Abstract
Growing empirical evidence indicates that invertebrates become more resistant to a pathogen following initial exposure to a nonlethal dose; yet the generality, mechanisms, and adaptive value of such immune priming are still under debate. Because life-history theory predicts that immune priming and large investment in immunity should be more frequent in long-lived species, we here tested for immune priming and pathogen resistance in ant queens, which have extraordinarily long life span. We exposed virgin and mated queens of Lasius niger and Formica selysi to a low dose of the entomopathogenic fungus Beauveria bassiana, before challenging them with a high dose of the same pathogen. We found evidence for immune priming in naturally mated queens of L. niger. In contrast, we found no sign of priming in virgin queens of L. niger, nor in virgin or experimentally mated queens of F. selysi, which indicates that immune priming in ant queens varies according to mating status and mating conditions or species. In both ant species, mated queens showed higher pathogen resistance than virgin queens, which suggests that mating triggers an up-regulation of the immune system. Overall, mated ant queens combine high reproductive output, very long life span, and elevated investment in immune defense. Hence, ant queens are able to invest heavily in both reproduction and maintenance, which can be explained by the fact that mature queens will be protected and nourished by their worker offspring.
Highlights
Researchers have long believed that the immune system of invertebrates lacked memory and specificity (Rowley and Powell 2007)
We did not find evidence of immune priming in virgin queens of L. niger, as the exposure to a low dose of the fungus did not increase their resistance to the fungal challenge (Fig. 2B; Beauveria–Beauveria vs. Control–Beauveria, v2 = 0.38, d.f. = 1, P = 0.76)
We found evidence for immune priming in naturally mated queens of L. niger exposed to B. bassiana
Summary
Researchers have long believed that the immune system of invertebrates lacked memory and specificity (Rowley and Powell 2007). Immune priming has been found in insect species exposed to fungi (Rosengaus et al 1999), bacteria (Sadd and SchmidHempel 2006; Pham et al 2007; Rosengaus et al 2013), protozoa (Rodrigues et al 2010) and viruses (Tidbury et al 2011). Immune priming has recently been documented in ant larvae exposed to bacteria (Rosengaus et al 2013), but no priming was detected in adult workers of another ant species exposed to fungi (Reber and Chapuisat 2012a), in damselflies exposed to bacteria (Gonzalez-Tokman et al 2010), or in pea aphids exposed to bacterial immune elicitors (ter Braak et al 2013). In some cases, immune priming depended on the pathogen tested (Pham et al 2007)
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