Immune function of the serosa in hemimetabolous insect eggs

Abstract

Insects comprise more than a million species and many authors have attempted to explain this success by evolutionary innovations. A much overlooked evolutionary novelty of insects is the serosa, an extraembryonic epithelium around the yolk and embryo. We have shown previously that this epithelium provides innate immune protection to eggs of the beetle Tribolium castaneum. It remained elusive, however, whether this immune competence evolved in the Tribolium lineage or is ancestral to all insects. Here, we expand our studies to two hemimetabolous insects, the bug Oncopeltus fasciatus and the swarming grasshopper Locusta migratoria . For Oncopeltus , RNA sequencing reveals an extensive response upon infection, including the massive upregulation of antimicrobial peptides (AMPs). We demonstrate antimicrobial activity of these peptides using in vitro bacterial growth assays and describe two novel AMP families called Serosins and Ovicins. For both insects, quantitative polymerase chain reaction shows immune competence of the eggs when the serosa is present, and in situ hybridizations demonstrate that immune gene expression is localized in the serosa. This first evidence from hemimetabolous insect eggs suggests that immune competence is an ancestral property of the serosa. The evolutionary origin of the serosa with its immune function might have facilitated the spectacular radiation of the insects. This article is part of the theme issue ‘Extraembryonic tissues: exploring concepts, definitions and functions across the animal kingdom’.

Diversity, duplication, and genomic organization of homeobox genes in Lepidoptera

“…In other gene families, large changes in copy number have been found to be adaptive and related to certain environments or behaviors ( Briscoe et al 2013 ; Cheng et al 2017 ; Rane et al 2019 ; Chakraborty et al 2021 ). The Shx genes are expressed in the serosa during development, an extraembryonic tissue implicated in innate immunity and desiccation resistance in insects ( Panfilio 2008 ; Jacobs et al 2013 , 2014 , 2022 ). It is therefore possible that Shx duplication is an adaptation associated with modifications to the egg, and indeed, many of the highly duplicated genes show increased rates of sequence evolution ( Fig.…”

The extended analogy of extraembryonic development in insects and amniotes

“…[48,51]). Downstream, RNA-seq after RNAi and pathogen-challenge studies have identified factors for serosal tissue maturation and physiology [24,55,56].…”

“…Many purported tissue-scale functions of polyploidy are probably applicable in this outer EE tissue. Serosal tissue integrity as a barrier epithelium of large cells confers cellular protection via detoxification [130] and innate immune responses to infection [55,56]. Furthermore, in many insect species, the serosa secretes a substantial cuticle that provides desiccation resistance [131][132][133] and mechanical protection [24].…”

Serine Protease Networks Mediate Immune Responses in Extra-Embryonic Tissues of Eggs in the Tobacco Hornworm, <b><i>Manduca sexta</i></b>

“…Although insect eggs are protected by the egg shell and the underlying vitelline membrane, they can be infected by pathogens through transovarial transmission or penetration of the eggshell [13,14]. Recent advances indicate that insect eggs can harbor endogenous immune defenses through the production of proteins by the serosa, an extra-embryonic tissue [15,16]. However, the serosa was secondarily lost in a group of derived flies (the Schizophora), which includes the wellstudied model insect D. melanogaster [17,18].…”