using RNA sequencing, we explored differential gene expression of lake trout (Salvelinus namaycush), a cold-adapted species, to examine the molecular processes that respond to elevated temperatures under conditions of within-generation (offspring) and transgenerational (parental) warm-acclimation. We hypothesized that genes associated with metabolism, growth and thermal stress/tolerance would be differentially expressed in juvenile lake trout offspring depending on their own acclimation temperature and that of their parents. We found enriched pathways for thermal stress, signaling processes, immune function, and transcription regulation, although the specific genes and direction of differential expression (up- or downregulation) depended on the combination of offspring and parental thermal rearing conditions. While parental warm-acclimation did have a transgenerational effect on gene expression in their offspring, within-generation warm-acclimation had a larger effect on differential expression, enriching more pathways. We provide evidence of the transgenerational response to warming at the transcriptional level in lake trout, which should be useful for future studies of transcriptomics and plasticity in these and other cold-adapted species.

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Plastic maternal effects of social density on reproduction and fitness in the least killifish, Heterandria formosa

Levell

Bedgood

Travis

2023

Ecology and Evolution

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Environmental parental effects, also known as transgenerational plasticity, are widespread in plants and animals. Less well known is whether those effects contribute to maternal fitness in the same manner in different populations. We carried out a multigenerational laboratory experiment with females drawn from two populations of the least killifish, Heterandria formosa, to assess transgenerational plasticity in reproductive traits in response to differences in social density and its effects on maternal fitness. In the first and second generations, increased density decreased reproductive rate and increased offspring size in females from both populations. There were complicated patterns of transgenerational plasticity on maternal fitness that differed between females from different populations. Females from a population with historically low densities whose mothers experienced lower density had higher fitness than females whose mothers experienced higher density, regardless of their own density. The opposite pattern emerged in females from the population with historically high densities: Females whose mothers experienced higher density had higher fitness than females whose mothers experienced lower density. This transgenerational plasticity is not anticipatory but might be considered adaptive in both populations if providing those “silver spoons” enhances offspring fitness in all environments.

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Thermal transgenerational effects remain after two generations

Cited by 10 publications

References 49 publications

Separating Paternal and Maternal Contributions to Thermal Transgenerational Plasticity

Separating Paternal and Maternal Contributions to Thermal Transgenerational Plasticity

Transcriptomic responses to within- and transgenerational environmental warming in a cold-adapted salmonid

Plastic maternal effects of social density on reproduction and fitness in the least killifish, Heterandria formosa

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