LECT15ev2021 - Notes on Muller\'s Ratchet, and the eNoevolution of sex, PDF

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Notes on Muller's Ratchet, and the eNoevolution of sex,...

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BIOS 317 - Evolution - Spring 2021 Lecture 15 (17 February) What is Muller’s Ratchet? How can sexual and asexual populations evade Muller’s Ratchet? How does sex lead to faster rates of evolution? How is sex favored in a changing environment? How does sex favor “selfish” genes and organelles? How did sex and recombination evolve? Evolution of Sex Keep in mind that here we are not focusing on sexual selection (when a member of the same species acts as a selective agent); here we are focusing on the evolution of whole cell fusion and whole genome recombination. Sexual selection came later, and we’ll discuss it as part of the “selection and adaptation” part of the course. Be that as it may, sex is clearly not necessary for reproduction in many extant organisms, and sex likely originated rather late in the history of life with the origin of the eukaryotes. Since sex is not necessary for reproduction, we are led to consider the Maynard Smith paradox that shows the reproductive advantage of asexual females (Fig. 8.23): imagine a population founded by 3 individuals, a sexual female, a sexual male, and an asexual female. Every generation each female produces 4 offspring, after which the parents die…. The asexual female produces all asexual females, while the sexual female produces males and females in equal numbers. Fraction of the population that is asexual doubles in just two generations! Given the Maynard Smith paradox (Fig. 8.23) and the “two-fold cost of sex” for sexual females relative to the reproductive advantage of asexual ones, yet the widespread occurrence of facultative sex in every eukaryotic clade, there must be advantages of sex to outweigh the obvious costs. What is the advantage of sex? First let's focus on the maintenance of sex (versus its origin): as Lane does in chapter 5 (note this is the first readings from Lane’s book), it is useful to organize the explanations in terms of the level that evolution acts on: (1) sex may benefit populations (like not having any cannibals), (2) sex may benefit individuals (e.g., evolution in changing environment—many tickets in a lottery is better than many copies of the same ticket), (3) sex may benefit genes (or organelles) (e.g., mobile genetic elements are spread by sex, even ordinary genes can get into new chromosomes by recombination during sex, organelles can move between cells subsequent to whole cell fusion). Evolution can act simultaneously on all these levels (population, organism, organelle, gene), and there need not be conflicts

between selection acting at each level. In fact most or all of the explanations likely act synergistically at more than one level. H&F don't recognize levels of selection and their arguments mix and match selection acting at different levels, but they do make a worthwhile point: In the context of population genetics, sex means genetic recombination, and the advantage of sex is to diminish L-Deq; selection at individual and population levels can favor traits that diminish L-Deq, such as sexual reproduction. And recall that for closely linked gene loci, selection or drift/mutation or migration can cause L-Deq. Linkage Disequilibrium (L-Deq) and Drift/mutation: We've seen that if drift acts on a combination of traits controlled by different loci, L-Deq is the result. The role of sex in countering L-Deq caused by drift is termed.... Muller's Ratchet. (after HJ Muller, a student of TH Morgan, and an adherent to the classical view of genetic variation) Consider a finite (of measurable size) asexual population in which every locus bears the allele that is best suited for the current environment. Because of copying errors, there will be an inexorable increase in the number of deleterious mutations; since each deleterious mutation has a small negative effect on fitness, selection will of course oppose this increase (note that selection has a role in Muller’s Ratchet, eliminating the unfit). These are loss-of-function mutations, so back mutation rates are small in a finite population. Recall that when mutation and selection are in equilibrium (q hat = u/s), there will be an optimal, "least-loaded" class of genotypes that will represent a small fraction of the population (figure 8.27). Though these individuals have a high fitness, the difference in fitness between individuals with no mutations and those with 1 or 2 will be small, so the numbers in this optimal class will vary merely by sampling error in a finite population and will undergo a "random walk" (e.g., recall genetic drift, e.g., Figure 7.15). Eventually, by genetic drift the number in this class will reach zero. Mutation-selection equilibrium will continue with a new "least-loaded" class of genotypes, but this class will have 1 more mutation. Again this class will be small and drift will occur until this class too is lost. Similarly for the next least-loaded class, and the next. Finite asexual populations incorporate a sort of ratchet mechanism and can never bear fewer deleterious mutations than are currently present in the least-loaded class of genotypes. They are therefore doomed to progressive loss of adaptation and eventual extinction. (to phrase this more in terms of L-Deq: deleterious mutations at 1 locus become associated with deleterious mutations at other loci by chance events.) Bacteria usually evade Muller's ratchet by having essentially infinite, limitless populations: least-loaded line is too large to experience much genetic drift and also in a large population back mutation, gain-of-function can have an appreciable effect....

Finite sexual populations might also avoid this deadly ratchet. Recombination breaks up associations between deleterious alleles. Gametes produced by recombination will vary, some bearing many deleterious mutations, some bearing few. The zygotes produced by fusion between heavily-loaded gametes will have low fitness, and their death will rid the population of many deleterious mutations simultaneously. Sex produces variation and in combination with selection can restore the original vigor of the population. George Bernard Shaw quote and… Another population-level example from Lane shows the advantages of sex with respect to rates of evolution; spread of favorable mutations in a population...Figure 5.1 in Lane (Maynard Smith and Szathmary slides); again sex diminishes L-Deq in this case caused by mutation/drift here with favorable mutations and this leads to faster rates of evolution; “selective sweeps” and EHH can occur rapidly. It starts off with an association between A and b and c, and an association between B and a and c; this association is broken by recombination and the recombinants, first AB, then ABC, are favored by selection. (Further selection will thus again increase L-Deq in the population.) In the asexual population this cannot happen, so the only way for alleles A and B to break their initial association with b and a is by mutation happening twice on the same chromosome…. We've seen that if selection acts on a combination of traits influenced by different loci, L-Deq is the result. This sort of thing is inevitable when selection acts on a phenotype of many traits influenced by many separate loci. So in populations of real organisms, selection will create high levels of L-Deq; sexual recombination is a way for the population to recreate genotypic variation by recreating the genotypic classes and thus the phenotypic classes lost by selection. So if genetic diversity is adaptive, sex will be adaptive (in a lottery, it is better to have many different tickets rather than many copies of the same ticket or when you are planning retirement it is better to have many investments rather than a lot of only one investment, i.e., in an uncertain world, don’t put all your eggs in one basket). Why is recreating genetic diversity adaptive? After all, if selection removed particular genotypes, won't it just continue to remove those same genotypes? Key here is that the environment is variable, thus there may not be an allpurpose, “better” allele (note that this thinking is very different from that which led to Muller’s ratchet). And this is the key to many organismal life cycles. Let me work through an example. Imagine Hydra living in Lake Shabbona (Figure 8.22). These are carnivorous, simple animals, imagine that these are the animals in the example from the text, figure 8.4) and that the environment changes from year to year, but it is constant within years (like the example of Darwin’s finches, or California—very wet one year, then very dry). So there might be many predators and lots of food one year (all under size 13 are killed), and other years there may be few predators and little food (all 13 and over die of starvation). Hydras can

either replicate clonally by budding or sexually via gametes. What sort of schedule (or life cycle) of sexual and asexual reproduction would be favored? Prediction is very difficult, especially about the future—we can’t do it, so how is a little hydra going to do it? remember that recombination increases genetic variability; highly varied offspring increase likelihood that one’s lineage will survive in a changing environment. And typically, you see sexual reproduction when environment is changing, asexual when the environment is relatively constant. So Hydra will reproduce asexually all summer, but when winter comes they reproduce sexually (like the aphid, Volvox, and the strawberry). (In a lottery do you want many copies of the same ticket or many different tickets?). So the population here (Fig 8.3) is obviously in a predator- and food-rich environment. So individuals don’t have sex (no point in recreating lost haplotypes when selection will just kill them again) and do reproduce clonally (as offspring will be “13s” or greater, they will be immune from predation all summer long). But then as fall and winter approaches, hydra begin to go dormant for the year. What will next year be like? No way for hydras to predict this. (Not even the best meteorologists predicted wet weather would lead to record high-water levels in the Great Lakes only a few years after record low levels!) Maybe it will be predator- and food-poor? (Then all individuals in the current population, and all of their clonal descendents will be killed.) What to do? Have sex, diminish the levels of L-Deq in the population. But note that while in theory recombination produces variation, recombination can’t do everything; here note that the missing ab haplotype cannot be immediately recreated because recombination can only occur within existing individuals, prior to gamete formation. Even with recombination, AB/AB individuals can only produce AB gametes, Ab/AB can only produce Ab or AB, aB/AB can only produce aB or AB, and so on (note that populations with little genetic variability have only limited response to a changing environment [this is a concern with many endangered species]—in this case there is no effect of recombination). But in addition to recombination, sex mixes haplotypes in outcrossing (usually a result of whole cell fusion unless selfing), ignoring for now the possibility of hermaphrodites. So some offspring will form from Ab and aB gametes and phenotype will be “12.” If following year has low food, low predator environment, only “12s” will survive. But at the next following year these could recreate all haplotypes (note that recombination can now form the missing ab and AB chromosome). So sex is not just recombination, but mixing of haplotypes, and both may be important for the evolution of sex). Applying the same logic to the aphids in Figure 8.21, we can now understand why they reproduce parthenogenetically in the spring and summer but in the fall sexually produce eggs that will overwinter. Strawberry plants in the wild do

something similar, and Volvox shows similar reproductive patterns related the drying up of freshwater habitats. So there are convincing arguments for the maintenance of sex once it evolved, and I’ve outlined 3 such arguments: (1) recombination and deleterious mutations (Muller’s ratchet—usually applied at the level of the population, but may work at individual level for sexual/asexual breeders); (2) recombination and favorable mutations in a population (likely related to rates of evolution of populations in a changing environment); (3) recombination, outcrossing, and (mostly) individual fitness in a changing environment; and (4) in passing we noted that whole cell fusion and whole genome recombination is a way for intracellular symbionts to move around in an almost horizontal manner. but how might sex have originated? Lane discusses a “mitosis first” model of how the mechanics of eukaryotic sex evolved (mss): (a) haplodiploid life cycle with one step meiosis, (b) haplodiploid life cycle with cell fusion and one-step meiosis (this step could have evolved precisely because of the benefits of mixing of haplotypes as in above example), and (c) modern sexual life cycle with haplodiploid life cycle and two step meiosis including whole-genome recombination. If mitosis came first, however, how did the population survive Muller’s Ratchet? Another theory, from Bill Martin and colleagues, suggests that meiosis may have come first and relates all of these innovations to the problem of chromosomes isolated in a nucleus and no longer able to attach to the cell membrane during division. We will return to these issues during the history of life part of the course, but let me mention that genetic recombination itself clearly predates the evolution of eukaryotes, so we have to look at bacteria, which don't have cell fusion and whole-genome recombination, but they do exchange bits of DNA and sometimes have partial recombination. When both strands of a DNA molecule are damaged, extra copies allow fixing this damage by copying the extra copy, hence an advantage of having multiple copies of DNA. Recombination may have evolved in this context; imagine you miss a lecture and have a gap in your notes, what do you do?, get someone else's notes and copy them; just so, if a bacteria has only damaged copies of a gene, it gets someone else's copy of the same gene and uses this as a template to copy the missing gene. The enzymes used in DNA repair likely evolved early and then by a process of accident and cooption evolved the process of recombination. Recombination evolved in the context of DNA repair. A better understanding of “archaean sex” would clarify this picture. related to this, recall the evolution of sex and the gene level of selection: most genes replicate only when the cell replicates, but transposable elements or transponsons, a kind of mobile genetic element (MGE), jump to a new site in the genome leaving a copy behind...if they can trigger outcrossing and sex they can jump to a new genome; these may be the ultimate selfish genes (i.e., parasites,

like viruses, but don’t have the equipment to move between cells on their own), though likely in most cases they are commensals, that is, their effect on the host is largely neutral (or in some cases mutualists, e.g. telomerase seems to have features co-opted from MGEs). There are a number of alleles that are “segregation distorters” and use sex to gain an advantage over other genes and alleles simply because the gametes without the selfish genetic element die (note parallels to gene duplication via crossing over). This process is now referred to as “gene drive.” Whole cell fusion unleashed many potentially parasitic elements which otherwise would be constrained by vertical transmission: “safe sex” is a contradiction in terms. But evolution may sometimes favor risk-taking because of the possibility of a big reproductive payoff. So much for the evolution of sex. Now recall a couple lectures ago I said that the single locus population genetic approach is general to the extent that (1) traits are controlled by single loci, and (2) populations are in linkage equilibrium (L-Eq) for these loci. And we now understand how L-Deq happens and how sex is the cure. But what if a single trait is directly influenced by many genes? What if the effects of genes are additive (like the example in figure 8.4), or worse, if you have interactions among alleles at different loci as in epistasis (like dominance but between alleles at different loci)? Such traits are often considered quantitative traits....