Drosophila larvae and adults possess a potent innate immune response, but the response of Drosophila eggs is poor. In contrast to Drosophila, eggs of the beetle Tribolium are protected by a serosa, ...an extraembryonic epithelium that is present in all insects except higher flies. In this study, we test a possible immune function of this frontier epithelium using Tc-zen1 RNAi-mediated deletion. First, we show that bacteria propagate twice as fast in serosa-less eggs. Then, we compare the complete transcriptomes of wild-type, control RNAi, and Tc-zen1 RNAi eggs before and after sterile or septic injury. Infection induces genes involved in Toll and IMD-signaling, melanisation, production of reactive oxygen species and antimicrobial peptides in wild-type eggs but not in serosa-less eggs. Finally, we demonstrate constitutive and induced immune gene expression in the serosal epithelium using in situ hybridization. We conclude that the serosa provides insect eggs with a full-range innate immune response.
Immune function of the serosa in hemimetabolous insect eggs Jacobs, Chris G C; van der Hulst, Remy; Chen, Yen-Ta ...
Philosophical transactions of the Royal Society of London. Series B. Biological sciences,
12/2022, Letnik:
377, Številka:
1865
Journal Article
Recenzirano
Odprti dostop
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
It remained elusive, however, whether this immune competence evolved in the
lineage or is ancestral to all insects. Here, we expand our studies to two hemimetabolous insects, the bug
and the swarming grasshopper
. For
, RNA sequencing reveals an extensive response upon infection, including the massive upregulation of antimicrobial peptides (AMPs). We demonstrate antimicrobial activity of these peptides using
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
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'.
The burying beetle Nicrophorus vespilloides has emerged as a model system for the investigation of adaptations that allow the utilization of carrion as a diet and as a resource for reproduction. The ...survival of beetles and their offspring given their exposure to soil-dwelling and cadaver-borne microbes requires mechanisms that reduce bacterial contamination in the diet and that achieve sanitation of the microhabitat. To explore the role of antimicrobial peptides (AMPs) in this context, we analyzed burying beetle males and females at different stages of their breeding cycle using the RNA-Seq and proteomics approaches. To address variation in immune functions, we investigated the impact of adult sex, the presence or absence of offspring (social context), and the presence of carrion (environmental context) on the expression of the identified immune effector genes. We found that particular AMPs are sex-specific and tightly regulated by the presence of a carcass or offspring and identified the two most context-dependent antimicrobial proteins in anal secretions. The context-specific expression dynamics of particular AMPs and lysozymes reveals a complex regulatory system, reflecting adaptations to specific ecological niches. This study highlights how burying beetles cope with microorganisms found on carrion and identifies candidates for both internal and external immunity.
•Eggs of the beetle Tribolium can mount an immune response comparable to adults.•Antimicrobial peptides (AMPs) are weakly upregulated in challenged eggs of Drosophila.•Tribolium eggs possess an ...extraembryonic serosa in contrast to Drosophila.•Serosa-less Tribolium eggs reveal little upregulation of AMPs upon infection.•The serosa plays a crucial role in the immune response of Tribolium castaneum eggs.
Innate immunity is common to all metazoans and serves as a first line of defense against pathogens. Although the immune response of adult and larval insects has been well characterized, it remains unknown whether the insect egg is able to mount an immune response. Contrary to Drosophila, Tribolium eggs develop an extraembryonic epithelium, the serosa. Epithelia are well known for their ability to fight infection, so the serosa has the potential to protect the embryo against pathogens. To test this hypothesis we created serosa-less eggs by Tc-zen1 parental RNAi. We found that the Tribolium egg upregulates several immune genes to comparable levels as adults in response to infection. Drosophila eggs and serosa-less Tribolium eggs, however, show little to no upregulation of any of the tested immune genes. We conclude that the extraembryonic serosa is crucial for the early immune competence of the Tribolium egg.
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 zerknüllt1 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 knock-down 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.
National city ranks do not describe a settlement's local and regional relevance adequately. We introduce a method to rank settlements' centrality based on travel time and settlement size. We ...investigate the relationship between a settlement's size, whether it is a local or regional centre, and its service endowment. The approach explains per capita service endowments in Europe well, adding nuances that national rankings do not fully capture. In addition, it establishes a characterization of service types by empirically discernible preferences in spatial scale. Finally, results suggest that service endowment in settlements can be reshuffled because of faster road connections, with services spatially concentrating in better connected areas.
Resumen
Las clasificaciones nacionales de ciudades no describen adecuadamente la relevancia local y regional de una población. Este estudio introduce un método para clasificar la importancia de las poblaciones en función del tiempo de viaje y el tamaño de la población. Se investigó la relación entre el tamaño de una población, si es un centro local o regional, y su dotación de servicios. El enfoque explica adecuadamente las dotaciones de servicios per cápita en Europa y añade matices que las clasificaciones nacionales no captan plenamente. Además, establece una caracterización de los tipos de servicio por preferencias discernibles empíricamente en la escala espacial. Por último, los resultados sugieren que la dotación de servicios en las poblaciones puede reorganizarse debido a la mayor rapidez de las conexiones por carretera, con servicios que se concentran espacialmente en las zonas mejor conectadas.
抄録
国の都市ランキングは、集落の地域的な重要性を適切に説明するものではない。移動時間と集落の規模に基づいて集落の中心性をランク付けする手法を導入した。地域の中心であるか否かにかかわらず、集落の規模とサービスエンダウメントとの関係を調査する。このアプローチは、ヨーロッパの一人当たりのサービスエンダウメントをうまく説明するもので、国別ランキングでは完全には捉えきれていない微妙な部分が示される。さらに、空間スケールで経験的に認識できる選好性によってサービスタイプの特性評価を確立する。結論として、結果からに集落のサービスエンダウメントはより速い道路接続によって刷新されることが可能であり、サービスはより良い道路接続の地域に空間的に集中することが示唆される。
Insects have been extraordinary successful in colonizing terrestrial habitats and this success is partly due to a protective cuticle that mainly contains chitin and proteins. The cuticle has been ...well studied in larvae and adults, but little attention has been paid to the cuticle of the egg. This cuticle is secreted by the serosa, an extraembryonic epithelium that surrounds the yolk and embryo in all insect eggs, but was lost in the Schizophoran flies to which Drosophila belongs. We therefore set out to investigate serosal cuticle formation and function in a beetle (Tribolium castaneum) using RNAi-mediated knockdown of three candidate genes known to structure chitin in the adult cuticle, and we aimed to identify other serosal cuticle genes using RNA sequencing. Knockdown of Knickkopf (TcKnk-1) or Retroactive (TcRtv) affects the laminar structure of the serosal cuticle, as revealed by Transmission Electron Microscopy in knockdown eggs. In the absence of this laminar structure, significantly fewer eggs survive at low humidity compared to wild-type eggs. Survival in dry conditions is also adversely affected when cross-linking among proteins and chitin is prevented by Laccase2 (TcLac-2) RNAi. Finally, we compare the transcriptomes of wild-type eggs to serosa-less eggs and find serosa-biased expression of 21 cuticle-related genes including structural components, chitin deacetylases and chitinases. Our data indicate that the serosal cuticle utilizes the same machinery for structuring the cuticle as adults. We demonstrate that the structure of the cuticle is crucial for desiccation resistance, and we put forward the serosal cuticle of Tribolium as an excellent model to study the ecological properties of the insect cuticle.
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•The insect egg is known to be protected against dehydration by the serosal cuticle.•Knickkopf1, Retroactive and Laccase2 are involved in structuring the serosal cuticle.•TcKnk-1, TcRtv or TcLac-2 knockdown reduces survival of eggs at dry conditions.•Many cuticle genes show serosa specific expression.•The Tribolium egg provides a model for the study of cuticle synthesis.
In order to survive microbe encounters, insects rely on both physical barriers as well as local and systemic immune responses. Most research focusses on adult or larval defenses however, whereas ...insect eggs are also in need of protection. Lately, the defense of eggs against microbes has received an increasing amount of attention, be it through endogenous egg defenses, trans-generational immune priming (TGIP) or parental investment. Here we studied the endogenous immune response in eggs and adults of Tenebrio molitor. We show that many immune genes are induced in both adults and eggs. Furthermore, we show that eggs reach comparable levels of immune gene expression as adults. These findings show that the eggs of Tenebrio are capable of an impressive endogenous immune response, and indicate that such inducible egg defenses are likely common in insects.
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•Eggs of Tenebrio molitor induce multiple immune genes upon infection.•The same immune genes are induced in adults and eggs of T. molitor.•Transcript levels in eggs come close to those in adult beetles.•Endogenous egg defenses are likely important for many insect species.
Understanding uncertainties in land cover projections is critical to investigating land‐based climate mitigation policies, assessing the potential of climate adaptation strategies and quantifying the ...impacts of land cover change on the climate system. Here, we identify and quantify uncertainties in global and European land cover projections over a diverse range of model types and scenarios, extending the analysis beyond the agro‐economic models included in previous comparisons. The results from 75 simulations over 18 models are analysed and show a large range in land cover area projections, with the highest variability occurring in future cropland areas. We demonstrate systematic differences in land cover areas associated with the characteristics of the modelling approach, which is at least as great as the differences attributed to the scenario variations. The results lead us to conclude that a higher degree of uncertainty exists in land use projections than currently included in climate or earth system projections. To account for land use uncertainty, it is recommended to use a diverse set of models and approaches when assessing the potential impacts of land cover change on future climate. Additionally, further work is needed to better understand the assumptions driving land use model results and reveal the causes of uncertainty in more depth, to help reduce model uncertainty and improve the projections of land cover.
Cytonuclear discordance in contact zones between related lineages is common, with mitochondrial clines often being displaced from clines in nuclear allele frequency. Proposed explanations for such a ...pattern include adaptive introgression of mtDNA or a neutral wake of mtDNA being left behind following hybrid zone movement. However, studies investigating these hypotheses are rare. Our previous survey of genetic variation in the long‐toed salamander (Ambystoma macrodactylum) highlighted a potential case of cytonuclear discordance between two lineages in western Canada. Here, we use additional markers and samples to clarify the extent of this discordance. We simultaneously assess the feeding performance of individuals in a common environment to test for an association between mitotype and individual performance. The genetic results confirm a general pattern of cytonuclear discordance in the focal region. However, we also observed more limited introgression of a diagnostic nuclear marker. Intriguingly, although there were differences in individual performance associated with the transition between mitotypes, these differences were not fully explained by mitotype. Instead, the lowest performance was observed in individuals demonstrating the greatest mismatch between mtDNA and all nuclear markers, suggesting the potential for cytonuclear incompatibilities to be acting. These results highlight the complexity of understanding the causes and consequences of mtDNA introgression and cytonuclear discordance in contact zones.
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