Live-bearing cockroach genome reveals convergent evolutionary mechanisms linked to viviparity in insects and beyond

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.

Lipid metabolism dysfunction following symbiont elimination is linked to altered Kennedy pathway homeostasis

“…Thus, a distinct commonality of viviparity among animals is the requirements of specific B vitamins for lipid metabolism to meet the energetic demand of internal progeny development. This expands on genomic similarities (Fouks et al 2022) to other physiological processes that are similar between invertebrate and vertebrate viviparity.…”

“…Along with the role among arthropod systems, genomic studies have identified significant functional convergence among live-bearing systems in invertebrate and vertebrate lineages (Fouks et al, 2022). This includes aspects that range from metabolism to immune function (Fouks et al, 2022).…”

“…Along with the role among arthropod systems, genomic studies have identified significant functional convergence among live-bearing systems in invertebrate and vertebrate lineages (Fouks et al, 2022). This includes aspects that range from metabolism to immune function (Fouks et al, 2022). In the vertebrate systems, fetal development requires essential fatty acids and long chain polyunsaturated fatty acids (Herrera, 2002; Knopp et al, 1998; Ryckman et al, 2015).…”

“…Other insects that rely on symbiont-derived B vitamins, including bed bugs and lice (Benoit et al, 2016; Boyd et al, 2017; Hosokawa et al, 2010; Kirkness et al, 2010), are likely to experience impaired lipolysis and reduced fecundity in the absences of their symbiotic partner(s), as the molecular mechanisms underlying this process are not unique to Glossina (Thomas et al, 2020). Furthermore, similarities in live birth across animal systems indicate that micronutrient deprivation is likely to have significant impacts on metabolic processes with similar negative consequences that extend from invertebrates to vertebrates (Fouks et al, 2022).…”

Lipid metabolism dysfunction following symbiont elimination is linked to altered Kennedy pathway homeostasis

“… 26 Furthermore, similarities in live birth across animal systems indicate that micronutrient deprivation is likely to significantly impact metabolic processes with similar negative consequences that extend from invertebrates to vertebrates. 27 …”