3.5 ∣ Evolutionary metamorphosis
According to gene clustering analyses, 24,923 gene families could be
used for evolutionary comparison between WWS and other 15 representative
insects (Supplementary Figure 7, Supplementary Table 10). A phylogenetic
tree was generated with robust and consistent results on key taxa from
extant insect orders representing hemimetabolic, holometabolic and
ametabolic species, and estimated divergence dates based on validated
fossils (Figure 2c). Regardless of the reference genomes and
tree-building methods used, the genome phylogeny strongly supported the
interspecific relationships shown in the tree based on the analyses of
reference genomes (Figure 2c). Estimation of divergence times suggests
that the aphids Acyrthosiphon pisum and Diuraphis noxiaform a sister group and diverged from the WWS in the Middle Triassic
(∼218.0 ± 60.7 Mya). Further, our analysis indicated that the last
common ancestor of Holometabola and Hemimetabola separated in the Late
Carboniferous (∼301.6 ± 9.7 Mya). This differs from a previous report,
which found that fossils of holometabolic insects were first seen at the
end of Permian (∼252 Mya) and constitute a monophyletic group
(Kristensen, 1975;
Nel et al., 2013). Our research indicates
that complete metamorphosis emerged in the Late Carboniferous (∼301.6 ±
9.7 Mya, Figure 2c), at least 50 million years earlier than the previous
study, and followed by a period were terrestrial plants diversified
dramatically (Misof et al., 2014). Based
on the phylogenetic analysis, ametabolous represent a primitive group
located in the basal branch of the tree, whereas hemiptera and
holometabola reside in the lower and upper branches separately. WWS
represents an important transitional model between hemimetaboly and
holometaboly. Our study provides evidence that holometamorphosis derived
from hemimetamorphosis in the Late Carboniferous. Clearly, there is an
evolutionary trend from ametabolous to hemimetabolous insect
development, followed by the emergence of holometabola (Figure 1b, 2c).