Silencing of the DNA methyltransferase 1 associated protein 1 (DMAP1) gene in the invasive ladybird Harmonia axyridis implies a role of the DNA methyltransferase 1‐DMAP1 complex in female fecundity

Abstract

The invasive harlequin ladybird Harmonia axyridis is a textbook example of polymorphism and polyphenism as the temperature during egg development determines the frequency of melanic morphs and the number and size of black spots in nonmelanic morphs. Recent concepts in evolutionary biology suggest that epigenetic mechanisms can translate environmental stimuli into heritable phenotypic changes. To investigate whether epigenetic mechanisms influence the penetrance and expressivity of colour morphs in H. axyridis, we used RNA interference to silence key enzymes required for DNA methylation and histone modification. We found that neither of these epigenetic mechanisms affected the frequency of different morphs, but there was a significant impact on life‐history traits such as longevity and fecundity. Strikingly, we found that silencing the gene encoding for DNA methyltransferase 1 associated protein 1 (DMAP1) severely reduced female fecundity, which correlated with an abundance of degenerated ovaries in DMAP1‐knockdown female beetles. Finally, we observed significant differences in DMAP1 expression when we compared native and invasive H. axyridis populations with a biocontrol strain differing in egg‐laying capacity, suggesting that the DNA methyltransferase 1‐DMAP1 complex may influence the invasive performance of this ladybird.

Epigenetic Control of Temperature-Dependent Female Reproductive Life History Trade-Offs in Seed Beetles, Callosobruchus maculatus

“…For instance, a recent study found that gene knockdown of Dnmt1 and methyl-DNA-binding protein 2/3 ( MBD2/3 ) - a gene involved in gene body methylation in insects - and methylation inhibition by 5-aza-2’-deoxycytidine (a pharmaceutical alternative to Zeb) impaired ovary development and reduced fecundity and hatch rates in developing silkworm ( Bombyx mori ), tobacco cutworm ( Spodoptera litura ) and migratory locust ( Locusta migratoria ), suggesting intragenic DNA methylation regulates insect reproduction [56]. Silencing the Dnmt1 associated protein 1 ( DMAP1 ) gene severely reduced fecundity and offspring survival in the harlequin ladybird ( Harmonia axyridis ), suggesting a role of the DNMT-DMAP1 complex in life history traits in H. axyridis [23]. Similarly, Dnmt silencing reduced the number of offspring produced in the brown plant hopper ( Nilaparvata lugens ) [21] and reduced egg production and embryo viability in the large milkweed bug ( Oncopeltus fasciatus ) [22].…”

“…Temperature induced changes in Dnmt expression or DNA methylation levels have previously been found in many insect species ( [20] and references therein), and previous studies have further identified a role for DNA methylation in insect life history and fitness [21][22][23]. Here, in an insect model species, we evaluate temperature dependence of DNA methylation, and we further manipulate epigenetic potential to assess downstream consequences for temperature-mediated plasticity in life history traits.…”

“…CC-BY 4.0 International license made available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It Epigenetic mechanisms have previously been implicated in plastic responses to environmental change, including temperature change (reviewed in [20]), and have also been implicated in several critical life history allocation decisions [21][22][23]. Epigenetic mechanisms thus represent important candidates for adaptively matching life history trade-off structures to temperature.…”

“…Epigenetic mechanisms have previously been implicated in plastic responses to environmental change, including temperature change (reviewed in [20]), and have also been implicated in several critical life history allocation decisions [21–23]. Epigenetic mechanisms thus represent important candidates for adaptively matching life history trade-off structures to temperature.…”

“…The presence and function of DNA methylation and its associated enzymes are highly varied among insect taxa, and the relationship between DNA methylation and phenotypic plasticity in insects remains an active area of research [35–38]. Temperature induced changes in Dnmt expression or DNA methylation levels have previously been found in many insect species ([20] and references therein), and previous studies have further identified a role for DNA methylation in insect life history and fitness [21–23]. Here, in an insect model species, we evaluate temperature dependence of DNA methylation, and we further manipulate epigenetic potential to assess downstream consequences for temperature-mediated plasticity in life history traits.…”