Separating Paternal and Maternal Contributions to Thermal Transgenerational Plasticity

Sarah L Chang,Stephan B Munch,Who-Seung Lee

doi:10.3389/fmars.2021.734318

Sarah L Chang, Stephan B Munch + Show 1 more

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https://doi.org/10.3389/fmars.2021.734318

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Abstract

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 &lt; 0.001) and dam-offspring interactions (P &lt; 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.

Highlights

Global temperatures are predicted to rise by at least 2◦C by 2050–2100, a rapid shift that is significantly more than that of the past 420,000 years (Hoegh-Guldberg et al, 2007)
The ramifications of rapid climate change can be buffered by transgenerational plasticity (TGP), a carryover effect that is characterized by changes in the reaction norms of offspring that are closely correlated to the environment experienced by the parents (Mousseau and Fox, 1998; Donelson et al, 2018)
We evaluated the effect of parental temperature on offspring thermal performance, explicitly partitioning sire and dam contributions to growth rate and reproductive allocation using sheepshead minnows (Cyprinodon variegatus) as our model organism

Summary

Introduction

Global temperatures are predicted to rise by at least 2◦C by 2050–2100, a rapid shift that is significantly more than that of the past 420,000 years (Hoegh-Guldberg et al, 2007). Increased ocean temperatures can negatively affect marine organisms, e.g., shifts in metabolic rate (Gillooly et al, 2001), decreased body size at each key developmental stages (Atkinson, 1995), and declines in fish population size (Clark et al, 2003). The ramifications of rapid climate change can be buffered by transgenerational plasticity (TGP), a carryover effect that is characterized by changes in the reaction norms of offspring that are closely correlated to the environment experienced by the parents (Mousseau and Fox, 1998; Donelson et al, 2018). Parental contributions to offspring can alter the strength of selection on organisms during early life stages in response to climate change, allowing for population persistence and adaptation in populations with high genetic diversity (Heckwolf et al, 2018). Maternal effects are found in a wide range of both invertebrate and vertebrate taxa (Mousseau and Dingle, 1991; Mousseau and Fox, 1998; Galloway and Etterson, 2007; Shama, 2015; Ruebel and Latham, 2020; McGhee et al, 2021) and arise through a variety of mechanisms, e.g., provisioning of energy or nutrients (Berkeley et al, 2004), hormones (Groothuis and Schwabl, 2008), and antibodies (Grindstaff et al, 2003), or epigenetic mechanisms such as DNA methylation (Cooney et al, 2002) and histone modification (Upadhyaya et al, 2017)

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