Mosaic metabolic ageing: Basal and standard metabolic rates age in opposite directions and independent of environmental quality, sex and life span in a passerine

Abstract

Crucial to our understanding of the ageing process is identifying how traits change with age, which variables alter their ageing process and how these traits associate with fitness. Here we investigated metabolic ageing in outdoor‐living captive zebra finches experiencing foraging costs. We longitudinally monitored 407 individuals over 6 years and collected 3,213 measurements of two independent mass‐adjusted metabolic traits: basal metabolic rate (BMRm) at thermoneutral temperatures and standard metabolic rate (SMRm), measured as BMRm but at ambient temperatures below thermoneutrality. We define mosaic or asynchronous ageing as the difference in standardized absolute ageing rates between traits, and we estimate the degree of asynchrony using the within‐individual correlation of change in trait values with age. BMRm decreased linearly with age, consistent with earlier reports. In contrast, SMRm increased linearly with age. The absolute standardized change with age was significantly faster for BMRm compared to SMRm, and the within‐individual correlation of age related change was negligible. To the best of our knowledge, this is the first quantification of SMRm ageing, and the finding that SMRm and BMRm age in opposite directions. Neither metabolic rate nor metabolic ageing rate were associated with variation in life span between individuals. Moreover, experimental manipulations of environmental quality that decreased BMRm and SMRm and shortened life span by 6 months (12%) did not affect the ageing of either metabolic trait. Females lived 2 months (4%) shorter than males, but none of the metabolic traits showed sex‐specific differences at any age. Our findings indicate, in contrast to the current view, that baseline energy requirements increase with age, because animals do not generally live in thermoneutral conditions, and illustrate the importance of studying the ageing phenotype in an ecologically realistic setting. A free Plain Language Summary can be found within the Supporting Information of this article.

Natural Selection and the Evolution of Asynchronous Aging

“…From here, they asserted without making clear logical arguments that selection should act most strongly to resist senescence for those traits that degrade fastest. This anticipates the argument made much later by Rodríguez-Muñoz et al (2019) and Briga and Verhulst (2021) that selection acts to reduce senescence. Williams and Maynard Smith argued then that this should cause evolution to eventually lead to synchronous aging among traits (i.e., high among-trait correlations among rates of senescence within populations).…”

“…Previous verbal arguments made to explain the evolution of asynchrony make the argument that because senescence is maladaptive, it follows that selection should act to remove it (e.g., Rodríguez-Muñoz et al 2019). Others apply the concept of canalization (Waddington 1942, Flatt 2005 to the evolution of ageing to arrive at the same prediction (Boonekamp et al 2018, Briga andVerhulst 2021). In the case of the former, it is sufficient to observe that the logic and prediction that follows is inconsistent with what emerges from the formal theory.…”

“…However, much more recent arguments have attempted to reconcile evolutionary theory with observations of widespread asynchronous aging by suggesting a different role for natural selection. These later verbal models propose that because the fitness lost owing to senescence is greatest in those traits that are most important to fitness (Boonekamp et al 2018, Rodríguez-Muñoz et al 2019, Briga and Verhulst 2021, it should follow that selection to remove senescence is greatest for these traits. This logic leads to the prediction that senescence should evolve to be most pronounced in those traits that are under the weakest selection.…”

Sex‐specific body mass ageing trajectories in adult Asian elephants

“…Hence, the ageing trajectories do not synchronize between traits in females. Empirically, this heterogeneity of ageing patterns is more the rule than the exception as found in other species (Briga & Verhulst, 2021;Hayward et al, 2015;Walker & Herndon, 2010). In our population, this mismatch can be explained by the fact that body mass is a poor predictor of reproductive success, number of offspring produced or raised up to independence (5 years old), and that no relationship between height and survival has been found in females (Crawley et al, 2017).…”

Sex-specific body mass ageing trajectories in adult Asian elephants

“…Hence, the ageing trajectories do not synchronise between traits in females. Empirically, this heterogeneity of ageing patterns is more the rule than the exception as found in other species (Briga & Verhulst, 2021;Hayward et al, 2015;Walker & Herndon, 2010). In our population, this mismatch can be explained by the fact that body mass is a poor predictor of reproductive success, number of offspring produced or raised up to independence (5 years old), and that no relationship between height and survival has been found in females (Crawley et al, 2017).…”