An intra-population heterothermy continuum: notable repeatability of body temperature variation in food-deprived yellow-necked mice

Abstract

Theoretical modelling predicts that the thermoregulatory strategies of endothermic animals range from those represented by thermal generalists to those characteristic for thermal specialists. While the generalists tolerate wide variations in body temperature (T b ), the specialists maintain T b at a more constant level. The model has gained support from inter-specific comparisons relating to species and population levels. However, little is known about consistent among-individual variation within populations that could be shaped by natural selection. We studied the consistency of individual heterothermic responses to environmental challenges in a single population of yellow-necked mice (Apodemus flavicollis), by verifying the hypothesis that T b variation is a repeatable trait. To induce the heterothermic response, the same individuals were repeatedly food deprived for 24 h. We measured T b with implanted miniaturised data loggers. Before each fasting experiment, we measured basal metabolic rate (BMR). Thus, we also tested whether individual variation of heterothermy correlates with individual self-maintenance costs, and the potential benefits arising from heterothermic responses that should correlate with body size/mass. We found that some individuals clearly entered torpor while others kept T b stable, and that there were also individuals that showed intermediate thermoregulatory patterns. Heterothermy was found to correlate negatively with body mass and slightly positively with the BMR achieved 1-2 days before fasting. Nonetheless, heterothermy was shown to be highly repeatable, irrespective of whether we controlled for self-maintenance costs and body size. Our results indicate that specialist and generalist thermoregulatory phenotypes can co-exist in a single population, creating a heterothermy continuum.

Energy allocation shifts from sperm production to self-maintenance at low temperatures in male bats

“…In this treatment, heavier individuals may have allocated energy to thermoregulation as well as spermatogenesis, while maintaining mass, similar to what was found in ad libitum fed bats in a food deprivation experiment 26 . Our results correspond to other observations 44 , 45 which showed that torpor use in other small heterothermic mammals decreases with an increase in body mass.…”

Modeling heterothermic fitness landscapes in a marsupial hibernator using changes in body composition

“…The fact that the repeatability of a trait is high and significant indicates that the trait maintains its ranking in the population and also suggests that there could be genetic variation associated with it (Boratynski et al 2019 ; Bushuev et al 2010 ). This is also interpreted as a potential to respond to natural selection (i.e., evolutionary potential, see Hayes 2010 ; Mousseau and Roff 1987 ).…”

“…Despite the evident adaptive significance of hibernation and daily torpor (hereinafter referred to as the “heterothermic phenotype”), few authors have characterized this phenotype at the intra-population level. This is important, because to respond to natural selection a trait should exhibit: (1) consistent variation (i.e., significant repeatability; Boratynski et al 2019 ; Dohm 2002 ; Hayes et al 1998 ; Labocha et al 2004 ) and (2) fitness consequences (i.e., a significant selection gradient; Arnold 1983 ; Lande and Arnold 1983 ). Several authors have addressed these questions in a range of organisms, populations, and traits in what is known collectively as “phenotypic selection studies” (Kingsolver et al 2001 ; see reviews in Hoekstra et al 2001 ; Kruuk et al 2008 ; Mousseau and Roff 1987 ).…”

“…Several authors have addressed these questions in a range of organisms, populations, and traits in what is known collectively as “phenotypic selection studies” (Kingsolver et al 2001 ; see reviews in Hoekstra et al 2001 ; Kruuk et al 2008 ; Mousseau and Roff 1987 ). However, few explorations of selection surfaces exists (i.e., bi-variate fitness profiles, according to Phillips and Arnold 1989 ) on the heterothermic phenotype (Boratynski et al 2019 ; Dammhahn et al 2017 ; Lane et al 2011 ). Some authors used heterothermic indexes, quantifying the extent of heterothermy based on body temperatures, T B s (Boyles et al 2011 ), which resulted in being practical for comparing large datasets on intra- and inter-specific heterothermic patterns (Boyles et al 2013 ; Dammhahn et al 2017 ).…”

Thermal flexibility is a repeatable mechanism to cope with environmental stressors in a passerine bird

“…"repeatable"; reviewed in Boake 1989;Wolak et al 2012). Over the past two decades, numerous studies have reported moderate to high degrees of repeatability among traits associated with the stress response and whole-animal metabolism (Nespolo & Franco 2007;Rensel & Schoech 2011;Müller et al 2018;Boratyński et al 2019;but see Ouyang et al 2011). While these finding strongly suggest that stress-induced changes in T s and q Tot are also likely to be repeatable in endotherms, the degree of this repeatability remains largely unclear (but see Careau et al 2012).…”