Early Life Conditions Influence Milk Production

Maternal nutritional conditions during pregnancy are known to have substantially affect infant development. This was most clearly demonstrated by research into the outcomes of infants from the Dutch Hunger Winter of 1944. Because determination and differentiation of cell lines occur during embryonic development, nutritional conditions and other environmental insults early during pregnancy can substantially alter offspring phenotype, including behavior and general health. For example, the Hunger Winter produced different results depending on whether the mother’s nutrition was most interrupted during the first, second, or third trimester, or during lactation. 

 photo from Dutch Resistance Museum

Since then, systematic research into fetal programming and developmental origins of health and disease (DoHAD) has identified that early life nutritional conditions affect numerous physiological systems and organ structures, putting individuals at later risk for kidney, liver, heart, pancreatic, neurobiological, endocrine, and reproductive dysfunction (Schug et al., 2012).

Simply put, our early life experiences leave their mark.

Factors within the mother and the environment beyond nutrition affect offspring development because of constraints and trade-offs. Life history theory, an area within evolutionary biology, is predicated on the fact that organisms have limited energy and resources that must be allocated toward several biological “imperatives”- maintenance, development, and reproduction (Stearns, 1992). Maintenance is basically keeping your body alive -- such as thermoregulation and immune responses. Growing (i.e., adding mass) and development (i.e., skeletal ossification) also require energy and resources. And producing that most valuable currency of natural selection – BABIES -- does not come cheap.

Because you can only spend, or burn, a calorie once, individuals face trade-offs among maintenance, growth, and reproduction. Under famine conditions children don't grow very well and they can't always "catch-up" - for example in terms of height, they are permanently stunted (Gørgensa et al., 2012). Female Olympic athletes often have reduced fertility due to altered ovarian function (DeSouza et al., 2010). Basically the body says "Why cycle if body fat reserves are too low to sustain pregnancy or lactation?" And once pregnant and lactating, females face trade-offs between the kid they are investing in now vs. the kids that they will have later- aka current and future reproduction. Allocating too much energy to the current offspring can deplete body reserves, extend maternal recovery, and delay subsequent conceptions.

In this day and age of pregnancy planning and the demographic transition to smaller families, delaying subsequent reproduction is a often the goal. But our physiology has been shaped by a mammalian life history very different than our modern world. 

 Liverpool Library Family History Archives

Natural selection favors adaptations that allow females to maximize their lifetime reproductive success -- the total number of offspring produced over their reproductive careers.  Underlying mechanisms in female reproductive physiology are seemingly sensitive to nutritional intake and body condition, and through these mechanisms fertility, pregnancy, and lactation are regulated and resources allocated to the developing offspring.

In some mammalian species, females can produce more offspring over their lifetime if they can sustain overlapping pregnancy and lactation. This is actually a characteristic feature of some marsupials (Tyndale-Biscoe and Renfree, 1987). For example the tammar wallaby, close relative of the kangaroo, can be pregnant, have a tiny pouch joey attached to the nipple continuously and a larger joey that still consumes milk.

photo by Thorsten Milse

Fun fact: the different mammary glands produce different milk composition fine-tuned to the developmental states of the two differently-aged joeys (Trott et al. 2002, Nicholas et al. 2012).

 Fig. 2. Lactation in the tammar wallaby. Nicholas et al. 2012.

While simultaneous pregnancy and lactation can increase reproductive output, it also sets the stage for competition for maternal resources between milk synthesis for the infant and nutrient transfer via the placenta for the fetus. 

 ________________________

Enter the awesomest* lactation biology animal model: 

The Dairy Cow

*Yeah I know it should be 'most awesome' but I prefer to use 'awesomest.'

In December 2012, González-Recio and colleagues reported that overlapping pregnancy and lactation had consequences for the fetus that manifested in adulthood. They used a sample of >40,000 Holsteins, and admirably controlled for other genetic and environmental factors.  Cows that were gestated by a mom who was also lactating produced significantly less milk and died at younger ages! 

Of course, just like when signing a contract, it’s important to read the fine print. These cows produced ~52 kg less milk per lactation, but since the average production per annum for a Holstein is on average ~10,000 kg of milk, translated that is ~0.005% less milk. They also died only 16 days earlier than cows that were gestated by a mom who was not lactating. 

However, these  effects, while relatively modest, demonstrate that early embryonic and fetal development *IS* sensitive to any reductions in resource allocation. Moreover, from a biological perspective, we would expect this effect to be greater in wild-living mammals that aren’t fed or provided with any veterinary care like domesticated dairy cows.

Lascaux cave art of Bos primigenius

the wild predecessor of domesticated cattle. 

Along similar lines, Soberon and colleagues showed that among calves reared on milk replacer, trade-offs between maintenance and growth reduced milk yield in adulthood (2012). Standard rations of milk replacer were provided to calves, but calves born during the winter had to burn more calories to stay warm- thermoregulation is energetically costly. Less energy was available for growth and these calves grew more slowly. Calves that grew better had better milk production in adulthood. For every additional kilogram gained per day resulted in 850-1100 kg more milk on their first lactation. This was directly linked to the amount of milk replacer the calves got above their maintenance needs. Thermoregulation wasn’t the only maintenance cost some calves had to pay. Getting sick in early life also impacted future production -- calves that received antibiotics went on to produce ~500 kg less milk on their first lactation. Immune response, like staying warm, isn’t free, and those costs- diverting energy from growth and development reduced future ability to synthesize milk.

The precise underlying mechanisms by which mammary gland function is impacted by early life trade-offs (either by the dam or the calf) are not yet clear. However, the effects are likely through epigenetic modification of gene expression. Important questions remain about the length of critical windows in which developing organisms are sensitive to environmental influences and the possibility for reversing or mediating early life programming. Until we better understand the proximate pathways, these phenomenological results still provide valuable insights. Dairy scientists may be able to further improve milk production by shaping animal husbandry practices to optimize early life development. And most importantly, these results illustrate the value of theoretical and evolutionary perspectives for understanding lactation biology (Hinde and German 2012).

Citations

De Souza MJ, Toombs RJ, Scheid JL, O'Donnell E, West SL, Williams NI. 2010. High prevalence of subtle and severe menstrual disturbances in exercising women: confirmation using daily hormone measures. Hum Reprod. 25(2):491-503. doi: 10.1093/humrep/dep411

González-Recio O, Ugarte E, Bach A. 2012. Trans-generational effect of maternal lactation during pregnancy: a Holstein cow model. PLoS One. 2012;7(12):e51816. doi: 10.1371/journal.pone.0051816.

Gørgensa T, Mengb X, Vaithianathanc R. 2012. Stunting and selection effects of famine: A case study of the Great Chinese Famine. Journal of Development Economics. 97: 99-111

Hinde K, German JB. 2012 Food in an evolutionary context: insights from mother's milk. J Sci Food Agric. 92(11):2219-23. doi: 10.1002/jsfa.5720.

Nicholas, K., Sharp, J., Watt, A., Wanyonyi, S., Crowley, T., Gillespie, M., & Lefevre, C. (2012). The tammar wallaby: A model system to examine domain-specific delivery of milk protein bioactives. In Seminars in Cell & Developmental Biology (Vol. 23, No. 5, pp. 547-556). Academic Press.

Schug TT, Erlebacher A, Leibowitz S, Ma L, Muglia LJ, Rando OJ, Rogers JM, Romero R, vom Saal FS, Wise DL. 2012. Fetal programming and environmental exposures: implications for prenatal care and preterm birth. Ann N Y Acad Sci. 1276:37-46. doi: 10.1111/nyas.12003.

Soberon F, Raffrenato E, Everett RW, Van Amburgh ME. 2012. Preweaning milk replacer intake and effects on long-term productivity of dairy calves. J Dairy Sci. 95(2):783-93. doi: 10.3168/jds.2011-4391.

Stearns, Stephen C., 1992. The Evolution of Life Histories. Oxford University Press, London

Trott, J. F., Simpson, K. J., Moyle, R. L., Hearn, C. M., Shaw, G., Nicholas, K. R., & Renfree, M. B. (2003). Maternal regulation of milk composition, milk production, and pouch young development during lactation in the tammar wallaby (Macropus eugenii). Biology of reproduction, 68(3), 929-936.

Tyndale-Biscoe H. Renfree M. 1987. Reproductive physiology of marsupials. Cambridge University Press