Evolved changes in DNA methylation in response to the sustained loss of parental care in the burying beetle

Mashoodh, Rahia; Sarkies, Peter; Westoby, Jennifer; Kilner, Rebecca M.

doi:10.1101/2021.03.25.436923

Cited by 9 publications

(18 citation statements)

References 63 publications

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“…Some studies have, however, hinted at an association between gene expression and differential methylation; for example: in the burying beetle, Nicrophorus vespilloides, 51% of genes that were differentially expressed in the brain after one generation of selection for no parental care were also associated with differential methylation. However, this relationship was not present after 30 generations of selection [69]. DNA methylation may also mark a sub-set of genes allowing them to be 'poised' for later gene expression, as has been documented for a histone modification in the honeybee [70].…”

Section: What Are the Functions Of Dna Methylation In Insects?mentioning

confidence: 95%

“…However, some evidence does exist to link methylation to gene expression differences associated with different behaviours. Mashoodh and colleagues [69] showed differentially methylated genes were overrepresented among differentially expressed genes for the burying beetle, Nicrophorus vespilloides, with some different parental care regimes, but this was not true of all of their treatments.…”

Section: How Does Dna Methylation Respond To Environmental Change and Phenotypic Plasticity?mentioning

confidence: 98%

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Phenotypic Plasticity: What Has DNA Methylation Got to Do with It?

Duncan

Cunningham

Dearden

2022

Insects

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How does one genome give rise to multiple, often markedly different, phenotypes in response to an environmental cue? This phenomenon, known as phenotypic plasticity, is common amongst plants and animals, but arguably the most striking examples are seen in insects. Well-known insect examples include seasonal morphs of butterfly wing patterns, sexual and asexual reproduction in aphids, and queen and worker castes of eusocial insects. Ultimately, we need to understand how phenotypic plasticity works at a mechanistic level; how do environmental signals alter gene expression, and how are changes in gene expression translated into novel morphology, physiology and behaviour? Understanding how plasticity works is of major interest in evolutionary-developmental biology and may have implications for understanding how insects respond to global change. It has been proposed that epigenetic mechanisms, specifically DNA methylation, are the key link between environmental cues and changes in gene expression. Here, we review the available evidence on the function of DNA methylation of insects, the possible role(s) for DNA methylation in phenotypic plasticity and also highlight key outstanding questions in this field as well as new experimental approaches to address these questions.

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Section: What Are the Functions Of Dna Methylation In Insects?mentioning

confidence: 95%

Section: How Does Dna Methylation Respond To Environmental Change and Phenotypic Plasticity?mentioning

confidence: 98%

Phenotypic Plasticity: What Has DNA Methylation Got to Do with It?

Duncan

Cunningham

Dearden

2022

Insects

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“…Not surprisingly, we found a larger transcriptional response in offspring than in parents. Thousands of differentially expressed genes (DEGs) were detected in larvae spanning many functional categories, consistent with the very rapid development and growth occurring at this early stage (Won et al 2018) and the strong influence of parenting (Capodeanu-Nägler et al 2018;Mashoodh et al 2021). In comparison to the dramatic changes that occur in larvae once they are accepted by parents, the behavioral switch required for parents to accept their larvae and begin active parenting is relatively subtle, occurring more than 50 hours into care (Oldekop et al 2007).…”

Section: Discussionmentioning

confidence: 77%

“…While we cannot disentangle the direct effects being parented per se on gene expression (Capodeanu-Nägler et al, 2018;Mashoodh et al, 2021) from indirect effects associated with the rapid development and growth occurring at this early stage (Won et al, 2018), our sampling design was biologically realistic given that orphaned N. orbicollis larvae usually succumb to starvation within a day (Capodeanu-Nägler et al 2018). In comparison, changes of parental gene expression associated with having larvae to parent were subtle (~100-200 differentially expressed genes), in line with the hypothesis that the modification of behavior within a state involves a much smaller subset of the genes required to transition between states (i.e., N.…”

Section: Discussionmentioning

confidence: 99%

“…In some cases, this plasticity may be immediately detectable as a change in behavior. For example, many birds compensate for harsh breeding season conditions by increasing the density of food loads delivered to chicks (Grissot et al 2019) or by extending incubation times (McClintock et al 2014;Sharpe et al 2021), while offspring have been shown to upregulate metabolic and immune pathways in response to the removal of a caring parent (Ziadie et al 2019;Körner et al 2020;Mashoodh et al 2021) or exposure to pathogens (Körner et al 2020). However, when parents and offspring are pushed to their physiological limits, maintaining a stable phenotype is likely just as important for ensuring offspring success as is altering behavior.…”

Section: Introductionmentioning

confidence: 99%

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Limited plasticity in gene expression for providing or receiving parental care under different temperatures

Moss

Cunningham

McKinney

et al. 2021

Preprint

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Parenting buffers offspring from hostile environments, but it is not clear how or if the genes that underlie parenting change their expression under environmental stress. We recently demonstrated that for the subsocial carrion beetle, Nicrophorus orbicollis, temperature during parenting does not affect parenting phenotypes. Here, we ask if transcriptional changes associated with parenting are likewise robust to environmental stress. The absence of a transcriptional response for parenting under stress would suggest that the genetic ‘programs’ for parenting and being parented are canalized. Conversely, a robust transcriptional response would suggest that plasticity of underlying gene expression is critical for maintaining behavioral stability, and that these mechanisms provide a potential target for selection in the face of environmental change. We test these alternatives by characterizing gene expression of parents and offspring with and without parent-offspring interactions under a benign and a stressful temperature. We found that parent-offspring interactions elicit distinct transcriptional responses of parents and larvae irrespective of temperature. We further detected robust changes of gene expression in beetles breeding at 24° C compared to 20° C irrespective of family interaction. However, no strong interaction between parent-offspring interaction and temperature was detected for either parents or larvae. We therefore conclude that canalization, not plasticity of gene expression, most likely explains the absence of behavioral plasticity under thermal stress. This result suggests that species may not have the genetic variation needed to respond to all environmental change, especially for complex phenotypes.IMPACT STATEMENTParenting is thought to evolve to buffer offspring from harsh or inhospitable conditions. However, once evolved, does parenting continue to buffer against new environmental challenges such as might occur under global warming? One way organisms achieve different phenotypes without evolving different genes for each trait is by changing timing or extent of gene expression. Changes in gene expression influencing physiological traits such as hypoxia have been shown to facilitate adaptation to changing environments. It is less clear if changes in gene expression are also important for behavioral plasticity in complex social traits, such as parental care. In this study, we ask whether families of the subsocial burying beetle, Nicrophorus orbicollis, show altered expression of parent or offspring genes that may help compensate for reduced offspring success under global warming. To test the extent that gene expression underlies behavioral plasticity in parenting and offspring responses to parenting, we characterize the gene expression profiles of whole families (males, females, and larvae) with and without parent-offspring interactions under two thermal conditions: 20° C and 24° C. We found that heat stress predominantly induced downregulation of genes, consistent with a constrained acclimation response. However, when temperature was considered in conjunction with parent-offspring interactions, genetic plasticity was extremely limited. That is, the genes underlying parent-offspring interactions did not show strong signatures of differential expression under more stressful thermal conditions. Given that we previously found no effects of temperature on parental behavior, we suggest that constrained, not plastic gene expression, underpins stability of parent-offspring interactions and limits the buffering capacity for family interactions under environmental stress. Insights from this study deepen our understanding of the interplay between genetic and phenotypic plasticity in complex behavioral traits and how traits such as parenting may limit responses to novel environmental challenges.

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Genome-wide DNA methylation patterns in bumble bee (Bombus vosnesenskii) populations from spatial-environmental range extremes

Rahman,

Lozier

2023

Sci Rep

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Unraveling molecular mechanisms of adaptation to complex environments is crucial to understanding tolerance of abiotic pressures and responses to climatic change. Epigenetic variation is increasingly recognized as a mechanism that can facilitate rapid responses to changing environmental cues. To investigate variation in genetic and epigenetic diversity at spatial and thermal extremes, we use whole genome and methylome sequencing to generate a high-resolution map of DNA methylation in the bumble bee Bombus vosnesenskii. We sample two populations representing spatial and environmental range extremes (a warm southern low-elevation site and a cold northern high-elevation site) previously shown to exhibit differences in thermal tolerance and determine positions in the genome that are consistently and variably methylated across samples. Bisulfite sequencing reveals methylation characteristics similar to other arthropods, with low global CpG methylation but high methylation concentrated in gene bodies and in genome regions with low nucleotide diversity. Differentially methylated sites (n = 2066) were largely hypomethylated in the northern high-elevation population but not related to local sequence differentiation. The concentration of methylated and differentially methylated sites in exons and putative promoter regions suggests a possible role in gene regulation, and this high-resolution analysis of intraspecific epigenetic variation in wild Bombus suggests that the function of methylation in niche adaptation would be worth further investigation.

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Evolved changes in DNA methylation in response to the sustained loss of parental care in the burying beetle

Cited by 9 publications

References 63 publications

Phenotypic Plasticity: What Has DNA Methylation Got to Do with It?

Phenotypic Plasticity: What Has DNA Methylation Got to Do with It?

Limited plasticity in gene expression for providing or receiving parental care under different temperatures

Genome-wide DNA methylation patterns in bumble bee (Bombus vosnesenskii) populations from spatial-environmental range extremes

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