7. The Adaptive Significance of of Sex Why is sexual reproduction so common in multicellular organisms?

Sex is costly and dangerous Energetic costs: mate finding, courtship, male - male competition Increased predation risk Disease: STDs Genetic cost: sexual reproduction means that a parent passes on only 1/2 of its genes to offspring Demographic cost: all other things being equal, an asexual clone will replace sexual individuals in a “mixed” population, because asexual females will produce twice as many daughters as sexual females (John Maynard Smith)

Assumptions of the model: Maynard Smith’s model for the demographic advantage of parthenogenetic reproduction Parthenogenesis is reproduction via diploid eggs without fertilization (aphids, Daphnia, rotifers, some lizards, etc.). Parthenogenetic populations are all-female (or produce males only when switching to sexual reproduction) Assumptions of the model: A female’s reproductive mode does not affect the number of offspring that she can make A female’s reproductive mode does not affect the probability that her offspring will survive

Asexual reproduction has a 2-fold demographic advantage compared to sexual reproduction (Fig. 7.17)

The prevalence of sexual reproduction is a paradox Despite the apparent advantages of asexual reproduction, the vast majority of multicellular species reproduce sexually (many exclusively) This suggests that sexual reproduction must in general confer higher fitness than asexual reproduction; that is, one or both of the assumptions of Maynard Smith’s model are incorrect Assumption #1 - equal numbers of offspring - might be violated if males provide parental care Assumption #2 would be violated if offspring of sexual females have higher survivorship than offspring of asexual females

Experiments with the flour beetle, Tribolium Red beetles and black beetles compete in the presence of insecticide (malathion) One color of beetle, say red, is designated as the sexual strain. It must survive in the presence of insecticide by evolving resistance without “outside” help from the experimenters The other color of beetle, say black, is designated as the “asexual” strain. Every generation, all the black adults are removed and replaced with three times as many black adults from a culture that is not exposed to insecticide. The black beetles have a strong demographic advantage but cannot evolve resistance to the insecticide

Competition between sexual and “asexual” flour beetles in the presence of insecticide – 1 (Fig. 7.18) 10 20 30 Generation

Does sexual reproduction allow populations to adapt more quickly to changing environments? These experiments suggest that the advantage of sexual reproduction is that it increases the chance that a population can adapt to a changing environment. The 3-fold demographic advantage of the black beetles was not enough to keep them from going extinct when faced with an evolutionary challenge (competition with red beetles and insecticide). This argument is supported by the fact that the red beetles “won” more quickly at higher concentrations of insecticide (= stronger selection).

Competition between sexual and “asexual” flour beetles in the presence of insecticide – 2 (Fig. 7.18) The outcome of the experiment does not depend upon which color of beetle is “asexual” 10 20 30 Generation

Why does sexual reproduction enhance evolutionary adaptation? Sex = genetic recombination Crossing-over during meiosis Mixing of genes from 2 parents Sex “reshuffles” genes to create new multilocus genotypes in every generation

Artificial selection on other traits often results in increased recombination (Fig. 7.19)

R.A. Fisher: Sex increases the rate of evolution – 1 Suppose 2 favorable mutations, A´ and B´, occur in a population – most likely they will occur in separate individuals In a sexual population, these two favorable mutations can be combined in the same individual by mating between carriers of A´ and B´ In an asexual population, the only way that both mutations can be in the same individual is if the B´ mutation occurs in an individual that is already A´ (or vice versa)

Objections to Fisher’s model Fisher’s argument requires a relatively high rate of favorable mutations. Suppose A´ occurs first. Selection will tend to fix it in the population (either sexual or asexual). If B´ occurs after A´ is fixed in the population, then it will necessarily occur in an individual that is already A´, in which case sex has no advantage. For sex to have an advantage, B´ must occur before A´ rises to high frequency. Fisher’s model is generally considered to be a group selection argument: sex is good for the “group”; sex is common because species that reproduce sexually are less likely to go extinct – most evolutionary biologists prefer arguments that posit an advantage to individuals

Muller’s Ratchet: Deleterious mutations will accumulate in asexual lineages Most individuals (clones) will carry one or more harmful mutations A small number of individuals might have zero harmful mutations. They might have a slight fitness advantage, compared to individuals with 1 or 2 mutations. But they are also likely to be few in number and may be lost from a population by drift. If the zero-mutation class is lost from a population then the most fit class will be those individuals with 1 harmful mutation (the ratchet has clicked once). If those individuals with 1 mutation are lost from the population, then the most fit class will be those with 2 mutations (the ratchet has clicked again).

Muller’s ratchet (Fig. 7.20)

Muller’s Ratchet: Sexual recombination can produce individuals with fewer deleterious mutations Suppose a sexual male and female both carry a harmful mutation, C´. If they are both heterozygous, then we expect 1/4 of their offspring to not have C´

Objections to Muller’s ratchet It’s “groupy”: groups (species or populations) that reproduce asexually accumulate genetic load and are more likely to go extinct than groups that reproduce sexually Although there is both theoretical and experimental support for Muller’s ratchet, it works best when population size is small (< 1,000) and drift is important. It does not appear to be a general explanation for the prevalence of sexual reproduction.

Sex is good in a changing environment The Tribolium experiments suggest that sex may increase individual fitness when selection is strong, or when environments change on a time-scale similar to the generation time of a species. If the environment experienced by offspring is different from that experienced by parents, then it may pay to reshuffle genes to produce genetically variable offspring, at least one of which may have a genotype that is well-suited to the new environment

Sex is like buying lottery tickets with different numbers The environment in the next generation is like a lottery 10 tickets, each with a different number, will give you a better chance of winning (= variable offspring produced by sex) 10 tickets, all with the same number (= identical offspring produced asexually), is a bad strategy

Host – parasite coevolution and sex: the Red Queen Hypothesis One important component of the environment for many species is parasites Hosts and parasites are involved in a coevolutionary “arms race” in which the host evolves defenses against the parasite, and the parasite, in turn, evolves to overcome host defenses — both sides must constantly evolve just to maintain the status quo Evolution by the parasite represents a changing environment for the host, and sexual reproduction allows the host to produce offspring that are more likely to be resistant to prevalent parasite genotypes.

The Red Queen’s race in Alice in Wonderland The Red Queen's race is an incident that appears in Lewis Carroll's Through the Looking-Glass and involves the Red Queen and Alice constantly running but remaining in the same spot. "Well, in our country," said Alice, still panting a little, "you'd generally get to somewhere else — if you run very fast for a long time, as we've been doing.” "A slow sort of country!" said the Queen. "Now, here, you see, it takes all the running you can do, to keep in the same place. If you want to get somewhere else, you must run at least twice as fast as that!"

A host-parasite arms race can make sex beneficial - 1 (Fig. 7.22)

A host-parasite arms race can make sex beneficial - 2 (Fig. 7.22)

Sex and parasitism in a freshwater snail (Potamopyrgus antipodarum) (Lively 1992) Parasitized by several species of trematodes (flukes) that eat the gonads Snail populations consist of: males obligately sexual females (which produce male and female offspring) obligately asexual females Populations with higher incidence of parasitism had higher proportion of males (= higher proportion of sexual females)

Frequency of sexual individuals in snail populations with differing degrees of parasitism (Fig. 7.23) a. White “slice” indicates the frequency of males b. Fequency of males versus proportion of snails with trematode parasites