Abstract
Insects provide an unparalleled opportunity to link genomic changes with the rise of novel phenotypes, given tremendous variation in the numerous and complex adaptations displayed across the group. Among these numerous and complex adaptations, live-birth has arisen repeatedly and independently in insects and across the tree of life, suggesting this is one of the most common types of convergent evolution among animals. We sequenced the genome and transcriptome of the Pacific beetle-mimic cockroach, the only truly viviparous cockroach, and performed comparative analyses including two other viviparous insect lineages, the tsetse and aphids, to unravel the genomic basis underlying the transition to viviparity in insects. We identified pathways experiencing adaptive evolution, common in all viviparous insects surveyed, involved in uro-genital remodeling, maternal control of embryo development, tracheal system, and heart development. Our findings suggest the essential role of those pathways for the development of placenta-like structure enabling embryo development and nutrition. Viviparous transition seems also to be accompanied by the duplication of genes involved in eggshell formation. Our findings from the viviparous cockroach and tsetse reveal that genes involved in uterine remodeling are up-regulated and immune genes are down-regulated during the course of pregnancy. These changes may facilitate structural changes to accommodate developing young and protect them from the mothers immune system. Our results denote a convergent evolution of live-bearing in insects and suggest similar adaptive mechanisms occurred in vertebrates, targeting pathways involved in eggshell formation, uro-genital remodeling, enhanced tracheal and heart development, and reduced immunity.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
BF performed the multiple sequence alignments, detection of selection, and functional categories enrichment analyses, wrote the first version of the manuscript; MCH performed the genome assembly and annotations, ortholog clustering, gene family evolution analyses, wrote the first version of the manuscript; AAM performed the annotation of chemoreceptors; EM participated in the organisation of the project; SE participated in the RNA-seq analysis; MC performed the RNA-seq analysis; ECJ performed the RNA-seq analysis and collected samples for DNA sequencing; GMA contributed to figure development; MP assisted in the genome assembly; JBB provided funding, performed the RNA-seq analysis, and functional gene suppression studies; EBB provided funding and supervised bioinformatics analyses and organization of the project; SST provided funding and participated in early organization of the project. All authors contributed to revisions of the manuscript with the exception of SST†.
Data deposition: The data reported in this paper have been deposited in the National Center for Biotechnology Information Genome Archive (GenBank assembly accession no. GCA_XXXXXXXXX.1, BioProject accession no. PRJNA803029, BioSample accession no. SAMN25610536) and the source code of the comparative genomic pipeline in github repository (github.org//xxxx/).
↵† Stephen S. Tobe sadly passed away during the final production of this manuscript. Dr. Tobe made critical contributions to this article and his work on invertebrate biology has been foundational