Abstract
Host–pathogen associations change rapidly during a biological invasion and are predicted to impose strong selection on immune function. It has been proposed that the invader may experience an abrupt reduction in pathogen‐mediated selection (“enemy release”), thereby favoring decreased investment into “costly” immune responses. Across plants and animals, there is mixed support for this prediction. Pathogens are not the only form of selection imposed on invaders; differences in abiotic environmental conditions between native and introduced ranges are also expected to drive rapid evolution. Here, we use RNA‐Seq to assess the expression patterns of immune and environmentally associated genes in the cane toad (Rhinella marina) across its invasive Australian range. Transcripts encoding mediators of costly immune responses (inflammation, cytotoxicity) showed a curvilinear relationship with invasion history, with highest expression in toads from oldest and newest colonized areas. This pattern is surprising given theoretical expectations of density dynamics in invasive species and may be because density influences both intraspecific competition and parasite transmission, generating conflicting effects on the strength of immune responses. Alternatively, this expression pattern may be the result of other evolutionary forces, such as spatial sorting and genetic drift, working simultaneously with natural selection. Our findings do not support predictions about immune function based on the enemy release hypothesis and suggest instead that the effects of enemy release are difficult to isolate in wild populations, especially in the absence of information regarding parasite and pathogen infection. Additionally, expression patterns of genes underlying putatively environmentally associated traits are consistent with previous genetic studies, providing further support that Australian cane toads have adapted to novel abiotic challenges.
Highlights
Invasive species pose a massive threat to biodiversity (Bax et al, 2003; Clavero et al, 2009)
We examined the effects of range expansion on expression of immune and environmentally-associated genes in the invasive Australian cane toad (Rhinella marina) using
Spatial heterogeneity in pathogen pressure or environmental conditions may play a role in gene expression; parasite prevalence is generally higher in intermediate-age populations than in younger and older populations (Freeland et al, 1986), inconsistent with the general pattern for down-regulation of immune transcripts in toads from aCC-BY-ND 4.0 International license
Summary
Invasive species pose a massive threat to biodiversity (Bax et al, 2003; Clavero et al, 2009). Because of this, Lee & Klasing (2004) predict that invaders may down-regulate powerful immune responses such as systemic inflammation due to a decreased need (Cornet et al, 2016; Lee & Klasing, 2004; Martin et al, 2010) Such immune responses are costly due to energetic expenditure (the reduction of nutrients available for partitioning across tissues due to their use in mounting immune responses (Klasing & Leshchinsky, 1999)) and to the potential for collateral damage (tissue injury due to the effects of the immune response (Martin et al, 2010)). Invaders are predicted to exhibit lower investment in costly (but not all) immune responses than are seen in their native ranges (Cornet et al, 2016; Lee & Klasing, 2004)
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