scholarly journals Selection for increased mass-independent maximal metabolic rate suppresses innate but not adaptive immune function

2013 ◽  
Vol 280 (1754) ◽  
pp. 20122636 ◽  
Author(s):  
Cynthia J. Downs ◽  
Jessi L. Brown ◽  
Bernard Wone ◽  
Edward R. Donovan ◽  
Kenneth Hunter ◽  
...  

Both appropriate metabolic rates and sufficient immune function are essential for survival. Consequently, eco-immunologists have hypothesized that animals may experience trade-offs between metabolic rates and immune function. Previous work has focused on how basal metabolic rate (BMR) may trade-off with immune function, but maximal metabolic rate (MMR), the upper limit to aerobic activity, might also trade-off with immune function. We used mice artificially selected for high mass-independent MMR to test for trade-offs with immune function. We assessed (i) innate immune function by quantifying cytokine production in response to injection with lipopolysaccharide and (ii) adaptive immune function by measuring antibody production in response to injection with keyhole limpet haemocyanin. Selection for high mass-independent MMR suppressed innate immune function, but not adaptive immune function. However, analyses at the individual level also indicate a negative correlation between MMR and adaptive immune function. By contrast BMR did not affect immune function. Evolutionarily, natural selection may favour increasing MMR to enhance aerobic performance and endurance, but the benefits of high MMR may be offset by impaired immune function. This result could be important in understanding the selective factors acting on the evolution of metabolic rates.

1997 ◽  
Vol 273 (1) ◽  
pp. R337-R343 ◽  
Author(s):  
M. Konarzewski ◽  
B. Sadowski ◽  
I. Jozwik

The upper limits of metabolic rates and the links between maximal and resting metabolic rates in vertebrates have recently received a lot of attention, mainly due to their possible relationship to the evolution of endothermy. We measured peak metabolic rates during 3 min swimming in 20 degrees C water (Vo2swim), maximal metabolic rate (Vo2max) in -2.5 degrees C Helox, and basal metabolic rate (BMR) in two lines of mice selected for high (HA) and low (LA) swim stress-induced analgesia (SSIA). We found that exercise combined with heat loss used for producing SSIA also acted as a selection agent, resulting in a 15% HA/LA line difference in Vo2swim. Core body temperature of HA mice (characterized by lower Vo2swim) was also on average 3.2 degrees C lower than that of LA mice. Furthermore, Vo2max of HA mice was lower than that of LA mice by 8% and accompanied by larger hypothermia. Thus mice with exceptionally high (or low) Vo2max tended to have exceptionally high (or low) Vo2swim, resulting in a positive correlation between Vo2swim and Vo2max. All these suggest that selection for SSIA produced genetically correlated responses in both Vo2swim and Vo2max. However, we did not observe HA/LA differences in BMR. Hence, changes in resting and maximum metabolic rates are not necessarily correlated. We hypothesize that the lack of such a correlation was partially due to the modulation of metabolic responses by SSIA.


2011 ◽  
Vol 278 (1721) ◽  
pp. 3135-3141 ◽  
Author(s):  
Montserrat Gomendio ◽  
Maximiliano Tourmente ◽  
Eduardo R. S. Roldan

The hypothesis that sperm competition should favour increases in sperm size, because it results in faster swimming speeds, has received support from studies on many taxa, but remains contentious for mammals. We suggest that this may be because mammalian lineages respond differently to sexual selection, owing to major differences in body size, which are associated with differences in mass-specific metabolic rate. Recent evidence suggests that cellular metabolic rate also scales with body size, so that small mammals have cells that process energy and resources from the environment at a faster rate. We develop the ‘metabolic rate constraint hypothesis’ which proposes that low mass-specific metabolic rate among large mammals may limit their ability to respond to sexual selection by increasing sperm size, while this constraint does not exist among small mammals. Here we show that among rodents, which have high mass-specific metabolic rates, sperm size increases under sperm competition, reaching the longest sperm sizes found in eutherian mammals. By contrast, mammalian lineages with large body sizes have small sperm, and while metabolic rate (corrected for body size) influences sperm size, sperm competition levels do not. When all eutherian mammals are analysed jointly, our results suggest that as mass-specific metabolic rate increases, so does maximum sperm size. In addition, species with low mass-specific metabolic rates produce uniformly small sperm, while species with high mass-specific metabolic rates produce a wide range of sperm sizes. These findings support the hypothesis that mass-specific metabolic rates determine the budget available for sperm production: at high levels, sperm size increases in response to sexual selection, while low levels constrain the ability to respond to sexual selection by increasing sperm size. Thus, adaptive and costly traits, such as sperm size, may only evolve under sexual selection when metabolic rate does not constrain cellular budgets.


2016 ◽  
Vol 187 (3) ◽  
pp. 295-307 ◽  
Author(s):  
Cynthia J. Downs ◽  
Jessi L. Brown ◽  
Bernard W. M. Wone ◽  
Edward R. Donovan ◽  
Jack P. Hayes

Author(s):  
Kaitlyn E. Kortright ◽  
Rachel E. Done ◽  
Benjamin K. Chan ◽  
Valeria Souza ◽  
Paul E. Turner

There is increasing interest in phage therapy as an alternative to antibiotics for treating bacterial infections, especially using phages that select for evolutionary trade-offs between increased phage resistance and decreased fitness traits such as virulence in target bacteria. A vast repertoire of virulence factors allows the opportunistic bacterial pathogen, Shigella flexneri , to invade human gut epithelial cells, replicate intracellularly, and evade host immunity through intercellular spread. It is previously shown that OmpA is necessary for intercellular spread of S. flexneri . We hypothesized that a phage which uses OmpA as a receptor to infect S. flexneri , should select for phage-resistant mutants with attenuated intercellular spread. Here we show that phage A1-1, requires OmpA as a receptor and selects for reduced virulence in S. flexneri . We characterized five phage-resistant mutants by measuring phenotypic changes in various traits: cell-membrane permeability, total lipopolysaccharide (LPS), sensitivity to antibiotics, and susceptibility to other phages. Results separated the mutants into two groups: R1 and R2 phenotypically resembled ompA knockouts, whereas R3, R4 and R5 were similar to LPS-deficient strains. Whole genome sequencing confirmed that R1 and R2 had mutations in ompA , while R3, R4 and R5 showed mutations in LPS inner-core biosynthesis genes gmhA and gmhC . Bacterial plaque assays confirmed that all phage-resistant mutants were incapable of intercellular spread. We concluded that selection for S. flexneri resistance to phage A1-1 generally reduced virulence (i.e. intercellular spread), but this trade-off could be mediated either by mutations in ompA or in LPS-core genes that likely altered OmpA conformation. Author Summary Shigella flexneri is a facultative intracellular pathogen of humans, and a leading cause of bacillary dysentery. With few effective treatments and rising antibiotic resistance in these bacteria, there is increasing interest in alternatives to classical infection management of S. flexneri infections. Phage therapy poses an attractive alternative, particularly if a therapeutic phage can be found that results in an evolutionary trade-off between phage resistance and bacterial virulence. Here, we isolate a novel lytic phage from water collected in Cuatro Cienegas, Mexico that uses the OmpA porin of S. flexneri as a receptor. We use phenotypic assays and genome sequencing to show that phage A1-1 selects for phage-resistant mutants that can be grouped into two categories: OmpA-deficient mutants and LPS-deficient mutants. Despite these underlying mechanistic differences, we confirmed that naturally-occurring phage A1-1 selected for evolved phage resistance that coincided with impaired intercellular spread of S. flexneri in a eukaryotic infection model.


2004 ◽  
Vol 26 (1) ◽  
pp. 111
Author(s):  
AJ Hulbert ◽  
PL Else

Mammals, being endotherms have very high metabolic rates compared to ectothermic reptiles. Similarly, small mammals have high rates of mass-specific metabolism compared to larger mammals. This review examines the mechanistic basis of why particular mammal species have a specific metabolic rate. Initial studies compared mammals with arid zone reptile species of the same size and Tb. Mammals have larger internal organs, with more mitochondrial membrane surface area than the reptiles. The cells of mammals are leakier to Na+ ions and their mitochondrial membranes are leakier to H+ ions than in reptile cells. These leakier membranes have membrane lipids that are polyunsaturated and less monounsaturated than their less leaky counterparts. Examination of the cellular basis of allometric variation in metabolism in mammals reveals very similar findings with polyunsaturated membranes associated with the high mass-specific metabolic rates of small mammal species and monounsaturated membranes with low rates of metabolism of large mammals. These findings have resulted in the development of the ?membrane pacemaker? theory of metabolism, which proposes that membrane bilayer composition is regulated in animals and that highly polyunsaturated membranes result in enhanced molecular activity of membrane proteins and in turn this results in an elevated metabolic rate of cells, tissues and consequently whole animals. This theory is also supported by the recent examination of the basis of body-size variation in the metabolic rates of birds. The ?membrane pacemaker? theory of metabolism is currently the only explanation of the mechanisms determining the metabolic rate and thus the cost of living of animals. It has implications for the effect of food habits on metabolism and the relationship between metabolism and lifespan.


2020 ◽  
Vol 93 (1) ◽  
pp. 23-36
Author(s):  
Cynthia J. Downs ◽  
Jessi L. Brown ◽  
Bernard W. M. Wone ◽  
Edward R. Donovan ◽  
Jack P. Hayes

2008 ◽  
Vol 21 (6) ◽  
pp. 1744-1754 ◽  
Author(s):  
S. C. COTTER ◽  
J. P. MYATT ◽  
C. M. H. BENSKIN ◽  
K. WILSON

Author(s):  
William A. Buttemer ◽  
Vincent Careau ◽  
Mark A. Chappell ◽  
Simon C. Griffith

Evidence from a number of species suggests behaviours associated with social rank are positively correlated with metabolic rate. These studies, however, are based on metabolic measurements of isolated individuals, thereby ignoring potential effects of social interactions on metabolic rates. Here, we characterised three pertinent metabolic indices in the two predominant genetic colour morphs of the Gouldian finch (Erythrura gouldiae): diurnal resting metabolic rate (RMR), nocturnal basal metabolic rate (BMR), and exercise-induced maximal metabolic rate (MMR). Research reveals red-headed morphs consistently dominate the less aggressive black-headed morphs and the two morphs to differ in other behavioural and physiological traits. We measured daytime RMR of intermorph naïve birds (first-year virgin males maintained in total isolation from opposite colour morphs) and their metabolic responses to viewing a socially unfamiliar bird of each colour. Subsequently each bird was placed in a home cage with an opposite colour morph (intermorph exposed) and the series of measurements repeated. Daytime RMR was indistinguishable between the two morphs, whether intermorph naïve or intermorph exposed. However, both red- and black-headed birds showed a greater short-term increase in metabolic rate when viewing an unfamiliar red-headed bird than when seeing a black-headed bird, but only when intermorph naïve. Measurements of BMR and exercise-induced MMR did not differ between the two morphs, and consequently aerobic scope was indistinguishable between them. We propose that the suite of behavioural differences between these two sympatric morphs are functionally complementary and represent evolutionary stable strategies permitting establishment of dominance status in the absence of metabolic costs.


2016 ◽  
Vol 12 (3) ◽  
pp. 20160078 ◽  
Author(s):  
Cas Eikenaar ◽  
Arne Hegemann

Animals need a well-functioning immune system to protect themselves against pathogens. The immune system, however, is costly and resource trade-offs with other demands exist. For migratory animals several (not mutually exclusive) hypotheses exist. First, migrants reduce immune function to be able to allocate resources to migration. Second, migrants boost immune function to cope with more and/or novel pathogens encountered during migration. Third, migrants reallocate resources within the immune system. We tested these hypotheses by comparing baseline immune function in resident and migratory common blackbirds ( Turdus merula ), both caught during the autumn migration season on the island of Helgoland, Germany. Indices of baseline innate immune function (microbial killing capacity and haptoglobin-like activity) were lower in migrants than in residents. There was no difference between the groups in total immunoglobulins, a measure of baseline acquired immune function. Our study on a short-distance avian migrant supports the hypothesis that innate immune function is compromised during migration.


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