Most of you won’t know who Whitey Bulger is. He was for a while on the FBI’s ten most wanted list. He spent a lot of time overseas running from the Feds, but they eventually caught up with him, convicted him, and tossed him in jail.

Whitey was top dog in Boston’s Winter Hill gang. His brother was a Senator for the Commonwealth of Massachusetts, and served as Senate President for several years.

It is said that Whitey was an FBI informant, and that his handler, FBI Special Agent John Connolly, tipped Whitey off that he was about to be indicted on racketeering charges. No problem. Whitey had left stashes of cash in safe deposit boxes all around the world, in preparation for the day he had to go on the lam. So he took off in 1995. Special Agent Connolly spent several years on vacation in the stir.

I remember when Whitey disappeared, and ever since then, I’ve used him almost annually in lecture material describing the Trivers-Willard hypothesis. It goes like this:

The Trivers-Willard model (I prefer to call it a “model” rather than a “hypothesis” because it is not specific enough to really be a hypothesis … it’s a model that generates lots of hypotheses) states that selection should favor the ability to differentially bias investment in offspring by sex if the two sexes have differential variances in reproductive success, and if there is any way to predict offspring rank. That’s a bit thick, so it requires some examples and further explanation. Maybe a story about a mobster would help..

OK, so an example: Red deer (also known as Elk) give birth to one offspring (max) per year. Males compete for access to or to be chosen by females. So, only a small percentage of male red deer mate in a given year, a significant percentage may never mate at all, and a very small percentage sire many many little red deer. Male red deer have a high variance in reproductive success. If you tried to predict how many offspring a given randomly chosen male would have, knowing nothing at all, your best guess would be the average number of offspring red deer have in an average lifetime. But you would be wrong almost every time because the actual number is highly variable. Male red deer have high variance in RS.

Females, on the other hand, have a pretty standard number of offspring. There is not much competition among them, they can always find a male to mate with, etc. If you needed to guess how many offspring a particular randomly chosen female red deer would have in a life time, you could guess the average, and you would be right on or very close. Female red deer have low variance in RS.

So, male and female red deer have differential variance in RS. Males high, females low.

If a female red deer could somehow “predict” the likelihood of her offspring getting to mate, i.e., if she could tell if any offspring she had in the present year (male or female) would be average vs. high ranking, then selection should favor the evolution of a mechanism to actually give birth to the appropriate sex offspring (thus biasing investment in one sex or the other). It turns out that she can. A female red deer that is herself average or lower-quality (thin, ill, injured) is likely to give birth to an offspring that will be either low ranking or average. But if the mother-to-be red deer is high ranking, she is likely to give birth to an individual who will grow up to be high ranking.

Under these conditions, she should have a female offspring if she’s average or low ranking, but a male if she’s high ranking. And that, it turns out, is what red deer actually do.

That should be clear. But in case it isn’t, let’s take it down do real life, and bring in the gangsters.

You check the mail this afternoon, and there is a letter from a law firm you have never heard of. It says that your Great Aunt Tillie (whom you’ve also never heard of) just died, and left you with $1,000 in her will. The check is enclosed.

This may or may not be a recent photograph of a male red deer. Holy crap. Found money! What are you going to do with it? So you and your close advisors (your roommates, your cat, etc.) discuss it and you narrow it down to two choices. Choice A and Choice B.

Choice A is to go to your broker and buy $1000 worth of a nice, relatively safe mutual fund. The fund will buy and sell reliable blue chip stocks, thus spreading the risk over several companies, and over time you can expect to get a return of 50 bucks a years, easy.

Choice B is to buy 1000 one dollar lottery tickets. Your chances of winning are slim, but if you do, you will win 87 million dollars.

So, what do you do? The obvious sane choice is to buy the mutual fund.

But what if your cousin is Whitey Bulger? Whitey Bulger, as head of the Winter Hill Gang, is said to have owned the director of the Commonwealth Lottery agency.The connection between Whitey Bulger and the Lottery has never been proven. They don’t have a shred of evidence. He was, however, indicted for 21 counts of RICO-Murder. It is said that one of the things that tipped off authorities about this is that some of his relatives were winning the lottery a little more often than they should have. So, say your cousin is Whitey Bulger, and last time you saw him (at a family wedding) he told you … “hey, if you ever want to take a “chance” on the lottery, let me know … I can make that work for you…”

So now, you have two choices.

Choice A: Invest in a mutual fund and gain a return of 50 bucks a year (that’s dollars, not elk); and

Choice B: Buy 1000 PowerBall tickets and have a great deal of certainty of winning 87 million dollars.

What would you do?

In case it isn’t already clear. the baby male elk is a lottery ticket, the baby female elk is a mutual fund, but the female can guess pretty accurately if the lotter ticket (male offspring) will pay off. Because the elk’s cousin is Whitey Bulger. See?

This could be why what has become (inappropriately) known as “reversed sexual aggression” often goes unnoticed, and a recent study of the African antelope Damaliscus lunatus (a.k.a. “topi”) explores this possibility.

Consider mammals. Mammals have internal fertilization, so there is little opportunity for males to make much of an investment in offspring. Females gestate the young and then lactate to provide additional nutrition. So, females end up making most of the investment in offspring, or at least, a lot more than males do, in many species of mammal. Also, it is physically possible for a male to inseminate a fairly large number of females all of which can theoretically have that male’s offspring, while females reproduce at a much slower rate with fewer mates.

Herein lies the basis for most of the persistent sex differences we see in mammals. However, the totally obvious nature of this relationship between mammalian males and females, and the dramatic way in which it usually plays out, has caused scientists to loose sight of the fact that males do in fact pay reproductive (especially mating) costs. The article we are looking at now speaks mainly of sperm depletion, but there are two other major and obvious (though often overlooked) costs that males may suffer. One is direct competition. Mating may seem like a good idea at a particular moment, but the other male, the one that is not you, but has a similar idea and big antlers, horns, tusks, or claws, may hurt you for even having that thought.

I am told that for every male monkey on Cayo Santiago, a major Macaque colony off Puerto Rico, there is something like 1.7 testicles. The costs of mating can be significant.

The other major cost is the risk of venereal disease. It simply is not the case, despite rumors to the contrary, that venereal disease is a curse placed on certain humans by god. It can be safely assumed that all animals that have sexual contact are host to a suit of microbes that use this contact as a means of dispersal. When the microbes (and I use that term loosely … I mean viruses, bacteria, and protists, yeasts, fungi, the whole shebang) make you sick, it is called a venereal disease. When they don’t, well, we don’t call it anything generally because we don’t even know about it.

Anyway, there are real costs, and as a result of this, it is not always case that the optimal mating rate for males is infinity (though it sometimes seems that way). Since females are, and should be, choosy about males they mate with, they may also be in competition with each other. So the pattern of demure females observing males in competitive tournaments (head butting, horn locking, pissing contests, etc.) is not the only possible pattern.

According to the author of this report…

…in promiscuous species, females might benefit from high mating rates as a result of increased conception probability with favored males, whereas favored males benefit from mating selectively because of sperm depletion. When this results in higher optimum mating rates for females than for males, there is potential for reversed sexual conflicts between persistent females and resistant males. Here I report evidence of such a reversed sexual conflict in a promiscuous antelope, the African topi. Rather than mating randomly, favored males prefer to balance mating investment equally between females as predicted by strategic sperm allocation theory. Females, however, enhance their probability of mating with favored males through aggression toward mating pairs.

If a female is likely to mate with multiple males during one reproductive bout or season, there will be sperm competion. Sperm competitive capacities are thus selected for, so it is in the interest of a female to enhance competition as much as possible. The best way to do this is to mate with more males.

From the male perspective, it may make sense to mate many times with one female (lots of sperm) but it also makes sense to avoid mating with a previously mated female and mate with a new, different female. The male is weighting the trade off between winning the Sperm War being waged within one female on one hand vs. engaging in a novel opportunity on the other.

This leaves open the possibility that the female optimum and the male optimum are in conflict in the “opposite” relationship than they usually are in mammals.

This paper is a fairly sophisticated yet understandable exposition of a model of these conflicts. The system is described as having two theoretical traits … persistence and resistance. Commonly, among mammals, one expects persistence to be favored in males and resistance (choosiness) to be favored in females, but it would be incorrect (possibly) to assume that only one trait exists in each sex. Both exist, but one is typically overwhelmingly expressed (the traits in a sense, compete within the model).

Topi lek. Yes, that is a sentence. Topi have a lek system of mating, which is where males hang out on a “lek” (a place of no consequence other than as a breeding ground) and compete for position within the lek. Position is thought to reflect quality. The animals may also display traits that also reflect quality. Females pick a male to mate with on the lek. In many leking species, all the females tend to pick one or a small number of males. It could be partly because in Topi the females come into season almost at the same time (over a few weeks) that they actually mate with a larger number of males … sperm competition comes into play. Having a system with both lekking and sperm competition, and seasonal mating to boot, is fairly uncommon.

Under these conditions, you have such intense sperm competition that resistance may be selected for in males, and persistence in females. That is indeed what seems to happen with the topi.

BRO-JORGENSEN, J. (2007): Reversed Sexual Conflict in a Promiscuous Antelope. Current Biology, , doi:10.1016/j.cub.2007.11.026 .