Sex is for the Greater Good

Allegedly, men think about sex once every seven seconds. While this may seem like an exaggeration, regardless of gender, it’s likely an underestimate if you’re a life history biologist. I grew up as a graduate student in a life history lab, and trust me, there’s no end to the number of sex jokes that can be made when you’re talking about reproductive strategies that involve sneaker males or massive orgies among reef corals. However, all this thinking about sex comes to good use when they address one of the most intriguing topics in this field—why do organisms engage in sexual reproduction at all?

Moreover, how is sex as a reproductive strategy maintained over evolutionary time? Like many things in biology, we often assume that if a trait is widespread, then it must be advantageous. Such is the case for sex—most multicellular organisms engage in at least some form of sexual reproduction, so it must be advantageous, right? Not so fast. As with any trait, the existence of the trait does not imply adaptation. Most humans have an appendix, but it’s not an adaptation in the current environment in which we live. So is the same true for sexual reproduction? Is sex just a vestigial trait, like an appendix, or is it advantageous in some way? If it’s not advantageous, then why did sex ever evolve in the first place? It must have provided an advantage at some point.

A recent article in Ecology Letters by Jeremy Gray and Matthew Goddard (“Gene flow between niches facilitates local adaptation in sexual populations” vol. 15: 955-962, 2012) does a great job of laying out the theory behind why either sexual or asexual reproduction might be advantageous under certain conditions. Based on first principles, asexual reproduction should be twice as advantageous as sexual reproduction because an organism can pass along two copies of its genes instead of just one. So if a sexual organism is going to outcompete an asexual organism in the evolutionary game of “Who’s Most Fit?” (the fittest being the one who passes on the most copies of its genes), then it has a two-fold disadvantage to overcome.

Some genes are linked because they occur on the same chromosome. If the gene for blue eyes and the gene for blond hair are on the same chromosome, then most people with blue eyes should also have blond hair, and vice versa. But sexual reproduction can break down those linkages. During recombination that occurs during chromosome duplication, genes can jump between paired chromosomes, such that it’s possible for a blue-eyed, blond mother and a brown-eyed, brunette father to have a kid with blue eyes and brown hair. Now let’s say that blue eyes are a disadvantage, but blond hair is an advantage. One advantage to sex is that, by breaking down those linkages between genes, selection can act on eye color and hair color independently, because those traits are no longer completely linked to one another. People with brown eyes and blond hair can have higher fitness, but that wouldn’t be possible unless those gene linkages are broken down by sexual reproduction.

Related to that, another advantage of sex is that it increases the genetic variation in the population. Genetic variance is the fuel for natural selection and natural selection underlies any adaptation. If everybody in the population has the same eye color, then selection can’t act on eye color because everybody has the same fitness. There’s no advantage to a different eye color if the different eye color doesn’t exist! But when gene linkages are broken down, it creates a lot of different “looks” (or phenotypes) in the population. If we just think about eye color and hair color, the breaking down of linkages between those traits takes us from two phenotypes to four phenotypes. So sexual populations may be able to better adapt to an environment because sex introduces novel variants into the population and natural selection that acts on that variation is more likely to occur.

This advantage of sex might be favorable if the environment is either constant or only changes every once in a while. If the environment is constantly changing (e.g. more often than one generation), it becomes really hard to adapt to any particular set of conditions. Just as adaptation is starting to occur, the environment switches, and the adapted trait is no longer adaptive. However, there’s some evidence that asexual populations do a better job of adapting to these changing environments. Some individuals do well in one environment, while others do well in the other environment. This sets up a negative correlation between the genes that do best in either environment (in the biz, we call this linkage disequilibrium). Keeping with our example, blue eyes do well in Environment A, but not in Environment B. Likewise, brown eyes do well in Environment B, but not in Environment A. Depending on the environment, there are always some individuals that do best in that environment.

The problem with sex is that it breaks down this correlation. It mixes up all those associations among genes and makes it so that a greater number of offspring are maladapted. By chance, everybody probably has at least one trait that isn’t so useful in the current environment. So if sex makes adaptation difficult, then is there still any advantage to sex? Well, one argument says that sex can still be advantageous, but only if there is no gene flow between environmental niches. In that case, population A can adapt to environment A, and population B can adapt to environment B. But if there is any significant gene flow between the two populations, then linkages among genes breakdown and the advantage of sex is lost.

So that was a really long set up to this really cool paper by Gray and Goddard (who lay out the above arguments very nicely). They set out to test the advantages of sexual and asexual reproduction using populations of yeast. There’s a whole bunch of preliminary research that went into establishing the environments and populations needed for this experiment that I won’t go into here. Basically what you need to know is that there are two niches that affect the performance of yeast [I’ll call them niche A (cold, salty, and nitrogen-limited) and niche B (hot, non-salty, and carbon-limited)]. Furthermore, they have genetically engineered (by knocking out a few genes involved in sexual reproduction) two populations of yeast that are identical except for whether or not they reproduce sexually or asexually. They then set up an experiment in which sexual and asexual yeast evolve in both niches. Additionally, they create gene flow among replicate populations by transferring some yeast cells from culture to culture every so often. (Actually they used several levels of gene flow, but it turns out that the amount of gene flow doesn’t matter at all to the outcome of the experiment). The point of the gene flow is to force organisms to experience both environments as they evolve (i.e. heterogenous environment). After hundreds of generations of evolution under these conditions, they measure the competitive ability of sexual strains of yeast against the unevolved yeast.

Based on the arguments I’ve just told you above, I expected that sexual populations would outperform asexual populations, but only when there was no gene flow among the two niches (i.e. a homogenous environment). In a heterogeneous environment (or when there is lots of gene flow between environments), sex should be a disadvantage, and the asexual populations should win. It turns out this reasoning is all wrong. The sexual populations win every time! They do well in the homogenous environments (i.e. no gene flow) for all the reasons we expect—they adapt to either niche A or niche B. But it turns out they also do well in the heterogeneous environments (lots of gene flow) for a reason that had not been foreseen by all the theory on this subject. In the heterogeneous environments, generalists evolve. Those organisms with the right combination of genes that allow them to do well in both environments have the highest fitness. However, there is no opportunity for these generalists to evolve unless there is some amount of gene flow so that they experience both niche A and niche B. Otherwise, there is always selection for specialists in the particular niche.

In hindsight, this makes perfect sense. And I think that’s the best thing about science… Every time we discover something, it makes perfectly logical sense because nature and evolution work on sound logic. Sometimes we just didn’t have enough information (or hadn’t yet thought hard enough) to realize why that particular outcome makes sense. Life history theory is a great example of a field where people develop theory, test that theory with experiments, and then revise the theory with newfound knowledge….and then test it again! It’s the scientific method that we all learned in 6th grade science. It still works! Yay science!

Casey terHorst

About Casey terHorst

Casey is a community ecologist interested in how species interactions are affected by genetic variation within species and evolution that occurs on ecological time scales. He is currently a post-doc in Jen Lau's lab at the Kellogg Biological Station. In the Fall, he will be starting as an Assistant Professor at California State University, Northridge.
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