Friend or foe? The apparent benefits of gregarine (Apicomplexa: Sporozoa) infection in the European earwig

Arcila, Francisco; Meunier, Joël

doi:10.1016/j.ijpara.2020.01.007

Cited by 20 publications

(26 citation statements)

References 77 publications

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“…This absence of a link between rifampicin and maternal care may first suggest that earwig parental care is shaped by microbes that are non-sensitive to rifampicin. In insects, gut microbial communities do not only encompass a broad diversity of bacteria (among which some are resistant to rifampicin) but also fungi, protists and other microorganisms that could have key roles in hosts biology [41,64,65]. Even if the previous experimental works linking gut microbiota and host sociality focused on bacteria [17–21], future studies will be required to confirm that no other members of the gut microbiota shape parental care in our study species.…”

Section: Discussionmentioning

confidence: 99%

“…This may first suggest that earwig parental care is primarily shaped by microbes that are non-sensitive to rifampicin or that non-sensitive microbes can take over this function (functional redundancy). In insects, gut microbial communities do not only encompass a broad diversity of bacteria (among which some are resistant to rifampicin) but also fungi, protists and other microorganisms that could have key roles and functional redundancies in hosts biology [37,60]. Even if the previous experimental studies linking gut microbiota and host sociality focused on bacteria [15–17,19,20], future studies will be required to confirm that no other members of the gut microbiota shape parental care in our study species, and to explore causal links between the presence of certain members of the microbiome and the level of maternal care expressed by its host.…”

Section: Methodsmentioning

confidence: 99%

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Alteration of gut microbiota with a broad-spectrum antibiotic does not impair maternal care in the European earwig

Meyel

Devers

Dupont

et al. 2020

Preprint

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The microbes residing within the gut of an animal host often maximise their own fitness by modifying their host’s physiological, reproductive, and behavioural functions. Whereas recent studies suggest that they may also shape host sociality and therefore have critical effects on animal social evolution, the impact of the gut microbiota on maternal care remains unexplored. This is surprising, as this social behaviour is widespread among animals, often determines the fitness of both juveniles and parents, and is essential in the evolution of complex animal societies. Here, we address this gap in knowledge by testing whether life-long alterations of the gut microbiota with rifampicin - a broad-spectrum antibiotic - impair the expression of pre- and post-hatching maternal care in the European earwig, an insect exhibiting extensive forms of maternal care towards eggs and juveniles. Our results first confirm that rifampicin altered the mothers’ gut microbial communities and revealed that the composition of the gut microbiota differs before and after egg care. Contrary to our predictions, however, the rifampicin-induced alterations of the gut microbiota did not modify the expression of pre- or post-hatching care. Independent of maternal care, rifampicin increased the females’ feces production and resulted in lighter eggs and juveniles. By contrast, rifampicin altered none of the other 23 physiological, reproductive and longevity traits measured over the females’ lifetime. Overall, these findings reveal that altering the gut microbiota does not necessarily affect host sociality. More generally, our results emphasize that not all animals have evolved a co-dependence with their microbiota.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Alteration of gut microbiota with a broad-spectrum antibiotic does not impair maternal care in the European earwig

Meyel

Devers

Dupont

et al. 2020

Preprint

Self Cite

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“…One day later (i.e. day 6 after egg hatching), each nymph was exposed to either one of four pathogen suspensions or one of two control solutions using a protocol adapted from fungal exposures of adult earwigs (Arcila and Meunier, 2020;Kohlmeier et al, 2016). Each nymph was first gently deposited on a filter paper (Macherey-Nagel GmbH & Co. KG, Düren, Germany), then covered with 100 µL of either a conidiospore suspension of M. brunneum diluted in 0.05% Tween 20 at a concentration of 10 4 (n= 33), 10 5 (n= 35), 10 6 (n= 35) or 10 7 (n= 34) spores/ml, with 100 µL of a control spore-free solution of either 0.05% Tween 20 (n = 35; Sigma P-1379) or control water solution (n = 35).…”

Section: Methodsmentioning

confidence: 99%

“…We then maintained these juveniles at either 20°C or 24°C and subsequently recorded the days of moult to 3 rd instar and the day of death for the next 20 dayswithout providing food during this period. M. brunneum (formerly M. anisopliae) is a natural and lethal pathogen of F. auricularia (Arcila and Meunier, 2020;Günther and Herter, 1974;Kohlmeier et al, 2016;Körner et al, 2020;Vogelweith et al, 2017) for which the optimal temperatures of infections typically range between 20 and 30°C, with an optimum around 25°C (Arthurs and Thomas, 2001).…”

Section: Introductionmentioning

confidence: 99%

Effects of temperature, fungal infection and weight on intermoult duration and survival of starving earwig larvae

Coulm

Meunier

2021

Journal of Insect Physiology

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Moulting is a cornerstone of arthropods development. It can be determined by numerous factors such as body mass, temperature, and immunity. However, the effects of these factors can be dependent on each other, so that it is often difficult to predict whether and how they shape moulting, and whether their effects are additive or interactive. In this study, we addressed these questions by testing the effects of body mass, ambient temperature, fungal infection and their interaction on intermoult duration and survival in starved juveniles of the European earwig Forficula auricularia. We recorded the date of moult and death of a total of 207 earwig juveniles that were weighed, exposed to different doses of the entomopathogenic fungus Metarizium brunneum and then maintained at either 20°C or 24°C. Our results first reveal that juveniles moulted earlier when they were heavy compared to light on the day of exposure, as well as earlier when maintained at 24°C compared to 20°C. By contrast, pathogen exposure did not affect the moulting date. We also found that nymphs died faster when they were light compared to heavy on the day of exposure, when they were exposed to high (10 6 and 10 7 spores/ml) compared to low (10 4 , 10 5 and 0 spores/ml) pathogen concentrations, and when they were maintained at 24°C compared to 20°C. We detected no sign of interaction between temperature, fungal infection and body mass on both moulting and survival. Overall, these findings shed light on the limited importance of infection on moulting in starved juveniles, and reveal that weight, temperature, and infection have additive effects on their survival. More generally, this study emphasizes that the three tested factors do not necessarily interact to shape key physiological processes in an insect.

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“…We used standard protocols to test the effects of rifampicin on 7 proxies of female physiology, as well as 16 proxies of female reproduction and female longevity (Körner et al., 2016; Meunier et al., 2012). Proxies of females’ physiology were the number of faeces pellets produced per 24 hr (a number positively associated with their digestive/foraging activity (Arcila & Meunier, 2020)) and the gain in fresh weight between two life stages. Faeces production was measured two months after the beginning of the treatments.…”

Section: Methodsmentioning

confidence: 99%

Alteration of gut microbiota with a broad‐spectrum antibiotic does not impair maternal care in the European earwig

Meyel

Devers

Dupont

et al. 2021

J of Evolutionary Biology

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The microbes residing within the gut of an animal host often increase their own fitness by modifying their host's physiological, reproductive, and behavioural functions. Whereas recent studies suggest that they may also shape host sociality and therefore have critical effects on animal social evolution, the impact of the gut microbiota on maternal care remains unexplored. This is surprising, as this behaviour is widespread among animals, often determines the fitness of both juveniles and parents, and is essential in the evolution of complex animal societies. Here, we tested whether life-long alterations of the gut microbiota with rifampicin -a broad-spectrum antibiotic -impair pre-and post-hatching maternal care in the European earwig. Our results first confirm that rifampicin altered the mothers' gut microbial communities and indicate that the composition of the gut microbiota differs before and after egg care. Contrary to our predictions, however, the rifampicin-induced alterations of the gut microbiota did not modify pre-or post-hatching care. Independent of maternal care, rifampicin increased the females' feces production and resulted in lighter eggs and juveniles. By contrast, rifampicin altered none of the other 21 physiological, reproductive and longevity traits measured over the 300 days of a female's lifetime. Overall, these findings reveal that altering the gut microbiota with a large spectrum antibiotic such as rifampicin does not necessarily affect host sociality. They also emphasize that not all animals have evolved a co-dependence with their microbiota and call for caution when generalizing the central role of gut microbes in host biology.

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Friend or foe? The apparent benefits of gregarine (Apicomplexa: Sporozoa) infection in the European earwig

Cited by 20 publications

References 77 publications

Alteration of gut microbiota with a broad-spectrum antibiotic does not impair maternal care in the European earwig

Alteration of gut microbiota with a broad-spectrum antibiotic does not impair maternal care in the European earwig

Effects of temperature, fungal infection and weight on intermoult duration and survival of starving earwig larvae

Alteration of gut microbiota with a broad‐spectrum antibiotic does not impair maternal care in the European earwig

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