Immune and environment‐driven gene expression during invasion: An eco‐immunological application of RNA‐Seq

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.

Flight capacity increases then declines from the core to the margins of an invasive species' range

“…While studies of cane toads have shown that traits may have curvilinear responses with distance along an invasion gradient [36][37][38], here, I provide a clear demonstration across two transects that the trait of dispersal capacity itself can have a nonlinear relationship with distance from the core and, thus, its characterization requires more than two observations (e.g. core versus frontline).…”

A comparison of nonlethal sampling methods for amphibian gut microbiome analyses

“…Morphological and physiological traits underlie this accelerated expansion, yet it is also clear that behavioural traits have evolved across this invasion; western cane toads exhibit bolder behaviour than eastern toads (Gruber et al, ). Notably, these changes have occurred despite low genetic diversity in Australian toads (Lillie, Shine, & Belov, ; Selechnik, Richardson, Shine, Brown, & Rollins, ; Slade & Moritz, ). Environmental and intrinsic factors (e.g., genetic components) that may affect behavioural traits have been previously studied (Rollins, Richardson, & Shine, ; Selechnik, Richardson, Shine, DeVore, et al, ; Urban et al, ).…”

“…Morphological and physiological traits underlie this accelerated expansion, yet it is also clear that behavioural traits have evolved across this invasion; western cane toads exhibit bolder behaviour than eastern toads (Gruber et al, 2017). Notably, these changes have occurred despite low genetic diversity in Australian toads (Lillie, Shine, & Belov, 2014;Selechnik, Richardson, Shine, Brown, & Rollins, 2019;Slade & Moritz, 1998).…”

Host defense or parasite cue: Skin secretions mediate interactions between amphibians and their parasites

“…Conversely, at the invasion‐front, where there is a strong evolutionary pressure for dispersal ability via both natural selection and spatial sorting (Brown et al, 2014; Phillips & Perkins, 2019), increased host resistance might be favoured if parasite infection reduces dispersal ability. Moreover, some sets of immune genes are upregulated at the invasion‐front (Selechnik et al, 2019a), suggesting that heightened, possibly non‐specific, immune responses arising from exposure to other pathogens or conditions at the invasion‐front may increase resistance of toads (Brown et al, 2018; Mayer et al, 2021). This hypothesis is supported by the reduced longevity of larvae when exposed to skin secretions of toads from the invasion‐front.…”