Milk matters: offspring survival in Columbian ground squirrels is affected by nutrient composition of mother's milk

Abstract

Through maternal effects, information about environmental conditions experienced in the maternal generation can be transmitted to subsequent generations. Although maternal effects have been described and quantified in many mammalian species, the underlying causal links are often under-studied. The close association between mother and neonate during the extended period of lactation in mammals provides a unique opportunity for mothers to influence offspring phenotype through nutrient provisioning of milk. The purpose of this study was to examine sources of inter-individual variation in milk composition and impacts on offspring phenotype and survival. Variation in fat content, protein content, and energy density of mother's milk was associated with timing of reproduction. Mothers with intermediate birthdates produced milk that was higher in fat and energy density, but lower in protein than females with early or late birthdates. In turn, the pattern of change in milk composition affected juvenile overwinter survival. The protein content of Columbian ground squirrel milk typically increases to peak lactation and then declines before weaning. Pups consuming milk that was lower in protein in early lactation but then relatively high in protein at peak and late lactation had a higher probability of survival overwinter. Our results indicate that the interplay between the timing of reproduction and lactation performance has consequences for maternal and offspring fitness.

Causes and short‐term consequences of variation in milk composition in wild sheep

“…Our results support studies showing the importance of stored energy to sustain the costs of reproduction, that is "capital" breeding (Festa-Bianchet, 1998;Williams et al, 2017). In addition, our results support the contention that females in better "condition" would afford to increase the amount of fat in milk (Barboza, Parker, The difficulty in detecting strong links between physiology and life-history traits suggests that correlations between milk composition and fitness reported in previous studies (Landete-Castillejos, García, & Gallego, 2001;Landete-Castillejos, García, López-Serrano, & Gallego, 2005;Quesnel et al, 2017;Skibiel & Hood, 2015) might be driven by a direct influence of environmental variation and not by a maternal strategy. Our data cannot clearly distinguish whether mothers have no control on the content of their milk or have "flexible" milk composition in face of environmental variation.…”

“…The difficulty in detecting strong links between physiology and life‐history traits suggests that correlations between milk composition and fitness reported in previous studies (Landete‐Castillejos, García, & Gallego, ; Landete‐Castillejos, García, López‐Serrano, & Gallego, ; Quesnel et al., ; Skibiel & Hood, ) might be driven by a direct influence of environmental variation and not by a maternal strategy. Our data cannot clearly distinguish whether mothers have no control on the content of their milk or have “flexible” milk composition in face of environmental variation.…”

“…Two important life‐history parameters, body mass and growth rate of young (Iverson, Bowen, Boness, & Oftedal, ; Mellish, Iverson, & Bowen, ), have been shown to be influenced by milk composition, but several other life‐history parameters can be affected by the nutritive, immunological and hormonal constituents in milk (e.g., immune, cognitive and neurobiological development in infants; Hinde & Milligan, ). Focusing on its nutritional aspects, milk is often described by two well‐known nutritive components—average fatty acid and protein concentrations—and total gross energy derived from these components, especially in wild mammals (e.g., Quesnel, MacKay, Forsyth, Nicholas, & Festa‐Bianchet, ; Skibiel & Hood, ). Only a few studies, however, have investigated the simultaneous sources of variation—environmental and individual—on wild mammals’ milk composition including mineral, fat, protein and sugar contents, despite their evolutionary importance (Cook, Lentfer, Pearson, & Baker, ; Carlini, Márquez, Soave, Vergani, & de Ferrer, ; see review by Skibiel, Downing, Orr, & Hood, in captive and wild species).…”

Size, season and offspring sex affect milk composition and juvenile survival in wild kangaroos

“…Experimentally restricted diets have revealed the importance of nutrition on lactation performance (Roberts, Cole & Coward, ; Landete‐Castillejos et al ., ; Bovolenta et al ., ). If the timing of reproduction affects milk provisioning (Landete‐Castillejos et al ., ; Skibiel & Hood, ) then there could be large seasonal variation in maternal caring ability in the wild. Most studies investigating maternal care through milk, however, were performed in captive (Hinde, ; Robert & Braun, ), or semi‐captive (Landete‐Castillejos et al ., ) environments.…”

“…Male body size in kangaroos affects mating success (Rioux‐Paquette et al ., ); we predicted that mothers with a higher ability to care would provide milk with higher protein content to sons than to daughters. Finally, we tested whether protein concentration at peak lactation affected offspring survival (Skibiel & Hood, ).…”