The costs of parasite infection: Effects of removing lungworms on performance, growth and survival of free‐ranging cane toads

Finnerty, Patrick B.; Shine, Richard; Brown, Gregory P.

doi:10.1111/1365-2435.12992

Cited by 45 publications

(52 citation statements)

References 66 publications

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“…Consistent with the ERH, many species of bacteria, protozoan, and metazoan parasites of cane toads have been left behind in the native range (Selechnik, Rollins, Brown, Kelehear, & Shine, 2017a). A major parasite (lungworm Rhabdias pseudosphaerocephala) from the native range that infects toad populations in the Australian range core is absent from toads at the invasion front (Phillips et al, 2010); this lungworm has been reported to increase mortality by 17% in metamorph cane toads (Kelehear, Webb, & Shine, 2009) and 6% in adult cane toads (Finnerty, Shine, & Brown, 2017). Conversely, the Australian soil bacterium Brucella (Ochrobactrum) anthropi causes spinal spondylosis in toads primarily at the invasion front (Brown, Shilton, Phillips, & Shine, 2007), which may represent a novel infection that forces invaders to remain immunocompetent.…”

Section: Introductionmentioning

confidence: 80%

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

Selechnik

Richardson

Shine

et al. 2019

Ecology and Evolution

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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.

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Section: Introductionmentioning

confidence: 80%

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

Selechnik

Richardson

Shine

et al. 2019

Ecology and Evolution

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“…Infection by a macroparasite—parasites with multiple life stages that do not multiply within their host—can influence the physiology and behaviour of a host (Burns, Goodwin, & Ostfeld, ; Finnerty, Shine, & Brown, ; Smith, ). These infections can also amplify the effects of other environmental stressors and affect host fitness (Gooderham & Schulte‐Hostedde, ; Juliana, Khokhlova, Wielebnowski, Kotler, & Krasnov, ).…”

Section: Introductionmentioning

confidence: 99%

Botfly infections impair the aerobic performance and survival of montane populations of deer mice, Peromyscus maniculatus rufinus

et al. 2019

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Elevations >2,000 m represent consistently harsh environments for small endotherms because of abiotic stressors such as cold temperatures and hypoxia. These environmental stressors may limit the ability of populations living at these elevations to respond to biotic selection pressures—such as parasites or pathogens—that in other environmental contexts would impose only minimal energetic‐ and fitness‐related costs. We studied deer mice (Peromyscus maniculatus rufinus) living along two elevational transects (2,300–4,400 m) in the Colorado Rockies and found that infection prevalence by botfly larvae (Cuterebridae) declined at higher elevations. We found no evidence of infections at elevations >2,400 m, but that 33.6% of all deer mice, and 52.2% of adults, were infected at elevations <2,400 m. Botfly infections were associated with reductions in haematocrit levels of 23%, haemoglobin concentrations of 27% and cold‐induced VO2max measures of 19% compared to uninfected individuals. In turn, these reductions in aerobic performance appeared to influence fitness, as infected individuals exhibited 19‐34% lower daily survival rates. In contrast to studies at lower elevations, we found evidence indicating that botfly infections influence the aerobic capabilities and fitness of deer mice living at elevations between 2,000 and 2,400 m. Our results therefore suggest that the interaction between botflies and small rodents is likely highly context‐dependent and that, more generally, high‐elevation populations may be susceptible to additional biotic selection pressures. A plain language summary is available for this article.

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“… These impacts are nonadaptive by‐products of illness; that is, they are part of a general “sickness behavior” syndrome (Kavaliers, Colwell, & Choleris, ; Klein, ). These lungworms do indeed induce such effects (Finnerty et al, ; Finnerty, P. B. ), but the specific changes examined in the current study seem unlikely to have arisen in this way.…”

Section: Discussionmentioning

confidence: 51%

“…By staying closer to a body of water and reducing movement, prey intake would be curtailed (Child, Phillips, Brown, & Shine, ). Combined with the costs of an upregulation of a host's immune system when parasitized (Finnerty, ), the adaptive manipulation of host behavior may have ramifications for a host's overall growth, performance, and viability (Finnerty et al, ; Finnerty, ).…”

Section: Discussionmentioning

confidence: 99%

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Survival of the feces: Does a nematode lungworm adaptively manipulate the behavior of its cane toad host?

Finnerty

Shine

Brown

2018

Ecology and Evolution

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Parasites can enhance their fitness by modifying the behavior of their hosts in ways that increase rates of production and transmission of parasite larvae. We used an antihelminthic drug to experimentally alter infections of lungworms (Rhabdias pseudosphaerocephala) in cane toads (Rhinella marina). We then compared subsequent behaviors of dewormed toads versus toads that retained infections. Both in the laboratory and in the field, the presence of parasites induced hosts to select higher body temperatures (thereby increasing rates of lungworm egg production), to defecate in moister sites, and to produce feces with higher moisture content (thereby enhancing survival of larvae shed in feces). Because those behavioral modifications enhance rather than decrease parasite fitness, they are likely to have arisen as adaptive manipulations of host behavior rather than as host adaptations to combat infection or as nonadaptive consequences of infection on host physiology. However, the mechanisms by which lungworms alter cane toad thermal preference and defecation are not known. Although many examples of host manipulation by parasites involve intermediate hosts facilitating their own demise, our findings indicate that manipulation of definitive hosts can be as subtle as when and where to defecate.

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The costs of parasite infection: Effects of removing lungworms on performance, growth and survival of free‐ranging cane toads

Cited by 45 publications

References 66 publications

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

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

Botfly infections impair the aerobic performance and survival of montane populations of deer mice, Peromyscus maniculatus rufinus

Survival of the feces: Does a nematode lungworm adaptively manipulate the behavior of its cane toad host?

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