1 ∣ INTRODUCTION
Since the launch of the 5,000 Insect Genome Project (i5k) in 2011, at
least 497 insect genomes have been sequenced and annotated according to
the NCBI database (Robinson et al.,
2011). Most of the sequenced insect
genomes
are either important agricultural pests, vectors for pathogens, or
species that serve as model organisms
(Xianhui et al., 2014). Silkworm
(Bombyx mori ), honeybee (Apis cerana ) and WWS
(Ericerus pela ) are the top three resource insects that have
provided significant economic or medical benefits to humans for
millennia. The genomes of both honeybee and silkworm have been sequenced
and extensively annotated, whereas high-quality genomic data for WWS is
still absent so far (Consortium, 2006;
Xia et al., 2004). Found in the
subtropical and temperate regions of China, Japan and Russia
(Supplementary Fig. 1), WWS-derived white wax has been extensively used
in printing, pharmaceutical, food and cosmetic industries because of its
special chemical properties (Ma et al.,
2018; Wang et al., 2017).
The evolutionary origin of the insect metamorphosis is a much-debated
mystery in biology. Wing development in insects occurs during
metamorphosis, however, the evolutionary drivers led up to the invention
of metamorphosis are still poorly understood
(Misof et al., 2014). Juvenile hormone
mediates metamorphosis in a range of insect species
(Azinna et al., 2018;
Stillwell et al., 2010). Research on
firebugs has shown how juvenile hormone counteracts ecdysone during the
nymph instar in hemimetabolous insects
(Barbora et al., 2011;
Slama & Williams, 1965). During the
evolution of metamorphosis, a heterochronic shift in the time of the
appearance of juvenile hormone during embryogenesis appears to have
interrupted the ancestral growth trajectory in the developing insect
(Gilbert, 1994). Previous studies noted
that juvenile hormone plays a crucial role in mediating neoteny of
different insect species. Scale insects such as WWS convergently
acquired a unique mode of metamorphosis referred to as neometaboly,
which is reminiscent of holometaboly (Vea
et al., 2016). WWS males produce wax during the nymph stages and form
winged adults, resembling a holometabolous fate (Supplementary Fig. 2).
Females, however, remain stationary and appear to follow a
hemimetabolous route (Qi et al., 2019). Accordingly, WWS represents an
attractive research model not only to investigate the adaptive
mechanisms by which a herbivorous parasite overcomes plant defense
systems, but it also serves as an excellent model for the evolutionary
relationships between hemimetabolous and holometabolous insects. In this
study, we comprehensively analyzed the developmental differences between
males and females using high-quality whole genome data of WWS,
transcriptome profiling and DNA methylation. Our study paves the way to
understand the developmental processes during metamorphosis and the
hormone antagonism effect the sexual differentiation of metamorphosis in
insects.