Energetic mechanisms for coping with changes in resource availability

Abstract

Given current anthropogenic alterations to many ecosystems and communities, it is becoming increasingly important to consider whether and how organisms can cope with changing resources. Metabolic rate, because it represents the rate of energy expenditure, may play a key role in mediating the link between resource conditions and performance and thereby how well organisms can persist in the face of environmental change. Here, we focus on the role that energy metabolism plays in determining organismal responses to changes in food availability over both short-term ecological and longer-term evolutionary timescales. Using a meta-analytical approach encompassing multiple species, we find that individuals with a higher metabolic rate grow faster under high food levels but slower once food levels decline, suggesting that the association between metabolism and life-history traits shifts along resource gradients. We also find that organisms can cope with changing resource availability through both phenotypic plasticity and genetically based evolutionary adaptation in their rates of energy metabolism. However, the metabolic rates of individuals within a population and of species within a lineage do not all respond in the same manner to changes in food availability. This diversity of responses suggests that there are benefits but also costs to changes in metabolic rate. It also underscores the need to examine not just the energy budgets of organisms within the context of metabolic rate but also how energy metabolism changes alongside other physiological and behavioural traits in variable environments.

Genetic coupling of life-history and aerobic performance in Atlantic salmon

“…The timing of maturation, just as many life-history traits, depends on reaching a certain body size threshold, i.e., the acquisition of sufficient energy that can be allocated for maturation processes (Moghadam et al 2007;Taranger et al 2010;Verta et al 2020). Because of context-dependent covariation between metabolism and growth rate (see meta-analysis by Auer et al (2020b)), we tested if resource availability modified the genetic covariation between metabolic phenotypes and age-at-maturity. Against our predictions, our experiments did not reveal a change in SMR or MMR, or genotype-by-environment interactions, due to feed restriction, despite a strong decrease in growth rate.…”

Standard metabolic rate does not associate with age-at-maturity genotype in juvenile Atlantic salmon

“…Vgll3 genotype has been shown to have a strong effect on salmon life-history (Ayllon et al, 2015;Barson et al, 2015;Verta et al, 2020), and recent findings have suggested that this effect might be mediated by vgll3-induced differences in body condition (Debes et al, 2021). Taking this together with the connections between standard metabolic rate (SMR) and resource acquisition and assimilation (Armstrong et al, 2011;Auer, Bassar, et al, 2020;Auer, Solowey, et al, 2020;Bochdansky et al, 2005;Millidine et al, 2009;Rosenfeld et al, 2015), we hypothesized that vgll3 genotype might be asserting some of its effects through changes in energetic physiology that would be reflected in SMR. However, we did not detect any difference in either SMR or body condition between juvenile Atlantic salmon individuals of different homozygous vgll3 genotypes.…”

“…Metabolic phenotype is a multi-faceted set of traits, covering not just standard metabolic rate, but also the maximum metabolic rate, aerobic scope, and daily energy expenditure, to mention some. Additionally, the consequences of variation in metabolic traits are context-dependent and may change under different environmental conditions and life stages (Auer, Bassar, et al, 2020;Auer, Solowey, et al, 2020;Bochdansky et al, 2005;Millidine et al, 2009;Norin & Metcalfe, 2019). We initially planned to also measure metabolic rate under exhaustive swimming to obtain data on maximum metabolic rate (MMR), but had to abandon these trials as we were unable to motivate juvenile salmon of this age and size to do any exhaustive swimming, either by swim tunnel or by hand chasing.…”

“…Early-life performance in acquiring and efficiently using resources sets the stage for the timing of maturation: sexual maturation and reproduction are costly processes, and a key part of juvenile development is the accumulation and storage of excess energy to support future maturation (Hutchings & Jones, 1998;Simpson, 1992;Thorpe, 2007). Standard metabolic rate (SMR) (Chabot et al, 2016) is a potentially important trait with regards to this as it relates to the organism's maintenance energy requirements, capacity for nutrient assimilation, and responses to changing resource availability (Armstrong et al, 2011;Auer, Bassar, et al, 2020;Auer, Solowey, et al, 2020;Bochdansky et al, 2005;Millidine et al, 2009;Rosenfeld et al, 2015). The effect of vgll3 genotype on body condition, as well as its strong effect on age at maturity, raises the question of whether vgll3 might assert some of its effects via SMR, warranting an investigation on the potential influence of vgll3 on metabolic phenotype.…”

Life histories as mosaics: plastic and genetic components differ among traits that underpin life-history strategies

“…Increased population density and the resulting change in food availability could influence the expression of phenotypic traits in three separate, non-exclusive ways (Auer et al 2020). First, by reducing per-capita food availability, they may lead to plastic changes in resource-dependent traits.…”