Exposure to hot temperatures during lactation stunted offspring growth and decreased the future reproductive performance of female offspring

Abstract

Exposure to high temperatures (heatwaves) is rapidly emerging as an important issue of climate change, in particular for female mammals during lactation. High temperatures adversely affect the ability to dissipate heat, which has negative effects on reproductive output. The cumulative effects on growth of F1 offspring after weaning, and future reproductive performance of offspring, remain uncertain. In this study, F1 mice weaned from mothers lactating at 21 and 32.5°C were housed at 21°C from day 19 until day 56 of age, during which food intake and body mass were measured. The F1 adult females that were weaned at the two temperatures were bred and then exposed to 32.5°C during lactation. Energy intake and milk output, and litter size and mass, were determined. The F1 adults weaned at 32.5°C consumed less food and had lower body mass than their counterparts weaned at 21°C. Several visceral organs or reproductive tissues were significantly lower in mass in F1 weaned at 32.5°C than at 21°C. The exposure to 32.5°C significantly decreased energy intake, milk output and litter mass in F1 adult females during lactation. The F1 adult females weaned at 32.5°C produced less milk and raised lighter pups than those previously weaned at 21°C. The data suggest that transient exposure to hot temperatures during lactation has longlasting impacts on offspring, including stunted growth and decreases in future reproductive performance when adult. This indicates that the offspring of females previously experiencing hot temperatures have a significant fitness disadvantage.

Effects of ambient temperatures between 5 and 35 °C on energy balance, body mass and body composition in mice

“…Because 90% of the elevated energy requirements as it got colder were met by increased food intake the mice had to modify their alimentary tract and associated organs to sustain their digestive efficiency constant at around 80%. Similar changes are observed in mice during lactation in the face of large increases in food intake [ [84] , [85] , [86] , [87] ]. This included increases in the activity of various digestive enzymes in the small intestine, such as maltase, sucrase and aminopeptidase, combined with expansion in the size of the small intestine and the liver.…”

RISING STARS: The heat is on: how does heat exposure cause pregnancy complications?

“…A further important consideration for neonatal health is the effect of heat exposure on lactation, which is a highly metabolic, heat-producing process. There is limited information on this in humans although in dairy cows (Monteiro et al 2016) and mice (Bao et al 2020), heat exposure decreases milk production but the implications for milk composition are unclear.…”

Thermoregulatory trade-offs underlie the effects of warming summer temperatures on deer mice

“…Indeed, the high T a recently experienced by some tropical and desert endotherms has increased T b towards dangerous and even lethal temperatures (Danner et al, 2021;McKechnie and Wolf, 2019). Less severe increases in T a can constrain locomotor activity, reproduction and various other important performance traits, likely as a result of limits to metabolic heat production (Bao et al, 2020;Speakman and Król, 2010;Tapper et al, 2020). However, while our understanding of the effects of climate warming is improving for some endotherms, such as tropical and desert endotherms (Lovegrove et al, 2014;McKechnie and Wolf, 2010;Tewksbury et al, 2008) and some large temperate mammals (Hetem et al, 2014;McCain and King, 2014), the impacts of climate warming remain largely unknown for many other species (Levesque et al, 2016).…”