Genome assembly and methylome analysis of the white wax scale insect
provides insight into sexual differentiation of metamorphosis in
hexapods
Abstract
Scale insects are hemimetabolous, showing “incomplete” metamorphosis
and no true pupal stage. Ericerus pela, commonly known as the white wax
scale insect (hereafter, WWS), is a wax-producing insect found in Asia
and Europe. WWS displays dramatic sexual dimorphism, with notably
different metamorphic fates in males and females. Males develop into
winged adults, while females are neotenic and maintain a nymph-like
appearance, which are flightless and remain stationary. Here we report
the de novo assembly of the WWS genome with its size of 638.30 Mb
(69.68Mb for scaffold N50) by PacBio sequencing and Hi-C. From these
data, we constructed a robust phylogenetic analysis of 24,923 gene
families from 16 representative insect genomes, which indicates that
holometabola evolved from incomplete metamorphosis insects in the Late
Carboniferous, about 50 million years earlier than previously thought.
To study the distinct development of males and females, we analyzed the
methylome landscape in either sex. Surprisingly, WWS displayed high
levels of methylation (4.42% for males) when compared to other insects.
We observed differential methylation patterns for genes involved in
steroid and sesquiterpenoids production as well as related fatty acid
metabolism pathways. We show here that both males and females exhibit
distinct titer profiles for ecdysone, the principal insect steroid
hormone, and juvenile hormone (a sesquiterpenoid), suggesting that these
hormones are the primary drivers of sexually dimorphic features. Our
results provide a comprehensive genomic and epigenomic resource of scale
insects that provide new insights into the evolution of metamorphosis
and sexual dimorphism in insects.