The genomic and functional landscapes of developmental plasticity in the American cockroach

Sheng Li,Jianzhen Zhang,Daqi Li,Haigang Zhao,Chonghua Ren,Xiaoming Zhao,Shiming Zhu,Gangqi Fang,Qiaoyun Yue,Kang Li,Xiaoqiang Yu,Qiangqiang Jia,Shuai Zhan,Yanghui Cao,Dongwei Yuan,Suning Liu,Qili Feng,Yingying Cui,Yongliang Fan

doi:10.1038/s41467-018-03281-1

Abstract

Many cockroach species have adapted to urban environments, and some have been serious pests of public health in the tropics and subtropics. Here, we present the 3.38-Gb genome and a consensus gene set of the American cockroach, Periplaneta americana. We report insights from both genomic and functional investigations into the underlying basis of its adaptation to urban environments and developmental plasticity. In comparison with other insects, expansions of gene families in P. americana exist for most core gene families likely associated with environmental adaptation, such as chemoreception and detoxification. Multiple pathways regulating metamorphic development are well conserved, and RNAi experiments inform on key roles of 20-hydroxyecdysone, juvenile hormone, insulin, and decapentaplegic signals in regulating plasticity. Our analyses reveal a high level of sequence identity in genes between the American cockroach and two termite species, advancing it as a valuable model to study the evolutionary relationships between cockroaches and termites.

Highlights

Many cockroach species have adapted to urban environments, and some have been serious pests of public health in the tropics and subtropics
We present the functional studies and analyses of gene families and signaling pathways likely involved in major aspects of environmental adaptation and developmental plasticity in the American cockroach (Supplementary Fig. 2)
We identified 479 Blattodea-specific orthologs, representing approximately 1000 genes in each gene set of the two cockroaches, P. americana and B. germanica

Summary

Results and Discussion

We compared the gene repertoires of 12 representative insect species (Fig. 1a; Supplementary Table 6), including three sequenced blattodean species: (1) the German cockroach, B. germanica (Ectobiidae)[5]; (2) the dampwood termite, Z. nevadensis (Termopsidae)[6]; and (3) the fungus growing termite, Macrotermes natalensis (Termitidae)[7]. We identified 479 Blattodea-specific orthologs, representing approximately 1000 genes in each gene set of the two cockroaches, P. americana and B. germanica These two cockroach genomes encode the most genes across the species we analyzed. Chemosensory stimuli are mainly recognized by members of three related insect-specific chemosensory receptor families: olfactory receptors (ORs), gustatory receptors (GRs), and ionotropic glutamate receptors (IRs), while the odorantbinding proteins (OBPs) bind and transfer odors to ORs11–13 We manually annotated these gene families, and compared them among cockroaches, termites, and Drosophila

Pro-Spz

Injected time point

Methods