Rock, Paper, Scissors, Lizard, Sex

Frequency-dependent selection explains the many kinds of male mating strategies.

Posted Apr 13, 2018

Warning: Contains sex-strategy fairy tales...

There are many different kinds of men, just as there are many different kinds of lizards.

In one species of lizard in Costa Rica, the side-blotched lizard (Uta stansburiana), there are exactly three kinds of males. Their three strategies for gaining access to the opposite sex help explain the variety of males you are likely to encounter in the world. 

The cool Dr. Charm attracts all the women but can keep none of them. The shy non-threatening McFly sneaks up on your heart. And the bog-standard vanilla men can muster a little violence when they need to stake a claim but aren't afraid to run away when the going gets tough.

The side-blotched lizard has a male counterpart for each of these kinds of human males. But how do such strategies stick around? Given the high stakes of evolution, and assuming these traits are heritable (which they are in the side-blotched lizard at h 2=.96), why doesn't selection eliminate the losers? And who are the losers anyway? Might they all be losers on different days?

Here are some fairy tales to help explain.

Sex-Strategy Fairy Tale Number One: The Rise of the Male Mistress (Misteress?)

You are a lord over a great territory. You have many wives. You keep one in every township, from here to the horizon. The greater your territory, the greater your number of wives. And as you travel to each township, you can lay with your wives and bring many copies of your DNA into the world. 

But you are greedy, and you grow your territory too large. To keep a large territory with so many wives, you kill all the threatening males who you feel might compete for your love.

Unfortunately, it becomes easy for your wives to keep a male mistress. In fact, they probably even need one because you are never around. The male mistresses are so unthreatening, no one ever suspects them. 

When you are old, one day you decide it is time to pass your kingdom on to your heir. You hold a great feast and invite all your wives and heirs. They come from all over the land and there is great revelry. 

In the grand throne room, standing at your throne, in front of everyone, you announce your first born, Jason, as your successor. Snickering ensues. 

"Why are you laughing?" you shout.

"Because Jason is not your son!" says one of your close wives. And soon, you discover, very few of the rest are either. The kingdom is thrown into sexual-conquest-fueled disaster, as the male mistresses come to power. 

Sex-Strategy Fairy Tale Number Two: The Rise of the Blue-Caped Duke

The kingdom is ruled by male mistresses and you are one of them. 

You are unthreatening because you are the child of a male mistress.

As you one day go out to meet your lover, a new duke with a blue cape rides into town. He points to the castle on the far hill and says, "I live there. I need a new wife and yours looks quite nice. She's mine now. Thanks."

Because the duke stole your wife, when you grow old and look to pass something on to your heirs, it turns out you have no heirs nor territory. Blue-caped dukes rule the land.

Sex-Strategy Fairy Tale Number Three: The Rise of the Fiery-Haired King

As a blue-caped duke, you proudly rule over your little fiefdom and ride to visit each of your seven wives, one for each day of the week. Because you are clever and aren't a card-carrying psychopath, you try to keep your harem small enough to manage.

Every once in a while, you pay a surprise visit to one your villages to make sure there are none of those male mistresses sneaking around.

But then one day as you are out riding, a colossal war machine rolls to block the path, with skulls hanging from the rear-view mirror and a great fiery-haired demon behind the wheel. As soon as he spots you and your blue cape, he shoots you between the eyes with a cross-bow. The end.

Your heirs, with their happy blue capes, are rounded up and hung from the trees all across the realm, the realm of the fiery-haired king.

Fairy Tale Debriefing

Sinervo & Lively (1996)
Source: Sinervo & Lively (1996)

These three fairy tales explain the three male morphs that Sinervo and Lively (1996) found in their study of the side-blotched lizard. Orange-throated males, high in testosterone, rule over large territories.Yellow-throated males look like yellow-throated females, have the least testosterone, and don't have territory. They are called 'sneaker males,' which is a common strategy across many species. Blue-throated males have medium levels of testosterone and have medium-sized territories.

Sinervo and Lively found that over a period of years, each of the different male morphs took turns winning the evolutionary sweepstakes and being in the greatest abundance. First, the orange-throated males ruled the land, then the yellow-throated males, then the blue-throated males, and then the orange-throated males again, and so on.

This evolutionary mechanism for maintaining diversity in a population is called frequency-dependent selection. In frequency-dependent selection, like in rock-paper-scissors, a rare strategy can win. If everyone else plays rock, you should play paper and win the day. But if paper starts to be the preferred strategy, then it's best to play scissors. And so it goes.

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Sinervo, B., & Lively, C. M. (1996). The rock–paper–scissors game and the evolution of alternative male strategies. Nature, 380(6571), 240.