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Frontiers
Reproductive Ecology Stacking the Deck In the Game of Life

January 1996

Boy or girl? Many of us won't admit to having a preference.

Yet other mammals, including some primates, sometimes have a distinct preference for offspring of one gender or the other, depending upon the conditions for survival. Their bodies make sure they get what they want.

Strange but true.

"Parents who can adjust their reproductive investment to favor young of a particular sex may do so when environmental or social conditions favor the survival and fecundity of one sex over the other," according Martha McClintock, an animal biologist at The University of Chicago, whose research program was initiated and sustained with NSF support. McClintock and other animal biologists are funded through NSF's Directorate for Biological Sciences.

This sort of adjusting is called sex ratio biasing. Until recently, it was more theory than proven fact. But when scientists began observing animals in their natural environments--that is, outside the typical laboratory--sex ratio biasing became evident.


Baboons in a tree

In baboon society, daughters inherit their mothers' rank but sons earn their rank.

Credit: Jeanne and Stuart Altmann

Here is how it works: Over time, a species' male-to-female ratio hovers near 50-50. The balance may shift at any particular time, however, depending on the stresses--or the relative absence of stress--in the species' ecological and social environment. The shifts, which McClintock and her student Leslie Hornig would call "adjustments of the reproductive investment," serve the ultimate goal of improving the individual's chances for having more surviving grandchildren. Grandchildren are important since, genetically speaking, the ultimate goal of life is to reproduce and have those offspring long enough to reproduce as well.

VIVE LA DIFFERENCE

To understand how the balance between the ratios shifts, consider the basic reproductive differences between male and female rats. Most female rats reproduce at regular intervals, having several litters per breeding season. A male rat, on the other hand, may mate with many females if he is a dominant male, or may fail to mate entirely if he is not dominant.

When food is plentiful, male and female offspring are produced in equal numbers. In times of famine, female offspring predominate.

The reason is that when food is scarce, both mother and offspring are weak. A son is not likely to grow strong enough to become a dominant male. A weakling son probably will not mate often. In stark genetic terms, he is hardly worth the effort. On the other hand, daughters--even weak ones--are likely to reproduce.

Therefore, when pregnant females are consistently hungry or otherwise in less than tip-top shape, they simply abort male fetuses at an early stage.

With her laboratory full of Norway rats, McClintock worked on the stress theory and a corollary--mothers who give birth to pups out of sequence with the rest of the pack are likely to have a female bias in their offspring.

McClintock and her students Mark Blumberg and Julie Mennella found that mother rats suckle their cohorts' pups, sharing their milk and food to the benefit of all. A pup born out of sync is at a disadvantage because there are no surrogate mothers around. As in times of general famine, mothers reproducing out of sync tend to abort potentially weakened and costly sons. They produce the same number of pups per litter, but the litter is female biased.


McClintock with a rat

Martha McClintock studies rats to learn how external conditions, such as social behavior, influence gender ratio in a litter. (This rat is a pet, not a research subject.)

Credit: Steve Kagan

WE WANT YOU TO FEEL AT HOME

To study the rats' sex lives and maternal behavior, McClintock abolished most of the usual laboratory cages and gave her naked-tail subjects the run of the place. Her Norway rats -- normally residents of alleys, dumps, and sewers -- make themselves at home in her lab's plethora of pipes, newspapers, and other trash.

The rats need to be in a comfortable environment, says McClintock, or she cannot get an accurate look at their reproductive behavior. In fact, she has obtained a $2 million grant from NSF to help build an animal-friendly research facility dedicated to biophysiology.

With the rats in their semi-natural setting, she and her student Sarah Bacon have found that sex ratio is affected by such variables as:

  • Timing of insemination. Males are more likely to be born from inseminations that precede ovulation, while females are more likely to result when insemination and ovulation coincide.

  • Number of other suckling pups. When pups suckle during pregnancy, the proportion of males in the next litter is higher than when there are no suckling pups present.

  • Size of litter. In large litters (more than 13), the number of females increases while the number of males stays at the average.

ANOTHER APPROACH: SUPER MOM

Some mechanisms for sex ratio biasing may originate in the generation prior to the one that needs them. A former NSF grantee John Vandenbergh of North Carolina State University found that sex ratio biasing in house mice is influenced by the experiences of the mother herself in utero.

In most animals, humans included, the female brain is the basic model. Males develop their own distinct brain circuitry only after being bathed with testosterone.

Females surrounded in the womb by male siblings also get hit by testosterone. These so-called "masculinized" females grow up to be more aggressive than other females, and they maintain a bigger home base or territory. Masculinized females also have more sons, relative to daughters, than do other females.

In good times, when food and other resources are plentiful, masculinized females have no reproductive advantage--males do not seek them out.

But when populations are large and food is scarce, the advantage goes to mice ready to fight for food, and the masculinized female comes out on top. Since she can provide for herself and her offspring more effectively than her more feminine cousins, her sons stand an improved chance of growing up to be strong, dominant--and reproductive--males.

RANK HAS ITS PRIVILEGES

Another long-term NSF-funded study brings sex ratio biasing closer to home--to homo sapiens, that is.

Jeanne Altmann of The University of Chicago has examined social pecking orders among our not-too-distant relatives, baboons.

She has learned that top-ranking female baboons have first choice of best foods and reproduce at the youngest ages. For females, rank and its privileges are crucial.

Baboon mothers, consciously or not, pass on their rank to their daughters, who keep it for life. Sons, on the other hand, switch ranks several times during their lives.

Altmann theorized--and then proved--that this societal setup realigns the original goals of parents playing the gene game. It should be beneficial for top-ranking females to have daughters, so that the daughters get the all-important rank that enables them to eat and breed well. This in fact occurs.

Low-ranking females, on the other hand, are better off having sons, since sons have a shot at becoming dominant, reproductive males. Again, the evidence bears this out.

THE HUMAN ANIMAL

Humans are not above all of this. Nobody knows for certain how much sex ratio biasing takes place, but some of Martha McClintock's discoveries about rats certainly have parallels among homo sapiens. As with rats, the probability of having a son or daughter changes with the timing of the insemination -- sons are more likely when insemination occurs several days prior to ovulation. Chances of producing a daughter increases as insemination approaches the time of ovulation.

Hundreds of other possibilities remain to be explored. To Altmann, the point is to notice animals' sensitivity to stress in their lives. Unless we live in a stress-free corner of the globe, our bodies may well have similar response mechanisms.

While choosing the gender of a fetus with any accuracy may still be a ways off, we now know that the likelihood of having a son or daughter is more than a mere flip of the coin. For humans, like baboons, rats, or mice, it may well be an unconscious choice in the game of life.


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