A characteristic feature of parasites is their high reproductive output.

1. A characteristic feature of parasites is their high reproductive output. Other organisms that have hazardous phases in their life cycles, such as planktonic larvae, produce vast numbers of offspring. Organisms that live in transient environments, such as rainwater pools, have, like parasites, developed resistant and dispersal stages and are often capable of asexual reproduction. But even in parasites there is a relationship between fecundity and parental care. The monogeneans for example produce few well-provisioned eggs, tsetse vectors produce very few, but well provisioned larvae. How many eggs should be produced… how should they be produced? Trade offs……………

2. Asex vs SEX… Why do organisms have sex? Sex is an embarrassing subject for biologists…. Most organisms have sex. Why is it so common? Sex is very expensive Sex is not necessary for reproduction (is an "interruption" of mitosis) Costs time and energy finding a mate Big genetic cost

3. Evolution of Sex Bell (1982) commented that “Sex is the queen of problems in evolutionary biology. Perhaps no other natural phenomenon has aroused so much interest; certainly none has sowed as much confusion”.

4. The two-fold cost of sex (Maynard Smith, 1978) Sexually generated offspring are only 50% related to parent ("cost of meiosis") + only half of offspring reproductive ("cost of males"; slower rate of increase). Mutations for asexuality (e.g. "cut out meiosis") should rapidly spread: are passed on with 100% efficiency + 100% of offspring are reproductive Ratio of asexual to sexual females should double per generation It has been argued that unless sexual offspring are significantly fitter, sex is not an Evolutionary Stable Strategy

5. So, all other things being equal, sexual forms should be easily outcompeted by parthenogens There is a consistent trend for sex to be most prevalent where the habitat is not subject to dramatic fluctuations Parthenogens are more common early in succession and at extreme latitudes and altitudes in both animals and plants

6. The vast majority of eukaryotes reproduce sexually. This poses a central problem in evolutionary biology: a parthenogenetic female passes twice as many of her genes to progeny as a sexually reproducing female. Why are not all organism parthenogenetic? How can we explain sex persisting in populations? Are these explanations powerful enough relative to individual selection? Need sufficiently large short-term advantage to offset two-fold cost per generation

7. Five Costs of Sex 1. Recombination scrambles genotypes, disrupting favorably adapted gene combinations, whereas parthenogenesis preserves advantageous genotypes 2. Meiosis and syngamy takes longer than mitosis, slowing the pace of reproduction - decreased population growth rates 3. Courtship and mating may be risky; risk from predation or sexually transmitted disease - there may be waste of gametes and costs associated with maintenance of sexual dimorphism and sexual competition 4. At low population densities sexual reproduction may be difficult to coordinate. Parthenogenesis ensures that reproduction will be possible at any time or place 5. Most important of all, sexual females suffer from genome dilution. Consider parthenogenetic and sexual females producing eggs at the same size and rate. Because the sexual female contributes only half the genetic material to each egg, she suffers a greater (two-fold) cost relative to the parthenogen

8. Muller’s Ratchet Hypothesis: Recombination/sex is directly beneficial by purging deleterious mutations Fisher-Muller Hypothesis: Sex may facilitate response to environmental change by generating new gene combinations allowing populations to track a dynamic environment: This is because adaptive favorable mutations can be combined horizontally through a population Segregation Hypothesis: Similar to the Fisher-Muller Parthenogenetic clones cannot acquire favorable mutations in the population: once a favorable mutant A1A1 - A1A2 arises the adaptive transition A1A2 - A2A2 is not possible without segregation

9. Tangled Bank Hypothesis: heterogeneity in which a genotype favored at one location may perform poorly elsewhere: it may be advantageous to break up genotypes of offspring dispersing to random sites nearby or distant Red Queen Hypothesis: A related hypothesis attributes environmental heterogeneity to species interactions For example, sex would be favored in host-parasite interactions because it generates diverse progeny, some of which may have novel resistance genotypes and be able to withstand parasite attack or disease The high incidence of sex in physically stable environments where species diversity is high is consistent with both the Tangled Bank and Red Queen hypotheses where both intraspecific competition and interspecific interactions should be most intense

10. Fisher-Muller Hypothesis Sex may facilitate response to environmental change by generating new gene combinations allowing populations to track a dynamic environment • This is because adaptive favorable mutations can be combined horizontally through a population Asexual ABC A AB time A AB ABC Sexual B BC C time

11. Tangled Bank Hypothesis Sexual groups may be able to exploit a greater number of microsites than a limited number of parthenogenetic clones In addition to the greater number of microsites accessed by sexuals, siblings will compete less due to specialization in different microsites Red Queen Hypothesis Attributes environmental heterogeneity to species interactions For example, sex would be favored in host-parasite interactions because it generates diverse progeny, some of which may have novel resistance genotypes and be able to withstand parasite attack or disease

12. If sib competition is important, (Tangled Bank Hypothesis) then recombination should be most prevalent when litter size is high, when within-brood variation is possible (higher recombination being necessary for greater diversification) However, if parasites are important, (Red Queen Hypothesis) then recombination should be more important in long-lived species where the number of parasite generations will be greater than the number of host generations The high incidence of sex in physically stable environments where species diversity is high is consistent with both the Tangled Bank and Red Queen hypotheses where both intraspecific competition and interspecific interactions should be most intense

13. Burt and Bell (1987) Overall, there is support for the Red Queen Hypothesis since there is a positive correlation between recombination and generation time . . 40 R2 = 0.76 . . . 30 24 species of nondomesticated mammals 20 . . . . . . 10 10 50 100 500 1000 5000 10000 Age to Maturity (Days) - Semilog

15. What does sex actually do? • Sex can’t cause adaptation directly: i.e. can’t change allele frequencies. Instead, it affects the distribution of alleles in a population; breaks up linkage disequilibrium (non-random associations between alleles in the population). It stops offspring being the same as their parent. • Sex breaks up these associations between alleles and either maintains heritable variation, so allowing continual responses to variable selection, or (long-term) speeds up spread of of "good alleles“ or prevents the accumulation of deleterious alleles or less fit genotypes. • Sex shuffles alleles between genomes

16. A GENERALLY ACCEPTED RULE: Sex increases the rate of adaptation Sex increases rate of spread of good alleles, allows you to generate composite genomes; mutations that arise independently can spread together Asexual genomes = "selfish inventors" Sexual genomes = share technology/innovation, Reduces "waiting time" for good combination of alleles BUT: This is a long-term advantage… Does Natural selection act to favour long-term evolvability of populations (group selection vs individual selection) At individual level, asexuality should still spread within populations

17. Parasites and the Red Queen Parasites are a big source of mortality in nature (Spanish influenza; 25 Million people in four months, Plague in Europe 1300s); also evidence that immune systems genes evolve v. quickly relative to other genes Coevolution/arms race could provide appropriate timescale for constant advantage of sex "Best defence is the first that the enemy will counter" = constant need to switch from rare to common alleles (frequency dependent selection) Sustained oscillations in gene frequency between parasites and host: direction of selection changes every generation  

18. Empirical support for Red Queen Potomopyrgus: freshwater snail: (Lively, 1987). Sexual or asexual forms: sexual more common when parasite present (Red Queen) Correlation between number and age to maturity (Burt and Bell, 1987); longer generation time - need more recombination per generation to counter parasites Long lived trees are sexual (e.g. Douglas fir), only short-lived annuals tend to be asexual; longer time between generations for parasites to evolve More anecdotal: e.g. clonal crops are v. susceptible to sexual parasites e.g. potato blight fungus, Ireland, 1848. All potatoes grown were clones of single line.  

19. There is a 50% cost of sex per generation. Asexual mutants should spread rapidly. In contrast, sex is very widespread. Sex breaks up associations between alleles, so maintains variation for selection to act on. Clearly advantageous in long term…asexuals are "selfish inventors" To be continually advantageous, need constantly changing selection: Coevolution with parasites (Red Queen) may be a candidate, also explains evolutionary stasis. Coevolution between hosts and parasites could maintain sex and affect cyclic increases and decreases in frequency of resistance and defence alleles Requires close coupling of parasite and host (specialists), and severe fitness costs of infection (otherwise not much cost to not being resistant) Old defences need to periodically become useful again (so that sex prevents extinction of temporarily useless alleles); defence against one makes you susceptible to the other

20. Sex is widespread and very important in evolution, also has a big effect on how evolution works (e.g. speciation, sexual selection, intragenomic conflict). However, it is difficult to explain as it is clearly costly. Our understanding will benefit from future approaches - into the nature and rate of mutations and coevolution between parasites and hosts, and the genetic architecture of immune systems Have parasites been involved in maintaining sexual reproduction? What factors can influence evolution?

21. The joy of sex - courtesy of parasites by Kate Melville Why do we have sex? From an evolutionary perspective, the answer is not as obvious as we might think. And now, a fascinating new study in American Naturalist suggests that sex may have evolved primarily as a defense against parasites. Sex is something of an evolutionary mystery to biologists, as reproducing without sex - as microbes, some plants and even a few reptiles do - would seem like a much more efficient way to go. Every individual in an asexual species has the ability to reproduce on its own. But in sexual species, two individuals have to combine in order to reproduce one offspring. That gives each generation of asexuals twice the reproductive capacity of sexuals. Why then is sex the dominant strategy when the do-it-yourself approach is so much more efficient? One theory is that parasites keep asexual organisms from getting too plentiful. When an asexual creature reproduces, it creates clones - exact genetic copies of itself. Since each clone has the same genes, each has the same genetic vulnerabilities to parasites. If a parasite emerges that can exploit those vulnerabilities, it can wipe out the whole population. On the other hand, sexual offspring are genetically unique. So a parasite that can destroy some can't necessarily destroy all. That, in theory, should help sexual populations maintain stability, while asexual populations face extinction at the hands of parasites.

22. Now, thanks to Potamopyrgus antipodarum, a snail common in fresh water lakes in New Zealand, scientists have a chance to test this parasite theory. The snails exist in both sexual and asexual versions, thus providing biologists with an opportunity to compare the two versions side-by-side in nature. Researchers began observing several populations of these snails for ten years beginning in 1994. They monitored the number of sexuals, the number asexuals, and the rates of parasitic infection for both. They found that while clones were plentiful at the beginning of the study, they became more susceptible to parasites over time. And as parasite infections increased, the once plentiful clones dwindled dramatically in number. Meanwhile, sexual snail populations remained much more stable over time. This, the authors say, is exactly the pattern predicted by the parasite hypothesis. "The rise and fall of these female-only lineages was surprisingly fast and consistent with the prediction of the parasite hypothesis for sex," Jokela said. "These results suggest that sexual reproduction provides an evolutionary advantage in parasite rich environments."

23. Mites Re-Evolve Sexual Reproduction by Kate Melville Researchers from the University of Darmstadt in Germany and the SUNY College of Environmental Science and Forestry reported this week on a family of mites that have forsaken asexual reproduction and re-evolved to reproduce sexually. Reported in the Proceedings of the National Academy of Sciences, the revival of a complex trait such as sexual reproduction after it had been dormant for millions of years raises interesting questions about our understanding of evolutionary biology. "They found a way to re-evolve sex," Norton said. "We're talking about something that involves a lot of elements in both males and females." Mainly found in soils in the southern hemisphere, oribatid mites perform a vital role as decomposition agents, grazing on fungi, decaying leaves and other organic matter. The critters are also found on trees and rocks and Norton speculates that moving from their ancestral home in the ground, where organic material is plentiful, to trees and rocks, where food can be scarce, could account for the change in reproduction. "The increased exposure and competition for food may create a need for more responsive genetic defense mechanisms," he said. The discovery raises some intriguing questions. Why do some organisms continue to reproduce asexually, given the distinct evolutionary advantages - especially defenses against parasites, predators and competitors - from reproducing sexually and mixing genomes? And how can an organism jump-start a group of genes - such as those specific to sexual reproduction - after many millions of years of not being used?

24. Sex – Evolution’s Janitorby Kate Melville Asexual reproduction leads to a faster accumulation of bad mutations, says a report in this week's issue of Science. Indiana University evolutionary biologists used the water flea (Daphnia pulex) to establish their findings, which support the hypothesis that sex is an evolutionary housekeeper that efficiently reorders genes and removes deleterious gene mutations. Interestingly, the study also suggests that sexual reproduction maintains its own existence by "punishing" individuals of a species that meander into asexuality. The researchers say that the ability to reproduce asexually may be useful to organisms that can't get mates, but its long-term benefits are questionable. "It is known that sex is common in plants and animals, and that asexual species are typically short-lived, but why this should hold throughout evolutionary time is a great mystery," said study leader Susanne Paland. "Our results show that asexual deviants are burdened by an ever-increasing number of genetic changes that negatively affect the function of their proteins. It appears sex is important because it rids genomes of harmful mutations."

25. Sexual reproduction is a complicated, biologically costly business. In mammals, sex is usually preceded by intricate mating behaviors. It requires the compatibility of sexual structures, an insertion event, fertile eggs and sperm, and the successful unification of egg and sperm into a viable zygote. All of this adds up to a big energy investment - energy an organism might have used for other purposes. It's no surprise then, that scientists have long pondered what it is about sex that justifies such a big energy investment. One of the most widely accepted explanations has been that sexual reproduction confers the benefit of unlinking genes, so that bad versions of genes won't always get to hitch a ride with the good versions. This theory contends that natural selection operates optimally when parts of the genome are free to shuffle about. Sexual populations have recently and repeatedly spun off asexual strains. By comparing rates of protein evolution, the researchers found that the asexual lines accumulated bad mutations four times faster than sexual lines. If a switch to asexuality causes a big increase in the number of protein defects, a mechanism for removing those defects must somehow be missing when sex, too, is missing. The present report supports the notion that it is sex - or the genetic recombination that is a component of sexual reproduction - which is the purifying force that helps get rid of genetic mishaps that harm the overall evolutionary health of a population.

26. Sex Ratio Variation Why is it that we often observe a sex ratio of 1/1 or one close to a 1/1? • Fisher (1930) found that he could explain the 1/1 sex ratio in terms of selection at the level of the individual • Fisher reasoned that if there were, say, 10 females per male, selection would favor the production of males since the fitness of the parent would be enhanced by production of males as opposed to females

27. Sex Ratio Variation • The rare sex is also favored when one reverses the situation to 10 males per female, with the female having 10 times the average reproductive success of a male • Since a female produces an egg(s) that can be fertilized by a single male, chances are that the remaining 9 males will not breed. Therefore, it would be to the parents benefit to produce female offspring, ensuring that their genes are passed on

28. Sex Ratio Variation • In either case, the sex ratio would not be evolutionarily stable because a gene causing parents to bias the sex ratio towards a greater number of the rarer sex, would rapidly spread • Only when the sex ratio is exactly 1/1 will the expected success of a male and a female be equal and the population stable

29. Investment • If a male costs twice as much to produce in terms of energy invested and a female half as much (and yet both males and females produced the same number of young) it would be advantageous for the parent to produce females as opposed to males • In this case the stable strategy would balance out when the population became skewed to a 2/1 (female/male) sex ratio • Therefore, in terms of numbers one would expect a 1/1 ratio when the sexes are of equal cost but a skewed ratio in terms of numbers when there is a differential cost between males and females • However, there will be a 1/1 ratio in terms of investment even though the sex ratio is skewed in terms of numbers

30. Trivers and Willard (1973) • Assume that a female in good condition is better able to bear and nurse her calf than is a female in poor condition, so that at the end of the period of parental investment, the healthiest, strongest and heaviest calves will tend to be the offspring of the adult females who were in the best condition during the period of parental investment • Assume that there is some tendency for differences in the condition of calves at the end of the period of parental investment to be maintained into adulthood • Assume that such adult differences in condition affect male reproductive success more strongly than female reproductive success • In this case, male caribou in good condition tend to exclude other males from breeding, thereby inseminating many more females themselves, while females in good condition, through their greater ability to invest in their young, show only a moderate increase in reproductive success

31. Under these assumptions, an adult female in good condition who produces a son will leave more surviving grandchildren than a similar female who produces a daughter, while an adult female in poor condition who produces a daughter will leave more surviving grandchildren than a similar female who produces a son • So, as maternal condition declines, the adult female tends to produce a lower ratio of males to females

32. Can Parasites alter behaviour? Can Parasites affect sex? Sex… Can parasites affect mate selection? Can one gender determine the parasite status of a potential mate before deciding? In the animal world why are males usually larger and more colorful? What are the costs? What are the benefits?