Daily activity rhythms, sleep, and pregnancy are fundamentally related in the Pacific beetle mimic cockroach, Diploptera punctata

Abstract

Sleep and pregnancy are contentious bedfellows; sleep disorders and disturbances are associated with adverse pregnancy outcomes, although much is still unknown about this relationship. Sleep and pregnancy have been studied in many models, but most focus heavily on mammals. However, pregnancy is ubiquitous across the animal kingdom - a hallmark of convergent evolution; similarly sleep is a shared feature across diverse species. Here, we present an ideal model in which to study the dynamics between sleep and pregnancy in invertebrates. The Pacific beetle mimic cockroach, Diploptera punctata, is a viviparous cockroach species that uses milk proteins to nourish its young with a broodsac over a three month pregnancy. However, little is known about the relationship between this unique reproductive biology and daily rhythms of activity and sleep. We established that D. punctata displayed a peak in activity shortly following sunset, with males significantly more active than females. When scavenging behavior was examined, males and non-pregnant females emerged more often and traveled further from a shelter compared to pregnant females, suggesting reduced risk-taking behavior in late pregnancy. Chronic disturbance of sleep during pregnancy negatively impacted embryo development by increasing gestational duration and decreasing the transcription of milk proteins. These findings indicate that sleep is key to embryo development and that pregnancy has a significant impact on the daily rhythms of activity in Diploptera punctata. More broadly, we present a tractable invertebrate model for understanding the relationship between sleep and pregnancy, which will aid in the exploration of the poorly understood interface between these two ubiquitous and highly conserved traits.