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Mummy’s Boy

Male joeys are born bigger and stronger than females after receiving milk that i

Male joeys are born bigger and stronger than females after receiving milk that is higher in protein.

By Kylie Robert

An analysis of wallaby milk finds that male joeys receive better nutrition than their sisters.

In most mammals the majority of the investment and care of offspring lies with the mother, who makes a substantial commitment to pregnancy, lactation and the care of offspring until they become independent. Since the father’s role is completed after copulation, he can afford to sire more offspring with many females to enhance his reproductive output.

However, to do this successfully he needs to be the alpha male – the biggest and strongest – to keep his competition away and tend to his harem of females. Since a small, weak male rarely gets a look in and may never produce offspring, how a mother cares for her son in early life – through the resources she allocates to him – can determine his future reproductive success.

Recent research has found that deer, monkeys and humans produce different milk if they are raising sons or daughters. Our study has added to this list by discovering for the fourth time in any mammal – and the first time in a marsupial – that mothers make different milk for sons and daughters. This difference has lasting effects when the young become adults.

The maternal investment in lactation is no mild feat in marsupials. Instead of a long pregnancy they have a short pregnancy and an extended period of lactation and maternal care. Marsupials may spend 75–95% of the period between conception and infant independence on lactation compared with an average of 48% in other mammals. In effect marsupials replace the umbilical cord with the teat, so they have the most sophisticated form of lactation of all the mammals.

Because the milk of marsupials needs to support very different developmental stages, from the poorly developed “jelly bean” neonate to the near independent young, the composition of milk changes profoundly throughout lactation. During the Tammar wallaby’s 300-days in the pouch the joey consumes different milk on almost a weekly basis.

All mammalian milk is made up of a complex mix of proteins, carbohydrates, fats, water, vitamins, antimicrobials, digestive enzymes, hormones and ions that are specifically tailored for each species to ensure optimal growth, development and survival of the young. The composition of milk varies among species, reflecting the developmental priorities of the young, with each component of the milk having differing functions.

For example, young that need to grow fat, such as seals, require more fat. Fast-growing young like whales have greater requirements for protein. Young that grow slowly, like humans, have greater requirements for slow energy-yielding carbohydrates.

In marsupials, early lactation is characterised by a dilute milk with more carbohydrates than fats. Midway through lactation there is a switch, so that by the end of lactation the milk is rich in fats and proteins but low in carbohydrates.

What we now know is that even with milk compositional changes based on the growth stages of the joey there is also differences in these components based on the sex of the joey.

It is well-known that males and females are fundamentally different. In most mammals, adult males are bigger than females, often because males are born bigger and/or grow bigger. Gender differences in growth trajectories initially appear to be driven by the composition of milk during early development.

Natural selection favours adaptations that increase reproductive fitness. Put simply, producing the largest number of surviving and reproducing offspring is the primary objective of most species.

Having more descendants means an individual makes a greater genetic contribution to following generations, increasing its “reproductive fitness”. If male and female offspring have different reproductive fitness value to a mother there will be a strong advantage to producing offspring of the sex that will reproduce best.

Evolutionary biologists have developed hypotheses to explain the biased production of one sex over the other. For example, the Trivers-Willard hypothesis proposes that a mother who is in good condition and has lots of resources to pass onto her young will benefit by producing a son who gains an advantaged start to life and a better chance of becoming the alpha male that produces more offspring than a daughter could in a lifetime. On the other hand, mothers in poor condition lack the resources to invest in competitive sons but benefit by producing daughters who will reproduce even if they aren’t the best-conditioned female. A daughter is a safer bet than a disadvantaged son who may not grow big enough to outcompete larger males and sire any offspring.

The composition of milk and the sequence of changes throughout the life of the joey are most likely entirely driven by the mother and her body condition, and not by the joey. This was first recognised when researchers from Marilyn Renfree’s laboratory at the University of Melbourne took different aged Tammar wallaby joeys and swapped them to the pouches of other mothers raising younger or older offspring. Pouch young cross-fostered to a later lactation stage resulted in accelerated growth of the fostered joey, while those placed in the pouches of earlier lactation stages had significantly reduced growth rates.

Prior to our recent study on milk we found that if we cross-fostered Tammar wallaby pouch young of the same age but of different sexes, mothers who birthed a son had greater weaning success than mothers who birthed a daughter.This suggested that the lactating females had preferentially invested resources into male pouch young.

That study led us to our current work comparing the milk composition in wallabies raising sons with those raising daughters. We found that mothers allocated significantly more protein to their sons early in lactation than they did to their daughters. The significance of more protein to sons became most evident in their size differences at adulthood, with those sons allocated the highest protein gaining a significant size advantage over females and other males raised on milk containing less protein.

It has long been recognised that protein has direct relevance to growth in mammals. There is no short supply of protein supplements and protein shakes at the local bodybuilding gym. Likewise, mothers investing in protein-rich milk gain a fitness advantage with their sons being larger and stronger later in life, and hence having a better chance of becoming the alpha male.

We are currently following the paternity success of the sons allocated different protein in early lactation to establish if they truly do gain a reproductive advantage by siring more offspring.

We now have a greater understanding in this wallaby species that:

  • better conditioned mothers give birth to sons;
  • the mothers of sons have greater weaning success;
  • mothers allocate more resources to sons through higher levels of protein during early lactation; and
  • this allocation enhances growth into adulthood, which increases the chance that the sons will sire more offspring.

What we do not know is the initial maternal signal that influences the conception of a son or a daughter. Is there a cost to the mother in raising a son if conditions change? And what is the lifetime fitness advantage to choosing one sex over the other?

Kylie Robert is a lecturer in the Department of Zoology at La Trobe University.