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

Abstract

The main component of mammalian maternal care is milk production. The composition of milk has been hypothesized to determine offspring survival, and to vary with offspring sex. Few studies, however, have examined variation in milk composition of wild mammals in seasonal environments, where environmental conditions can impact the ability of mothers to provide care. We investigated individual differences in milk composition and offspring survival in wild eastern grey kangaroos (Macropus giganteus). We analyzed total protein and lipid concentrations in 103 milk samples from 91 females over 2 years. In a year of low forage production, few females that lactated were in poorer condition and produced milk of lower energy content compared to females lactating in a year of high forage production. Females nursing in late winter produced milk with more lipids compared to females at the same stage of lactation in late spring, whose milk had a higher proportion of protein. The milk of larger females contained more protein than lipid, and females in better condition allocated higher proportions of protein to sons than to daughters. Increased protein concentration in milk was correlated with offspring longevity, and this effect was stronger for sons than daughters. A seasonally modulated lactation strategy enables the adjustment of milk composition to available resources. Condition‐specific protein allocation in favor of sons for mothers of higher caring ability suggests adaptive sex‐biased maternal care in this highly sexually dimorphic mammal.

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).…”

Sex-Specific Human Milk Composition: The Role of Infant Sex in Determining Early Life Nutrition

“…Evidence of sex-specific milk production has also been reported for other ruminants, as well as marsupials. Wild eastern kangaroos ( Macropus giganteus ) [ 45 ] and Tammar wallabies ( Macropus eugenii ) [ 46 ] were found to produce milk with higher protein for male offspring but same energy content and volume for offspring of different sex. Similarly, Iberian red deer ( Cervus elaphus hispanicus ) mothers were observed to produce greater yields of milk with higher energy content for male calves, reflected by higher protein, fat and lactose content [ 47 ].…”

Peer Review #2 of "Marsupial and monotreme milk—a review of its nutrient and immune properties (v0.1)"

“…In marsupials, milk composition and yield also vary with sex of the young (Quesnel et al 2017;Waterman et al 2012). Both tammar wallabies and eastern grey kangaroos allocate more protein to sons than to daughters (Quesnel et al 2017;Waterman et al 2012).…”