Lecture 4 The central role of parasites in evolution

1. Lecture 4The central role of parasites in evolution

2. Today: • 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. 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

4. 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…

5. 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. • Mutant forms of genes can spread easily through a population • Recombination: the formation of hybrid DNA molecules combining genetic information from two sources into a new mosaic • (it’s a double-edged sword….Why?)

6. 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…)

7. 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.

8. 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. • The cyclical nature of these battles could be the key to much of the genetic diversity observed in nature. 

9. 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. (frequency dependent selection)

10. 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. • (see Hamilton Symposium pdf)

11. 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.  (tradeoff)

12. One of the main proponents of the Red Queen hypothesis was the late W. D. Hamilton. • “Sex must be shown to be advantageous to the individual sexist, not just to population or species as as a whole”

13. 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.

14. 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.

15.   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."

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19. 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.

20. "Well, in our country," said Alice, still panting a little, "you'd generally get to somewhere else—if you ran 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!"

21. “If the idea about parasites is right, species may be seen in essence as guilds of genotypes committed to free fair exchange of biochemical technology for parasite exclusion.” -Bill Hamilton

22. Case study II:Sexual selection, parasites and the Hamilton Zuk hypothesis

23. Why is life so colorful? • Many male birds, for example, have showy colors that are favored by females • The colors are status symbols…but of what, exactly? • Does a male peacock’s tail help it gather food, or avoid predators? 

24. It seems a sort of costly way to advertise…. • The high price is actually the key to understanding the information being communicated • Impressively adorned males must be the “fittest” of their kind, capable of investing more energy into their sexual signals • Cheap signals invite cheating

25. An honest signal must be costly to produce • Called the Handicap Principle by Amotz Zahavi: honest signals will be ones that are too pricey to be acquired by low-quality males, ensuring only the best males can invest in such signals (flashy sports car?) • A female prefers a male with a handicapping trait because this male must have high viability (good genes) to be able to survive with the handicap • But what it meant by “low” and “high” quality males?

26. Hamilton and Zuk suggested that genes for resistance might have important effects on fitness and always remain heritable (why?) • They suggested that bright colors might be a costly (and honest) signal of a robust immune system • This links showy sexually selected characteristics with disease… • Only males with good genes for parasite resistance would be in prime condition to express showy colors • Sick males (“low” quality) will look drab in comparison

27. “The choosing animal should unclothe the subject, weigh, listen, observe vital capacity, and take blood, urine, and fecal samples” • Or… • “Instead, if a male can present an elaborate bright plumage, prodeuce a song that is energetically costly, and display with an exhausting athletic behavior, it likewise has the currently needed genes for resistance because it so demonstrates that it is healthy.” • (From the Hamilton Symposium reading)

28. Various false starts: parasite load, testosterone, etc. • Carotenoids are a family of natural pigments, and are often the source of bright colors in animals • The pigments can be stored in various tissues, and are actually mainly made by plants and algae • They’re acquired through eating plants or eating other animals that have eaten plants

29. Females finches, guppies, sticklebacks, etc. prefer males with brighter carotenoid-based coloration • It turns out that they are costly. They’re used by the immune system and for detoxification to neutralize free radicals • They stimulate the proliferation of T and B lymphocytes • Scarce carotenoids can either be used for immunocompetence or showiness and unfit males just can’t fake it.  

30. 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  

31. 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  

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

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

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

35. Further reading: For a nice introduction to some of the best primary literature in evolutionary biology, including the Haldane paper on disease