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

Abstract

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.

Broad Concordance in the Spatial Distribution of Adaptive and Neutral Genetic Variation across an Elevational Gradient in Deer Mice

“…In the field, we live-trapped deer mice using baited Sherman traps. We also used liver samples from euthanized mice, and blood or tail clip samples from mice that were part of a mark-recapture study (e.g., Wilde et al 2019 ), in which individuals were released after capture. To augment our sample sizes for some sites, we used tissue samples from previously collected museum specimens that are cataloged in the mammal collections of the Denver Museum of Nature and Science, the University of Arizona Museum of Natural History Museum, the Museum of Vertebrate Zoology, and the Museum of Southwestern Biology (see Natarajan et al 2015 ).…”

“…Deer mice native to high elevations in the Rocky Mountains have evolved a suite of physiological changes that contribute to adaptive enhancements of whole-animal aerobic performance in hypoxia ( fig. 1 ; Cheviron et al 2012 , 2013 , 2014 ; Lui et al 2015 ; Ivy and Scott 2017 , 2018 ; Lau et al 2017 ; Dawson et al 2018 ; Scott et al 2015 ; Mahalingam et al 2017 , 2020 ; Nikel et al 2018 ; Tate et al 2017 ; Storz et al 2019 ), a trait that influences survival in this species ( Hayes and O’Connor 1999 ; Wilde et al 2019 ).…”

Haemosporidian infection does not alter aerobic performance in the Pink-sided Junco (Junco hyemalis mearnsi)

“…We are not aware of any other studies that have investigated relationships between aerobic scope and either parasite infection (of any kind) in birds or haemosporidian infection in non-avian hosts. However, other parasitic infections are associated with declines in aerobic scope in several non-avian systems (Kumaraguru et al 1995, Careau et al 2012, Bruneaux et al 2017, Hvas et al 2017, Wilde et al 2019). For example, Botfly ( Cuterebridae ) larval infection of deer mice ( Peromyscus maniculatus ) reduced host aerobic scope (via decreased summit metabolic rate) and was associated with lower host daily survival rates (Wilde et al 2019).…”

“…However, other parasitic infections are associated with declines in aerobic scope in several non-avian systems (Kumaraguru et al 1995, Careau et al 2012, Bruneaux et al 2017, Hvas et al 2017, Wilde et al 2019). For example, Botfly ( Cuterebridae ) larval infection of deer mice ( Peromyscus maniculatus ) reduced host aerobic scope (via decreased summit metabolic rate) and was associated with lower host daily survival rates (Wilde et al 2019). More studies characterizing the effects of parasites on aerobic scope are thus needed to test the generality of our findings in other birds.…”

Tick infestation effects on haemoglobin levels of deer mice (Peromyscus maniculatus)

“…fleas, mites) are consistently affecting the vulnerability of their host' immune response (Mize et al ., 2011), reducing the amount of iron in the blood due to constant blood loss (O'Brien et al ., 2003), which could cause an insufficient production of haemoglobin (Judy and Price, 1958; Andrews, 1997). Iron-deficient black rats ( Rattus rattus ) were found to be susceptible to infections of the pathogen Salmonella typhimurium (Baggs and Miller, 1973) and botfly infections can decrease haemoglobin levels in deer mice, potentially reducing their capacity for thermogenesis and aerobic performance (Wilde et al ., 2018). Investigating how ectoparasite feeding habits influence the haematology of deer mouse hosts – with and without the presence of ticks – will allow us to better understand how black-legged and American dog ticks may impact host populations as these ticks move northward (Leighton et al ., 2012).…”