Immune priming depends on age, sex and Wolbachia in the interaction between Armadillidium vulgare and Salmonella

Abstract

The protection conferred by a first infection upon a second pathogenic exposure (i.e. immune priming) is an emergent research topic in the field of invertebrate immunity. Immune priming has been demonstrated in various species, but little is known about the intrinsic factors that may influence this immune process. In this study, we tested whether age, gender and the symbiotic bacterium Wolbachia affect the protection resulting from immune priming in A. vulgare against S. enterica. We firstly primed young and old, symbiotic and asymbiotic males and females, either with a non‐lethal low dose of S. enterica, LB broth or without injection (control). Seven days post‐injection, we performed a LD50 injection of S. enterica in all individuals and we monitored their survival rates. We demonstrated that survival capacities depend on these three factors: young and old asymbiotic individuals (males and females) expressed immune priming (S. enterica‐primed individuals survived better than LB‐primed and non‐primed), with a general decline in the strength of protection in old females, but not in old males, compared to young. When Wolbachia is present, the immune priming protection was observed in old, but not in young symbiotic individuals, even if the Wolbachia load on entire individuals is equivalent regardless to age. Our overall results showed that the immune priming protection in A. vulgare depends on individuals’ states, highlighting the need to consider these factors both in mechanistical and evolutionary studies focusing on invertebrate's immunity.

Immune priming in Armadillidium vulgare against Salmonella enterica: direct or indirect costs on life history traits?

“…As expected, we showed a protective effect of immune priming on female survival rates: the first encounter with S. enterica improves survival ability of females after the second and lethal infection, confirming previous results described in Prigot-Maurice et al (2019 , 2021 ). In surviving females, we showed a negative effect of immune priming on body weight of females (Fig.…”

“…Among the numerous species in which immune priming has been observed, the common woodlouse Armadillidium vulgare ( Oniscidea , Isopoda , Crustacea ) is an appropriate model to investigate this issue. Armadillidium vulgare (Latreille, 1804) mount an immune priming response with two subsequent infections of living Salmonella enterica (Theobald Smith, 1855) injected seven days apart ( Prigot-Maurice et al 2019 , 2021 ). The underlying mechanism is expected to be a sustained immune response of primed individuals, which display long-lasting, higher viability of haemocytes compared to non-primed individuals ( Prigot-Maurice et al 2019 ).…”

Environmental variability affects optimal trade‐offs in ecological immunology

“…When we modeled the investment strategy as a function of time, either as a polynomial or as a bang‐bang control, we again found that the optimal investment function was dependent on the amount of environmental variability experienced by the host. Our results add to the growing number of studies exploring the causes and consequences of variation in host immunity (e.g., Rolff and Siva‐Jothy 2002, Zuk and Stoehr 2002, Lazzaro and Little 2009, Boots et al 2013, Metcalf et al 2017, Zeller and Koella 2017, Metcalf and Graham 2018, Ben‐Ami 2019, McNew et al 2019, Izhar et al 2020, Prigot‐Maurice et al 2020) by illustrating that environmental variability can impact optimal ecological immunology strategies despite not affecting mean host lifespan.…”