Increase in egg resistance to desiccation in springtails correlates with blastodermal cuticle formation: eco-evolutionary implications for insect terrestrialization

Abstract

AbstractLand colonization was a major event in the history of life. Among animals, insects exerted a staggering terrestrialization success, due to traits usually associated with post-embryonic life stages, while the egg stage has been largely overlooked in comparative studies. In many insects, after blastoderm differentiation, the extraembryonic serosal tissue wraps the embryo and synthesizes the serosal cuticle, an extracellular matrix that lies beneath the eggshell and protects the egg against water loss. In contrast, in non-insect hexapods such as springtails (Collembola) the early blastodermal cells synthesize a blastodermal cuticle. Here, we investigate the relationship between blastodermal cuticle formation and egg resistance to desiccation in the springtails Orchesella cincta and Folsomia candida, two species with different oviposition environments and developmental rates. The blastodermal cuticle becomes externally visible in O. cincta and F. candida at 22 and 29% of embryogenesis, respectively. To contextualize, we describe the stages of springtail embryogenesis, exemplified by F. candida. Our physiological assays then showed that blastodermal cuticle formation coincides with an increase in egg viability in a dry environment, significantly contributing to hatching success. However, protection differs between species: while O. cincta eggs survive at least 2 hours outside a humid environment, the survival period recorded for F. candida eggs is only 15 minutes, which correlates with this species’ requirement for humid microhabitats. We suggest that the formation of this cuticle protects the eggs, constituting an ancestral trait among hexapods that predated and facilitated the process of terrestrialization that occurred during insect evolution.Research HighlightsThe formation of the blastodermal cuticle produced during early embryogenesis coincides with a higher protection against water loss in springtail (Collembola) eggs.Orchesella cincta eggs are more resistant to drought than Folsomia candida ones.The formation of a protective egg cuticle would be an ancestral trait among hexapods that facilitated their process of terrestrialization.Graphical AbstractGraphical Abstract legend: Eggs when laid uptake water but are also prone to water loss. Late eggs acquire some protection against water loss, but at different levels, depending on the species.