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Increase in egg resistance to desiccation in springtails correlates with blastodermal cuticle formation : eco-evolutionary implications for insect terrestrialization
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Vargas, Helena Carolina Martins, Panfilio, Kristen A., Roelofs, Dick and Rezende, Gustavo Lazzaro (2021) Increase in egg resistance to desiccation in springtails correlates with blastodermal cuticle formation : eco-evolutionary implications for insect terrestrialization. Journal of experimental zoology. Part B, Molecular and developmental evolution, 336 (8). pp. 606-619. doi:10.1002/jez.b.22979 ISSN 1552-5015.
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Official URL: https://doi.org/10.1002/jez.b.22979
Abstract
Land colonization was a major event in the history of life. Among animals, insects exerted a staggering terrestrialization success, due to traits usually associated with postembryonic 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 noninsect 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 hr outside a humid environment, the survival period recorded for F. candida eggs is only 15 min, 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. [Abstract copyright: © 2020 Wiley Periodicals LLC.]
Item Type: | Journal Article | |||||||||
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Subjects: | Q Science > QL Zoology S Agriculture > SF Animal culture |
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Divisions: | Faculty of Science, Engineering and Medicine > Science > Life Sciences (2010- ) | |||||||||
SWORD Depositor: | Library Publications Router | |||||||||
Library of Congress Subject Headings (LCSH): | Blastoderm, Embryology, Collembola , Arid regions, Colonization (Ecology) | |||||||||
Journal or Publication Title: | Journal of experimental zoology. Part B, Molecular and developmental evolution | |||||||||
Publisher: | Wiley-Blackwell Publishing Ltd. | |||||||||
ISSN: | 1552-5015 | |||||||||
Official Date: | December 2021 | |||||||||
Dates: |
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Volume: | 336 | |||||||||
Number: | 8 | |||||||||
Page Range: | pp. 606-619 | |||||||||
DOI: | 10.1002/jez.b.22979 | |||||||||
Status: | Peer Reviewed | |||||||||
Publication Status: | Published | |||||||||
Reuse Statement (publisher, data, author rights): | "This is the peer reviewed version of the following article: Vargas, HCM, Panfilio, KA, Roelofs, D, Rezende, GL. Increase in egg resistance to desiccation in springtails correlates with blastodermal cuticle formation: Eco‐evolutionary implications for insect terrestrialization. J Exp Zool (Mol Dev Evol). 2020; 1– 14., which has been published in final form at https://doi.org/10.1002/jez.b.22979. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions." | |||||||||
Access rights to Published version: | Restricted or Subscription Access | |||||||||
Date of first compliant deposit: | 30 July 2020 | |||||||||
Date of first compliant Open Access: | 10 July 2021 | |||||||||
RIOXX Funder/Project Grant: |
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