On the Trails: The cost of making males

We humans are accustomed to thinking of reproduction as involving two sexes, male and female. But there are some animals that have dispensed with males altogether and produce offspring parthenogenetically (by ‘virgin birth’). This is true of some lizards, salamanders, fishes, and certain invertebrates, but no birds or mammals. If they can do it, why don’t we?

There would seem to be real advantages to parthenogenesis. A female would make all female offspring, like herself, and those offspring would do likewise. So if, for example, a parthenogenetic female made 10 offspring, and each of those made 10 more, and all of those also made 10, after just three generations, the original female would have 1,000 descendants.

Contrast that with a sexual female that also produces 10 offspring, but only half are female. Those five daughters each would make ten offspring but only five granddaughters and the twenty-five great-granddaughters would produce 125 female offspring. So the original female would end up with only 125 female descendants after three generations. At that rate, after many generations the sexual female would have a vanishingly small number of descendants, while the female descendants of the parthenogenetic female would dominate the population entirely (and males would be gone).

But that has seldom happened. (In fact, what then needs to be explained are the cases in which parthenogenesis has prevailed.) Why not?

Enter the Red Queen. Remember Alice’s many adventures in another world? When Alice meets the Red Queen, running along, the Red Queen says: Now, here, you see, it takes all the running you can do, to keep in the same place.

Some perceptive and wise biologists saw that no kind of organism lives in isolation from other organisms or the physical/chemical environment. There are therefore many interactions between any one kind of organisms and everything else. But ‘everything else’ is seldom constant — something will always be changing. To keep up with the many continuous changes, an organism has to change or get left behind and go extinct. Hence the Red Queen — changing just to keep up or possibly stay just ahead of the changes in ‘everything else.’

A parthenogenetic organism can’t do that very well, because all the descendants are identical (barring random mutations) to their ancestors. All of the females would be susceptible to the same diseases, or the same predators, or the same temperature fluctuations, for example, and would eventually be wiped out. (This, of course, begs the question of how the existing parthenogenetic organisms manage — do they live in special, unusual circumstances, or are they doomed to rapid disappearance?)

The invention of sexual reproduction — and the production of males — gets around the problem of uniformity. Sexual reproduction mixes up the genes in every generation. If a male and a female mate and produce ten offspring, it is very likely that all ten will be different from each other. Then, if the environment changes, there is a better chance that at least some of the offspring can meet the new conditions and survive, to reproduce in turn.

Thus, the cost of making males is that there may be fewer female descendants than is the case with parthenogenesis. However, those descendants are better able to cope with an ever-shifting environment. So, in the end, more of the sexual type will persist—and the ‘cost’ turns out to be worth it (for most organisms).

What are the kinds of changes that make sex useful in the long run? One can think of annual or decadal changes in weather patterns or predation risk, and all such may be important. But it turns out that arguably the most important changes are created by parasites!

There are probably more kinds of parasites in the world than any other kind of animal. Many of them have the ability to multiply non-sexually, in between episodes of sexual reproduction, so they can become very numerous very quickly and have a big impact on their hosts. Bad news for the hosts, especially if they produce parthenogenetically.

However, if the host can reproduce sexually, some of its offspring might escape the onslaught of the parasites. In fact, certain species are parthenogenetic in some populations but sexual in others. Clear demonstrations of the advantage of sex come from (for example) studies of New Zealand snails, which reproduce parthenogenetically except in populations that are afflicted with parasites; the afflicted populations produce males and reproduce sexually.

Not all animals can reproduce both sexually and parthenogenetically. Most multicellular animals have foregone the potential advantages of permanent parthenogenesis and reproduce only sexually. Why? One reason might be that the parasites themselves often have episodes of sexual reproduction, which allows them to keep up with changes in their hosts. The Red Queen works both ways! This might make the permanent adoption of sex advantageous, particularly for animals that are sufficiently large and complex to host many different parasites that occupy all the various nooks and crannies of their bodies. It takes a lot of ‘running’ to keep up with all the parasites, which are playing the same game!

• Mary F. Willson is a retired professor of ecology.


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