Sex at the limits and the limits of sex: Baker's Law
Some of the central ideas of my PhD that I found in an old folder, thought were pretty good, and polished up for blog form.
This piece was originally a draft ultimately intended for academic publication, but I removed highly technical parts, all citations, and any caveats that distract from the story for a general audience. I may add more appropriate explanatory links for a general audience later on.
In many plants and some insects, self-fertilization and asexuality tend to be more common at the edges of the species range. This is referred to as Baker’s Law. We can ask, “Why are self-fertilization and asexuality more common at the margin?” but it is more evolutionarily appropriate to ask “Why does the core population bother with sexuality at all?” After all, sex is expensive. For a typical animal, sex requires locating and attracting a mate, more difficult still locating and attracting a mate that isn’t a close genetic relative, and producing expensive gametes that won’t all be used. Even after successfully reproducing, each offspring carries only 50% of the parent’s genetic material and on average half of the offspring will be, in the words of John Maynard Smith, “frivolous” males that will not spend their reproductive effort on producing offspring by merely contributing chromosomes. For a typical plant, outbreeding requires elaborate sexual structures to produce pollen and seeds, most of which will never germinate, expensive floral advertising and production of nectar or extra pollen to attract pollinators, and all without any guarantee that their pollen will reach a receptive stamen.
Viewed this way, self-fertilization and flat-out asexuality seem like logical choices at any point in the species range. Self-fertilizing plants can thrive where they grow, regardless of the distribution of sexual relatives and their pollinators. An asexual organism can dispense with costly sexual structures altogether and put the liberated energy directly into producing more offspring that each carry 100% of its genes. Each asexual offspring in turn has higher reproductive potential than sexual offspring. By slashing the costs normally incurred by sex, asexual individuals should quickly out-compete their extravagant sexual relatives. And, yet, this is not what we see in nature.
Despite the seeming energy savings and reproductive boon afforded by asexuality, it is not the norm across Eukarya. Furthermore, the phylogenetic distribution of asexuality is “twiggy,” meaning the asexual eukaryotes we know today (with the interesting but increasingly unlikely-looking exceptions of Rotifera and Darwinulidae) developed the trait only recently, tend to have close sexual relatives, and, presumably, that asexual lineages that arose in the past did not survive. Clearly, there is something that justifies the cost of sexuality for most eukaryotes and vindicates the strategy of genetic recombination over the course of time.
In 1889, August Weismann provided one of the earliest attempts to explain the benefit of sex, suggesting that it generates variation among individuals upon which natural selection can act. Another classic explanation of the tendency of asexual lineages to fizzle out over time is Muller’s Ratchet. In an asexual population, the mutational load “ratchets” up with each new mutation as inherited mutations accumulate with each successive generation. In a sexual population, a mutation can arise in an individual lineage without dooming all of its future progeny to carry it—the individual’s other genes may disentangle themselves from the harmful mutations, and the mutation may eventually be lost by drift or purifying selection without taking the rest of the individual mutant’s genes down with it. If two harmful (unlinked) mutations arise in a sexual lineage, that lineage will likely still produce many offspring that have neither mutation, some that have one, and only a few that have both. The lucky few without either mutation will have a reproductive advantage. Recombination might also create individuals with both mutations, and they will face a reproductive disadvantage. Double mutants are more likely to be selected against, and the loss of the mutations does not doom the rest of the genome in which the mutations arose.
Why not have the best of both worlds, then? Asexuality to grow quickly and colonize new range and occasional sexuality to mix things up when the mutational load has been ratcheted up? In fact, many species do. Many fungi, for example, reproduce so predominantly asexually that it was not even known until recent decades that they had the capacity for sexual reproduction. How often these species engage in sex and how the capacity for sex is maintained despite periods of inactivity are interesting questions that may shed further light on the ultimate utility of sex. Unfortunately, however, for many species, it is difficult if not impossible to go back to sexuality from asexuality. Even if the initial switch from sexual to asexual did not preclude future sexuality, generations of successful asexual reproduction allows the deterioration of the expensive sexual and meiotic structures that contributed to the energy cost of sex. In fact, mutations in these now unused genes that freed up more energy and resources to go into reproduction by preventing the investment of energy in the development of sexual features are likely favorable as far as natural selection is concerned in an asexual population because they increase the reproductive success of the bearer. Therefore, it seems likely that eukaryotic asexuality, when it has arisen in the past, has been a spark that quickly dies.
What about self-fertilization, then? Going through the motions of meiosis and fertilization keeps all the structures in working order but saves the effort and uncertainty of mating with a partner. If, by some good fortune, a plant in the habit of self-fertilizing finds a genetically distant partner, it is ready for sex, but it hasn’t been holding its genetic breath. Baker, of Baker’s Law, proposed that self-fertilization is more common at the margin merely because those individuals were more likely to survive and reproduce there in the absence of available mates. This seems simple enough—tautological, even. But, if this is true at the margin, why is it not also true at the core? Why don’t self-compatibility alleles invade the core of the species range, where more favorable climate and abundant resources should make them even more successful? What differences are there between core and marginal habitat that lead again and again to this distribution of self-tolerances? What’s more, if Weismann were right, we would expect to see exactly the opposite pattern: sexuality and outbreeding producing high variation to cope with new conditions outside of the species’ comfort zone and asexuality or self-compatibility thriving in the more established core habitat.
Perhaps asexuality and self-compatibility are merely side-effects of properties that truly are beneficial at the species range limits but not at the core. For instance, hybridization or autopolyploidy can create polyploids more tolerant of extreme conditions than the parent species but whose only options for reproduction are self-fertilization and cloning. Agricultural crops tend to have high ploidy, perhaps because the associated traits, such as larger cells, originally made them easier to cultivate. Perhaps self-fertile and asexual individuals thrive at the range limits because they can adapt to the different local conditions without being “swamped” by gene flow, which would include genes for core-specific strategies, from the core population. Dandelions, for example, come in sexual and asexual varieties. The sexual varieties have a smaller range, whereas the asexual “clones” (here a clone refers to the entire genetically identical population) that are spun off every so often tend to be found further out— a pattern called geographic parthenogenesis. The asexual dandelions often cover more area than the sexual populations, but eventually the clones all die out.
Because mutations are vastly more likely to be harmful than beneficial, the process of Muller’s Ratchet generally leads to the accumulation of harmful mutations. But, surely, sex, by recombining different alleles, occasionally breaks up favorable combinations. What if a fortuitous combination of alleles allowed a rare individual to thrive at the edge of the species range—the only way this combination of alleles could persist is if that individual was also capable of self-fertilization or parthenogenesis. Perhaps the preservation of this suitable combination of alleles in a selfing or asexual individual is what made them thrive at the range limits. If self-fertility increases the capacity for local adaptation, this may be why successful marginal self-compatibility alleles don’t re-invade the core habitat—they are not superior competitors in core habitat despite their potential comparative reproductive advantage. If local adaption (or adaptation to self-fertility or asexuality) makes backcrossing difficult or impossible, this is a barrier to reproduction that could herald a speciation event.
Though the ideas presented thus far may explain proximate causes of Baker’s Law, they do not explain what appears to be an inherent value in sex and outbreeding. If the capacity for sex can be maintained even when sexual reproduction is dispersed between several asexual generations, why, then, are so many plants and animals obligately sexual outbreeders? The Red Queen Hypothesis puts forward a reason that variation may be favored for variation’s sake: constant genetic shuffling is the only way to “keep in the same place” in the constant arms race with parasites and other competitors. This could explain why self-fertilization and asexuality are permitted in higher frequencies at the margin than at the core. Many parasites are density-dependent and so a sparse, marginal host population is, in turn, a marginal habitat for them. The density-dependence of pathogens is one reason that Europeans transmitted so many diseases to pre-Columbian American peoples but not the other way around— their lower population densities over a long period of time meant that they had not supported the evolution of as many pathogens. At the margin, where the population is leaner and conditions slightly different, perhaps the pressure of Red Queen dynamics temporarily abates, allowing some self-compatible or asexual individuals to reap the energy savings without contending with the competitive forces at the core. Perhaps sexuality is an expensive and hard-won adaptation to constant competition for resources, a burden that is quickly and easily shirked when conditions allow. This might be why sex is an obligation for so many eukaryotes— those that weren’t obligated are dead or dying.
(Standard disclaimer— for instance I may go back and add links.)