Lecture 4 The central role of parasites in evolution (cont’d)

1. Lecture 4The central role of parasites in evolution (cont’d)

2. Today: • Haldane’s ideas on the importance of infectious disease in evolution and ecology • Case study I: Parasite Red Queen and the advantage of sex • Case study II: How the Peacock got its tail? Sexual selection and parasites

3. Disease and Evolution, 1949 • “In all species investigated the genetical diversity as regards resistance to disease is vastly greater than that as regards resistance to predators.” • “It is much easier for a mouse to get a set of genes which enable it to resist [bacteria] than a set which enables it to resist cats.” • These remarks have been borne out by decades of study and we’ll dissect them in detail later

4. Disease and Evolution, 1949 • Other ideas/speculations in his paper: • Large amount of unexplained biochemical diversity in serological tests may play a part in disease resistance (outlines tests for associations between, say, diptheria susceptibility and various blood groups) • Genes for generating resistance variation should be particularly mutable, as long as other genes not affected • Frequency-dependent selection

5. Disease and Evolution, 1949 • Pathogen-driven speciation • “Once a pair of races is geographically separated, they will be exposed to different pathogens. Such races will tend to diverge antigenically, and some of that divergence may lower the fertility of crosses.” • Does anyone know more about this?

6. Disease and Evolution, 1949 • Social aspects of disease “It will be on the whole an antisocial agency…it is doubtful that many birds could survive the faecal contamination which characterizes the colonies of many sea birds.” • Evolutionary psychology and Darwinian medicine: “A vast variety of apparently irrelevant habits and instincts may prove to have selective value as a means of avoiding disease.” Examples?

7. Disease and Evolution, 1949 • evolution of virulence: “Perhaps the theory that most diseases evolve into symbioses is somewhat Panglossist. I doubt if it occurs as a general rule, though it may do so.” Panglossist? Do most diseases evolve into symbioses?

8. Disease and Evolution, 1949 Given enough time a state of peaceful coexistence eventually becomes established between any host and parasite. -Rene Dubos

9. Disease and Evolution, 1949 • He also notes that resistance to disease is rarely absolute, in part because viruses and bacteria evolve so quickly • “The most that the average species can achieve is to dodge its minute enemies by constantly producing new genotypes, as the agronomists are constantly producing new rust-resistant wheat varieties.” • The banana clone (a word that Haldane coined) ‘Gros Michel’ was widely exported, but has been all but wiped out by a fungal root pathogen

10. Disease and Evolution, 1949 • http://www.gi.alaska.edu/ScienceForum/ASF9/977.html • Although commonplace today, bananas only became a staple in North America's diet late in the 19th century. • They could do so because of a genetic freak--a spontaneous mutation in a kind of banana native to Southeast Asia. • The new banana was triploid, big, sweet, and seedless • The new mutation also had a characteristic that made long-distance transport possible: all the bananas on a stalk ripen at once, about three weeks after they've grown to harvestable size.

11. Disease and Evolution, 1949 • The French transported cuttings of the new plant to the Caribbean, where it thrived. They named it Gros Michel. • The Gros Michel was a true commercial banana, and the variety that won the hearts of people living outside the tropics. • Gros Michel had a serious weakness: it was susceptible to two kinds of fungus diseases. • One, called yellow sigatoka, could be controlled by spraying. The other was soil-borne Panama disease, a kind of fusarium wilt, and could not be cured or prevented.

12. Disease and Evolution, 1949 • The growers' only option was to keep moving banana plantations to fresh land. By the 1960s, new land ran out • Instead, they found a new banana. This one, christened Cavendish, was discovered in a Saigon botanical garden. It too was a big, sweet, seedless triploid that ripened weeks after harvest, but it resisted Panama disease. Swiftly and with no fanfare, Cavendish bananas replaced Gros Michel. • The Cavendish is now the banana of commerce.

14. Case study I: Parasites and the advantage of sex Which reproductive mode is better: sexual or asexual? • JMS died last year • Student of Haldane • Aircraft engineer in WWII, came to biology later in life • Leading thinker on the “evolutionary scandal” of sex John Maynard Smith

15. Sex is costly, not to mention complicated and dangerous • Searching for mates takes time and energy, and has risks (?) • Potential mates may demand additional exertion or investment before mating • After all that, mating might prove to be infertile • Why go to all the trouble?

16. Case study I: Parasites and the advantage of sex Which reproductive mode is better: sexual or asexual? • Null model: (what a null model?) • A female’s reproductive mode does not affect the number of offspring she can make • A female’s reproductive mode does not affect the probability that her offspring will survive (John Maynard Smith, 1978)

17. Case study I: Parasites and the advantage of sex Which reproductive mode is better: sexual or asexual? • Imagine a population founded by three individuals: a sexual female, a sexual male, and an asexual female • Every generation each female produces four offspring, after which the parents die • All offspring survive to reproduce • Half the offspring of sexual females are female (the other half are male) but all the asexuals’ offspring are of course female • What happens?

18. In a population conforming to JMS’s assumptions, asexual females produce twice as many grandchildren as sexuals, and fraction of asexuals climbs

19. Asexuals should take over. And yet the vast majority of multicellular species are sexual. • What’s going on? • JMS’s model illustrates, as he intended it to, that these facts represent a paradox for evolutionary theory • It’s an evolutionary scandal!

20. Sex must confer benefits that allow it to persist in spite of the strong reproductive advantage of parthenogenesis. • The benefits must lie in the violation of one or both of those assumptions…. A female’s reproductive mode does not affect the number of offspring she can make A female’s reproductive mode does not affect the probability that her offspring will survive

21. The first assumption is actually violated in species in which fathers provide resources or parental care essential for producing young. • This includes humans. • But such species are in the minority. In most species, males contribute only genes. • A general advantage to sex is thus likely to be found in violation of the second assumption…

22. What might account for a difference in the probability of survival between sexual and asexual offspring? • Asexual reproduction (clonal) mode means offspring are identical to parent (mother) • Sexual mode leads to diversity. • Recombination • Linkage disequilibrium • Muller’s ratchet versus fluctuating environment

23. By the late 1980s, in the contest to explain sex, only two hypotheses remained in contention. • One, the deleterious mutation hypothesis, was the idea that sex exists to purge a species of damaging genetic mutations • Alexey Kondrashov has been its principal champion • He argues that in an asexual population, every time a creature dies because of a mutation, that mutation dies with it. In a sexual population, some of the creatures born have lots of mutations and some have few. If the ones with lots of mutations die, then sex purges the species of mutations. Since most mutations are harmful, this gives sex a great advantage. (imagine cars in a junkyard…)

24. The main defect in Kondrashov's hypothesis is that it works too slowly. • Pitted against a clone of asexual individuals, a sexual population must inevitably be driven extinct by the clone's greater productivity, unless the clone's genetic drawbacks can appear in time. • Currently, a great deal of effort is going into the testing of this model by measuring the deleterious mutation rate, in a range of organisms from yeast to mouse. But the answer is still not entirely clear.

25. In the late 1980s the Red Queen hypothesis emerged, and it has been steadily gaining popularity. • First coined by Leigh Van Valen of the University of Chicago, it refers to Lewis Carroll's Through the Looking Glass, in which the Red Queen tells Alice, "[I]t takes all the running you can do, to keep in the same place.” • This never-ending evolutionary cycle describes many natural interactions between hosts and disease, or between predators and prey: As species that live at each other's expense coevolve, they are engaged in a constant evolutionary struggle for a survival advantage.  

26. The Parasite Red Queen hypothesis for sex is simple: Sex is needed to fight disease. • Diseases specialize in breaking into cells, either to eat them, as fungi and bacteria do, or, like viruses, to subvert their genetic machinery for the purpose of making new viruses. • To do that they use protein molecules that bind to other molecules on cell surfaces. • The arms races between parasites and their hosts are all about these binding proteins. Parasites invent new keys; hosts change the locks. For if one lock is common in one generation, the key that fits it will spread like wildfire.

27. So you can be sure that it is the very lock not to have a few generations later • According to the Red Queen hypothesis, sexual reproduction persists because it enables host species to evolve new genetic defenses against parasites that attempt to live off them. • W. D. Hamilton

28. Sexual species can call on a "library" of locks unavailable to asexual species. • This library is defined by two terms: heterozygosity, when an organism carries two different forms of a gene • and polymorphism, when a population contains multiple forms of a gene. Both are lost when a lineage becomes inbred • What is the function of heterozygosity? In the case of sickle cell anemia, the sickle gene helps to defeat malaria. So where malaria is common, the heterozygotes (those with one normal gene and one sickle gene) are better off than the homozygotes (those with a pair of normal genes or sickle genes) who will suffer from malaria or anemia.  

29. One of the main proponents of the Red Queen hypothesis was the late W. D. Hamilton. • In the late 1970s, with the help of two colleagues from the University of Michigan, Hamilton built a computer model of sex and disease, a slice of artificial life • It began with an imaginary population of 200 creatures, some sexual and some asexual. Death was random. As expected, the sexual race quickly died out. • In a game between sex and "asex," asex always wins -- other things being equal. That's because asexual reproduction is easier, and it's guaranteed to pass genes on to one's offspring.

30. Next they introduced several species of parasite, 200 of each, whose power depended on "virulence genes" matched by "resistance genes" in the hosts. • The least resistant hosts and the least virulent parasites were killed in each generation. • Now the asexual population no longer had an automatic advantage -- sex often won the game. • It won most often if there were lots of genes that determined resistance and virulence in each creature.

31.   In the model, as resistance genes that worked would become more common, then so too would the virulence genes. Then those resistance genes would grow rare again, followed by the virulence genes. • As Hamilton put it, "antiparasite adaptations are in constant obsolescence.” • But in contrast to asexual species, the sexual species retain unfavored genes for future use. • "The essence of sex in our theory," wrote Hamilton, "is that it stores genes that are currently bad but have promise for reuse. It continually tries them in combination, waiting for the time when the focus of disadvantage has moved elsewhere."

32. A host parasite arms race can make sex beneficial: • Hosts resistant to parasite genotype I are necessarily susceptible to genotype II, and vice versa. • As the parasite population evolves in response to the hosts, it first selects for hosts resistant to parasite genotype I, then for hosts resistant to parasite genotype II. • Genes for sex ride to high frequency in the currently more-fit genotypes they help create.

35. Case study II:Parasites and the Hamilton Zuk hypothesis

36. Why is life so colorful? • Many male birds, for example, have showy colors that are favored by females • Hamilton and Zuk suggested that bright colors might be a costly (and honest) signal of a robust immune system • Scarce carotenoids can either be used for immunocompetence or showiness  

37. Further reading: For a readable introduction to the Red Queen and its links to human behavior

38. Further reading: For a brilliant synthesis on the role infectious disease has played in the unfolding of world history.

39. Further reading: For some great papers on the role of parasites in the evolution of sex and sexual selection