The extraembryonic serosa protects the insect egg against desiccation

Abstract

Insects have been extraordinarily successful in occupying terrestrial habitats, in contrast to their mostly aquatic sister group, the crustaceans. This success is typically attributed to adult traits such as flight, whereas little attention has been paid to adaptation of the egg. An evolutionary novelty of insect eggs is the serosa, an extraembryonic membrane that enfolds the embryo and secretes a cuticle. To experimentally test the protective function of the serosa, we exploit an exceptional possibility to eliminate this membrane by zerknü llt1 RNAi in the beetle Tribolium castaneum. We analyse hatching rates of eggs under a range of humidities and find dramatically decreasing hatching rates with decreasing humidities for serosa-less eggs, but not for control eggs. Furthermore, we show serosal expression of Tc-chitin-synthase1 and demonstrate that its knockdown leads to absence of the serosal cuticle and a reduction in hatching rates at low humidities. These developmental genetic techniques in combination with ecological testing provide experimental evidence for a crucial role of the serosa in desiccation resistance. We propose that the origin of this extraembryonic membrane facilitated the spectacular radiation of insects on land, as did the origin of the amniote egg in the terrestrial invasion of vertebrates.

Novel functions for Dorsocross in epithelial morphogenesis in the beetle Tribolium castaneum

“…8D-F, schematic). While the amnion then extends with the embryo, the serosa remains largely static under the eggshell, to which it becomes attached through its secreted cuticle (Hilbrant et al, 2016;Jacobs et al, 2013). After Tc-Doc RNAi, serosal window closure often does not occur ( Fig.…”

“…In order to first provide protection to the embryo in the form of desiccation resistance (Goltsev et al, 2009;Jacobs et al, 2013;Vargas et al, 2014) and defense against pathogens (Jacobs et al, 2014), and later to leave the embryo uncovered, they perform a wide array of morphogenetic rearrangements. The degree to which EE reorganization affects the embryo ranges from small-scale effects on germ band extension and retraction in Drosophila (e.g.…”

A limit on the extent to which increased egg size can compensate for a poor postnatal environment revealed experimentally in the burying beetle, Nicrophorus vespilloides

“…In N. vespilloides , egg size might function primarily to confer resistance to desiccation (Jacobs et al. 2013). Casual observation suggests that humidity levels in our laboratory breeding boxes are generally high, whether or not parents provide postnatal care.…”

Triboliumembryo morphogenesis

“…25 Recent experiments suggest that the extra-embryonic serosa is an evolutionary novelty of insect eggs to protect them against desiccation. 34 But does it play an active role during early embryonic morphogenesis? While it is still an open question whether initiation of serosa expansion is an active process or merely a consequence of tensile forces exerted by the contracting embryonic rudiment, our Tribolium imaging studies suggested that the serosa is needed during the later stages of epithelial rearrangement.…”