Maternal Programming of Social Dominance via Milk Cytokines

Abstract

Summary Regular physical activity improves physical and mental health. Here we found that the effect of physical activity extends to the next generation. Voluntary wheel running of dams, from postpartum day 2 to weaning, increased the social dominance and reproductive success, but not the physical/metabolic health, of their otherwise sedentary offspring. The individual's own physical activity did not improve dominance status. Maternal exercise did not disrupt maternal care or the maternal and offspring microbiota. Rather, the development of dominance behavior in the offspring of running mothers could be explained by the reduction of LIF, CXCL1, and CXCL2 cytokines in breast milk. These data reveal a cytokine-mediated lactocrine pathway that responds to the mother's postpartum physical activity and programs offspring social dominance. As dominance behaviors are highly relevant to the individual's survival and reproduction, lactocrine programming could be an evolutionary mechanism by which a mother promotes the social rank of her offspring.

Milking It for All It’s Worth: The Effects of Environmental Enrichment on Maternal Nurturance, Lactation Quality, and Offspring Social Behavior

“…Recent work has shown running wheel activity to alter milk quality in terms of specific inflammatory molecules such as leukocyte inhibitory factor, CXCL1, and CXCL2; however maternal care was not affected (Taki et al, 2020). This suggests there may be something special in the qualia of the EE condition that extends beyond increased physical activity in terms of its contribution to maternal-neonatal interactions.…”

“…While the physiological mechanisms that contribute to time-specific and sex-specific differences in behavior among EE offspring need further elucidation, the present results shed light on maternal care and maternal milk quality as pathways of interest for future studies to explore. Recent work has shown running wheel activity to alter milk quality in terms of specific inflammatory molecules such as leukocyte inhibitory factor, CXCL1, and CXCL2; however maternal care was not affected ( Taki et al, 2020 ). This suggests there may be something special in the qualia of the EE condition that extends beyond increased physical activity in terms of its contribution to maternal-neonatal interactions.…”

Gut microbiota shapes social dominance through modulating HDAC2 in the medial prefrontal cortex

“…To date, emerging knowledge is appreciated to explain why a particular individual, even under controlled laboratory conditions, obtains high social rank, whereas others become subordinates (Anacker et al, 2019;Hollis et al, 2015;Taki et al, 2020). As GM is prone to genetic and environmental cues and has a profound impact on host health, it may constitute the important individuality determining social dominance.…”

Milking it for all it’s worth: The effects of environmental enrichment on maternal nurturance, lactation quality, and offspring social behavior

“…Results of the present study bolster the argument that EE housing conditions encapsulate a more naturalistic environment than SD, especially with regard to maternal behavior and development (Zhao et al, 2021; Connors et al, 2015; Ratuski & Weary 2021). Recent work has shown running wheel activity to alter milk quality in terms of specific inflammatory molecules such as leukocyte inhibitory factor, CXCL1, and CXCL2; however maternal care was not affected (Taki et al, 2020). This suggests there may be something special in the qualia of the EE condition that extends beyond increased physical activity in terms of its contribution to maternal-neonatal interactions.…”