Evolution of Sex

1. 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�.

2. Why Bother?Cost of Sex Lewis (1987). The cost of sex. In: S.C. Stearns (ed.) The Evolution of Sex and its Consequences, states that there are five costs of sex.

3. Five Costs of Sex 1. Recombination scrambles genotypes, disrupting favorably adapted gene combinations, whereas parthenogenesis preserves advantageous genotypes 2. Syngamy and meiosis takes longer than mitosis, slowing the pace of reproduction (small organisms may be at a competitive disadvantage - decreased population growth rates)

4. Five Costs of Sex 3. In higher organisms, courtship and mating may be risky, because of the risk from predation or even sexually transmitted disease - there may also be wastage 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. Five Costs of Sex 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 cost relative to the parthenogen.

6. Maynard Smith (1978) asked the question � Which reproductive mode is better? Made two assumptions: 1. A female�s reproductive mode does not affect the number of offspring she can make. 2. A female�s reproductive mode does not affect the probability that her offspring will survive.

7. Showed that asexuals would leave twice as many grandchildren each generation

8. So, all other things being equal, sexual forms should be easily outcompeted by parthenogens

9. Are one or both of Maynard Smith�s assumptions wrong? The first assumption, that the number of offspring a female can make does not depend on whether she is sexual or asexual, is violated in species in which fathers provide resources or other forms of parental care essential for producing young � but species with male parental care are in the minority (examples include � humans, many birds and pipefish).

10. Are one or both of Maynard Smith�s assumptions wrong? A general advantage to sex is likely to be found in the violation of the second assumption � that the probability that a female�s offspring will survive does not depend on whether she produces them sexually or asexually

11. Dunbrack et al. 1995. The cost of males and the paradox of sex: an experimental investigation of the short-term competitive advantages of evolution in sexual populations. Proceedings of the Royal Society of London 262:45-49. Tested this second assumption in Tribolium beetles

14. The next question is, Why? Most theories about the evolution of sex are concerned with reasons why females that produce genetically diverse offspring will see more of them survive and reproduce than will females that produce genetic copies of themselves Of course there is a diverse array of theories about the advantages of sex

15. Distribution of Sex 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

16. Correlations might be interpreted in two ways 1. Might indicate that sex only enjoys an advantage over parthenogenesis in stable environments and we should seek an explanation for sex under these conditions. We need to address why recombination provides benefits in these environments which outweigh the costs.

17. Correlations might be interpreted in two ways 2. The advantages of sex may be widespread but parthenogenesis may be favored in hostile environments because density is low and colonization opportunities frequent, so that the costs of mate or gamete production may tip the balance toward parthenogenesis

18. Of course, both of these factors may be important

19. Hypotheses for the Maintenance of Sex (Recombination)

20. DNA Repair Hypothesis Repair is only possible when a suitable template exists - homologues provide the template & repair involves crossing over What�s less clear is whether DNA repair is the principle function of sex

22. Two Problems with the DNA Repair Hypothesis 1. Crossing over is absent in some circumstances (e.g., it is often absent in one sex), yet there is no obvious increase in mortality associated with the absence of repair 2. DNA repair should be greatest in environments where damage is highest, e.g., at high altitudes. However, parthenogenesis predominates in these habitats

23. So, perhaps we should regard DNA repair as a beneficial consequence of recombination and crossing over rather than its principle cause

24. Mutation Elimination HypothesisMuller�s Ratchet Recombination/sex is directly beneficial by purging deleterious mutations Idea is that deleterious mutations affect the success of parthenogens - each generation new mutations increase the average genome contamination

25. Anderson, D. and D. Hughes. 1996. Muller�s ratchet decreases fitness of a DNA-based microbe. PNAS 93:906-907. Salmonella typhimurium Set-up 444 experimental cultures each from a single individual Maintained the experiment for 2 months � 1,700 generations

26. Results are consistent with Muller�s Ratchet Found 5 or 1% of cultures with significantly lower fitness compared to the wild type Generation time ranged from 25-47.5 minutes compared to 23.2 minutes for the wild-type None had higher fitness than the wild-type

27. 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

29. Segregation Hypothesis Similar to the Fisher-Muller Hypothesis Parthenogenetic clones cannot acquire favorable mutations that occur elsewhere in the population for example, once a favorable mutant A1A1 - A1A2 arises the adaptive transition A1A2 - A2A2 is not possible without segregation

30. Gene/Environment Hypothesis Discussion of advantages for sexual reproduction initially focused on the apparently rapid changes facilitated by recombination - so changes in time (to track environmental change) seemed an appropriate explanation for the advantages of sex This hypothesis is no longer popular, because its central prediction is false; sex is not more prevalent in extreme or fluctuating environments - the opposite is true

31. Tangled Bank Hypothesis The concluding paragraph of Darwin�s Origin of Species begins with the following �It is interesting to contemplate an entangled bank, clothed with many plants of many kinds, with birds singing on the bushes, with various insects flitting about, and with worms crawling through the damp earth, and to reflect that these elaborately constructed forms, so different from each other, and dependent on each other in so complex a manner, have all been produced by laws acting around us�

32. Tangled Bank Hypothesis This image of a locally complex environment (a Tangled Bank) has been used by Bell (1982) to name a hypothesis which suggests that spatial heterogeneity is important in the maintenance of sex The arguments are based on spatial heterogeneity in which a genotype favored at one location may perform poorly elsewhere Therefore, it may be advantageous to break up genotypes of offspring dispersing to random sites nearby or distant

33. 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

34. 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

35. Some evidence that parthenogens are more susceptible to attack by parasites than sexually reproducing organisms Burdon and Marshall (1981) show that biological control of weeds is more likely to be successful when the target is parthenogenetic asexual species 48% complete control (N= 44 sp) sexual species 14% complete control (N=29 sp) also genetically uniform crops or zoo populations can be devastated by disease

36. Lively, C. 1992. Parthenogenesis in a freshwater snail: reproductive assurance versus parasitic release. Evolution 46:907-913. Studied the freshwater snail Potamopyrgus antipodarum in 66 lakes in New Zealand Snail is host to over a dozen species of parasitic trematode worms Trematodes eat the snails gonads causing castration Exerts strong selection pressure for resistance to infection Most populations contain two kinds of females � sexual and parthenogenetic Tested to see if sexual females were prevalent in highly parasitized populations

38. 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

39. An Example that Differentiates between the Tangled Bank Hypothesis & the Red Queen Hypothesis Burt, A. and G. Bell. 1987. Mammalian chiasma frequencies as a test of two theories of recombination. Nature 326:803-805.

40. Preface, start out with the following statement in their paper�A broad survey of asexuality in the animal kingdom is sufficient to reject all theories of sex and recombination except two: the Red Queen and the Tangled Bank

41. Burt and Bell (1987) Argue that the level of recombination in mammals is indicated by the frequency of excess chiasmata, or sites where crossing over has occurred They suggest that if sib competition is important, as suggested by the 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)

42. Burt and Bell (1987) However, if parasites are important, as suggested by the 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

43. Burt and Bell (1987) Overall, there is support for the Red Queen Hypothesis since there is a positive correlation between recombination and generation time

44. Burt and Bell (1987) Litter size and generation time were inversely correlated in mammals - so recombination is highest when litter size is smallest, not largest

45. Conclude that Crossing-over may function to combat antagonists with short generation times but does not function to reduce sib competition

46. Sex Ratio Variation Why is it that we often observe a sex ratio of 1/1 or one close to a 1/1?

47. Sex Ratio Variation You could argue, at least for birds and mammals, that an equal sex ratio could arise simply as a consequence of heterogametic chromosomal sex determination This makes it difficult to discern whether the equal sex ratio is an artifact of the sex determining mechanism, or the sex determining mechanism is a way of achieving the optimum sex ratio

48. Sex Ratio Variation 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

49. 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 its genes are passed on

50. 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

51. Investment Fisher refined his arguments in terms of investment If for example, 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

52. Investment 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

53. A test of Fishers sex ratio theory Metcalf, R.A.. 1980. Sex ratios, parent-offspring conflict, and local competition for mates in the social wasps Polistes metricus and Polistes variatus. The American Naturalist 116:642-654

54. Metcalf (1980) In Polistes metricus females were half the size of males, however, in Polistes variatus males and females were the same size The sex ratio of P. metricus in terms of numbers was 2/1 for females/males, but 1/1 in terms of investment In P. variatus the sex ratio was 1/1 in terms of number and investment since the sexes were of equal cost - so it apears that Fishers argument was upheld

55. R.L. Trivers and D.E.Willard (1973). Natural selection of parental ability to vary the sex ratio of offspring. Science 191:90-92. Argue that sex ratio can deviate on an individual basis, still maximize fitness, and be an evolutionary stable strategy so long as there is balancing selection at the level of the population

56. The prediction that parents should invest equally in sons and daughters does not always hold For example, in some bird species, males but not females stay at home and help - the end result is to invest slightly more in males than in females since they help the parent in its future reproduction

58. Translocation Experiments

60. In a case of inbreeding Fisher�s argument does not appear to fit, however, such a deviation is adaptive In the most extreme case, a viviparous mite, Acarophenox, produces only a single male and approximately 20 females The single male inseminates all females and then dies before he is born The difference between this and the earlier argument for a 1/1 sex ratio is that here the ratio of males to females in the rest of the population does not matter