Geographical variation in parasitism shapes larval immune function in a phytophagous insect

Abstract

Two of the central goals of immunoecology are to understand natural variation in the immune system among populations and to identify those selection pressures that shape immune traits. Maintenance of the immune system can be costly, and both food quality and parasitism selection pressure are factors potentially driving immunocompetence. In tritrophic interactions involving phytophagous insects, host plants, and natural enemies, the immunocompetence of phytophagous insects is constrained by selective forces from both the host plants and the natural enemies. Here, we assessed the roles of host plants and natural enemies as selective pressures on immune variation among natural populations of Lobesia botrana. Our results showed marked geographical variation in immune defenses and parasitism among different natural populations. Larval immune functions were dependent of the host plant quality and were positively correlated to parasitism, suggesting that parasitoids select for greater investment into immunity in moth. Furthermore, investment in immune defense was negatively correlated with body size, suggesting that it is metabolically expensive. The findings emphasize the roles of host plants and parasitoids as selective forces shaping host immune functions in natural conditions. We argue that kinds of study are central to understanding natural variations in immune functions, and the selective forces beyond.

Sources of variance in immunological traits: evidence of congruent latitudinal trends across species

“…Similar to our work, some previous studies using a damselfly and a ground cricket have found higher PO activity in higher latitude populations (De Block et al, 2008;Fedorka et al, 2013). Conversely, increased PO activity in the south has been reported in the European grapevine moth (Vogelweith et al, 2013b).…”

“…Indeed, lytic activity has previously been shown to vary less than PO activity, with the relative constancy having been primarily attributed to limited phenotypic plasticity in this trait (Triggs and Knell, 2012;McNamara et al, 2013a). Consistent with our observations on PP (but not the other two species), host plant has been shown to affect antimicrobial activity in a moth (Lobesia botrana; Vogelweith et al, 2013b) and lytic activity has been found to increase with temperature in Drosophila (Lazzaro et al, 2008;Fedorka et al, 2016). We are unaware of any studies showing among-population variation in lytic activity in insects, although a lack of variation has been reported for a crustacean (Daphnia magna; Mucklow et al, 2004).…”

“…Nevertheless, we note that such species-specific latitudinal differences are consistent with the frequently proposed crucial role of insect parasitoids as selective agents on immunological traits. Indeed, among-population differences in immunological indices have repeatedly been suggested to reflect adaptations to different rates of parasitism (Tinsley et al, 2006;Vogelweith et al, 2013b). If a major selective role of insect parasitoids was indeed the case, limited cross-species consistency in latitudinal trends of immunological traits should be the expected result.…”

“…In addition, even though it has been widely accepted that immunity bears costs (Luong and Polak, 2007;Iserbyt et al, 2012;Prokkola et al, 2013), we still do not sufficiently understand the nature of potential tradeoffs between immune function and life-history traits. In particular, it is unclear how general such trade-offs are across various species and environmental conditions (for case studies, see Diamond and Kingsolver, 2011;Vogelweith et al, 2013b).…”

A novel set of microsatellite markers for the European Grapevine MothLobesia botranaisolated using next-generation sequencing and their utility for genetic characterization of populations from Europe and the Middle East

“…In addition, L. botrana population densities vary from year to year in various viticultural areas probably related to climatic conditions and might also change within relatively short distances (Roehrich & Boller, 1991). Recently, Vogelweith et al (2013) demonstrated a marked geographical variation in immune defences and extent of parasitism among different natural L. botrana populations, again indicating the high potential of this species to adapt locally to different biotic and abiotic selective forces. All these aspects make L. botrana a suitable model species for understanding genetic mechanisms of both range expansion and adaptation to host plants and local abiotic factors.…”