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

Abstract

Land colonization was a major event in the history of life. Among animals, insects had 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 tenvironments 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. Physiological assays showed that blastodermal cuticle formation supports 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 protective cuticle is an ancestral trait among hexapods, predating and facilitating the process of terrestrialization that occurred during insect evolution.

Review of extra-embryonic tissues in the closest arthropod relatives, onychophorans and tardigrades

“…In arthropods and amniotes, it has been suggested that the presence of specialized extra-embryonic tissues is correlated with terrestrialization and egg deposition in corresponding habitats [3,13,74,75]. Extra-embryonic tissues surrounding the developing embryo might serve as a protective barrier against mechanical stress and desiccation and, thus, allowed arthropods and amniotes to conquer new habitats [3,13,74,75].…”

“…In arthropods and amniotes, it has been suggested that the presence of specialized extra-embryonic tissues is correlated with terrestrialization and egg deposition in corresponding habitats [3,13,74,75]. Extra-embryonic tissues surrounding the developing embryo might serve as a protective barrier against mechanical stress and desiccation and, thus, allowed arthropods and amniotes to conquer new habitats [3,13,74,75]. On the other hand, while onychophorans are exclusively terrestrial, they are all confined to humid microhabitats irrespective of their developmental mode or specific distribution (figure 2 A,B ; [9,38,39]).…”

The extended analogy of extraembryonic development in insects and amniotes

“…That both crickets and chickens, and mosquitoes and mice, develop within a fluid-filled amniotic cavity represents a convergent solution to common challenges, including the demands of a fully terrestrial lifestyle. Adaptations of the egg to prevent desiccation, chiefly including the EE tissues, have enabled insects and amniotes to colonize diverse ecological niches away from the aquatic and humid habitats to which species such as amphibians and springtails are constrained [7,8].…”