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Lecture 3 The central role of parasites in evolution Slide 2 Today: vitamins http://viscog.beckman.uiuc.edu/grafs/demos/15.html Constraints on adaptation Haldanes prescient 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 Slide 3 natural selection and adaptation Adaptation is both a process and a state The process of adaptation = what happens over successive generations of selection of heritable variation in reproductive success The state of adaptation = a particular trait that does a job very well, just as though it were designed by an engineer E.g. opposable thumb, acute hearing, vision, sex drive, camouflage, venom, crystallins in eyes Slide 4 Constraints on adaptation Natural selection does not produce perfection Rather it is a tinkerer that produces good- enough solutions to context dependant problems. Often this occurs through duplication and divergence Slide 5 Constraints on adaptation As natural selection acts by competition, it adapts the inhabitants of each country only in relation to the degree of perfection of their associates; so that we need feel no surprise at the inhabitants of any one country, although on the ordinary view supposed to have been specially created and adapted for that country, being beaten and supplanted by the naturalised productions from another land. Slide 6 Constraints on adaptation Nor ought we to marvel if all the contrivances in nature be not, as far as we can judge, absolutely perfect; and if some of them be abhorrent to our ideas of fitness. Slide 7 Constraints on adaptation Time is a major constraint on adaptation. It takes time to generate variation and select for it Absorption of milk sugar (lactose) by human adults Normally lactase is effective until weaning age (about 4). If you cant digest lactose you suffer flatulence, intestinal cramps, diarrhea, nausea, vomiting But in cultures where dairy has been used for thousands of years, >90% of adults can digest lactose, like giant, lumbering babies Thousands of years, but probably not decades, are sufficient for this selection to shape human evolution Slide 8 Constraints on adaptation Trade-offs are major constraints too E.g. sex is dangerous for fruit flies. There is a trade-off between survival and reproduction Similarly, there is a trade-off between having a robust immune system and suffering from asthma, or lupus, or diabetes type I Other trade-offs? Slide 9 Constraints on adaptation Historical constraints are also important: How strange it is that a bird, under the form of woodpecker, should have been created to prey on insects on the ground; that upland geese, which never or rarely swim, should have been created with webbed feet Slide 10 Constraints on adaptation Historical constraints are also important: The vertebrate eye has a basic flaw: the nerves and blood vessels that feed it enter right in the middle of the region of photosensitive cells. You would fire any engineer who designed an optical device in this way, but because of developmental constraints deriving from much simpler, ancestral eyes, thats what were stuck with If squid could talk, they would taunt us about our poorly designed eyes (maybe). Slide 11 Both vertebrates and cephalopods exhibit a single-lens eye structure that possesses a cornea, iris, and lens These two structures are in fact not homologous These similarities were all produced by convergent evolution a term used to describe the independent development of similar traits between species as a result of their having similar ecological roles and selection pressures Specifically, both cephalopods and vertebrates use their eyes extensively for hunting and survival and as a result require highly sophisticated visual systems Slide 12 Release from constraint: adaptive radiation Adaptive radiations can occur when new ecological niches open up, or a new adaptation opens up new possibilities (each beetles/flowering plants) Natural selection can operate very rapidly in such cases to generate new adaptations Islands, such as the Galapagos, are classic areas for observing evidence of adaptive radiation (eg Darwins Finches) But other favorable conditions also exist. Slide 13 The Great Lakes of Africa are home to the most species rich vertebrate radiation Hundreds of species in each lake, with relatively recent common ancestors A few million years for the ~500 species in Lake Malawi 12,000 years for Lake Victoria Slide 14 Evolutionary conflicts Lots of conflicts arise in nature: Predators and prey Parents and offspring Genes Insects and plants Fungi and crop plants they destroy Chromosomes competing for transmission through gametes Slide 15 Evolutionary conflicts Conflicts are where much of the action is in evolutionary biology Conflicts occur when genes have different patterns of transmission but interact, directly or indirectly, in the organisms that carry them Perhaps the most obvious example is genes of pathogens and genes of hosts Endless cycles of damage and damage control adaptations can lead to evolutionary arms races Slide 16 Evolutionary conflicts In one sense, these arms races lead to lots of adaptation In another, they present a serious constraint on adaptation and amount to running just to stay still. Slide 17 The central role of parasites in evolution J.B.S. Haldane (1892-1964) Slide 18 J.B.S. Haldane The son of a famous physiologist, he had a long history of using himself as a guinea pig in experiments with poisonous gases (along with his dad) Once lost two teeth, which exploded due to the rapid decompression in his sinuses, during one experiment Four stages of acceptance: i) this is worthless nonsense; ii) this is an interesting, but perverse, point of view; iii) this is true, but quite unimportant; iv) I always said so. Slide 19 J.B.S. Haldane (1892-1964) Though never awarded a doctoral degree, he made seminal contributions in several fields including biochemistry, enzymology, physiology In 1932 published The Causes of Evolution, a landmark in reconciling the theories of natural selection and Mendelian genetics Held the Galton Chair in Biometry, University College London, 1937-57 A visionary, who, earlier than perhaps anyone else, saw the importance of infectious disease in evolution Slide 20 Disease and Evolution, 1949 Obtaining food and mates and protection against natural forces such as cold, or predators, is only part of the story Useful to distinguish at this point between an organisms abiotic and biotic environment -abiotic? -biotic? Slide 21 Disease and Evolution, 1949 Of these, the biotic environment is probably much more important evolutionarily I want to suggest that the struggle against disease, and particularly infectious disease, has been a very important evolutionary agent Slide 22 Disease and Evolution, 1949 How important is disease as a killing agent in nature? One general trend may be disease as a density-dependent check on population growth (along with lack of resources, space) Why density dependent? The impacts of disease will of course differ for different speciesHow about for humans? Slide 23 Disease and Evolution, 1949 Slide 24 Slide 25 Huge difference between developed and developing world Infectious disease still kills > 1/3 of people worldwide Mostly in developing countries (big populations) and mostly kids Slide 26 Disease and Evolution, 1949 How do you think infectious disease has impacted the human population through history (and pre-history)? Slide 27 Disease and Evolution, 1949 A disease may be an advantage or a disadvantage to a species in competition with others Example of different cultures of Drosophila immune, or not, to a bacterial pathogen Example of wild southern African ungulates infected with trypanosomes Impossible to introduce cattle in such areas, and even African breeds have not had time to evolve immunity Native species (more to the point, individuals) are at an advantage because of the parasite, an important part of the biotic environment Slide 28 Disease and Evolution, 1949 Europeans have used their genetic resistance to such viruses as that of measles as a weapon against primitive as effective as fire-arms What other episodes in evolutionary history have been due to infectious disease rather than the sorts of adaptations we tend to focus on? http://viscog.beckman.uiuc.edu/g rafs/demos/15.html Slide 29 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 Slide 30 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 Negative and positive frequency-dependent selection: (when be rare or common is selectively advantageous) Slide 31 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. Slide 32 Disease and Evolution, 1949 Social aspects of disease It will be on the whole an antisocial agencyit 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? Slide 33 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? Slide 34 Disease and Evolution, 1949 Given enough time a state of peaceful coexistence eventually becomes established between any host and parasite.-Rene Dubos Slide 35 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 Slide 36 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. Slide 37 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. Slide 38 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. Slide 39 Which reproductive mode is better: sexual or asexual? John Maynard Smith Case study I: Parasites and the advantage of sex JMS died recently Student of Haldane Aircraft engineer in WWII, came to biology later in life Leading thinker on the evolutionary scandal of sex Slide 40 Sex is costly, not to mention complicated and dangerousSex is costly, not to mention complicated and dangerous Searching for mates takes time and energy, and has risks (?)Searching for mates takes time and energy, and has risks (?) Potential mates may demand additional exertion or investment before matingPotential mates may demand additional exertion or investment before mating After all that, mating might prove to be infertileAfter all that, mating might prove to be infertile Why go to all the trouble?Why go to all the trouble? Slide 41 Which reproductive mode is better: sexual or asexual? Null model: (what a null model?) 1.A females reproductive mode does not affect the number of offspring she can make 2.A females reproductive mode does not affect the probability that her offspring will survive (John Maynard Smith, 1978) Case study I: Parasites and the advantage of sex Slide 42 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? Case study I: Parasites and the advantage of sex Slide 43 In a population conforming to JMSs assumptions, asexual females produce twice as many grandchildren as sexuals, and fraction of asexuals climbs Slide 44 Asexuals should take over. And yet the vast majority of multicellular species are sexual.Asexuals should take over. And yet the vast majority of multicellular species are sexual. Whats going on?Whats going on? JMSs model illustrates, as he intended it to, that these facts represent a paradox for evolutionary theoryJMSs model illustrates, as he intended it to, that these facts represent a paradox for evolutionary theory Its an evolutionary scandal!Its an evolutionary scandal! Slide 45 Sex must confer benefits that allow it to persist in spite of the strong reproductive advantage of parthenogenesis.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.The benefits must lie in the violation of one or both of those assumptions. 1.A females reproductive mode does not affect the number of offspring she can make 2.A females reproductive mode does not affect the probability that her offspring will survive Slide 46 The first assumption is actually violated in species in which fathers provide resources or parental care essential for producing young.The first assumption is actually violated in species in which fathers provide resources or parental care essential for producing young. This includes humans.This includes humans. But such species are in the minority. In most species, males contribute only genes.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 Slide 47 What might account for a difference in the probability of survival between sexual and asexual offspring?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)Asexual reproduction (clonal) mode means offspring are identical to parent (mother) Sexual mode leads to diversity.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 (its a double-edged sword.Why? Slide 48 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) Slide 49 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. Slide 50 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. Slide 51 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) Slide 52 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 (see Hamilton Symposium pdf Ill post tomorrow) Slide 53 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. Slide 54 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. Slide 55 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. Slide 56 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." Slide 57 A host parasite arms race can make sex beneficial:A host parasite arms race can make sex beneficial: Hosts resistant to parasite genotype I are necessarily susceptible to genotype II, and vice versa.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.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.Genes for sex ride to high frequency in the currently more-fit genotypes they help create. Slide 58 Slide 59 Slide 60 "Well, in our country," said Alice, still panting a little, "you'd generally get to somewhere elseif 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!" Slide 61 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 Slide 62 Case study II:Sexual selection, parasites and the Hamilton Zuk hypothesis Slide 63 Why is life so colorful? Many male birds, for example, have showy colors that are favored by females The colors are status symbolsbut of what, exactly? Does a male peacocka tail help it gather food, or avoid predators? Slide 64 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 Slide 65 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, $5000 suit, etc.) But what it meant by low and high quality males? Slide 66 Hamilton and Zuk 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 Slide 67 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 Theyre acquired through eating plants or eating other animals that have eaten plants Slide 68 Females finches, guppies, sticklebacks, etc. prefer males with brighter carotenoid-based coloration It turns out that they are costly. Theyre 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 cant fake it. Slide 69 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 Slide 70 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 Slide 71 Further reading: For a readable introduction to the Red Queen and its links to human behavior Slide 72 Further reading: For a brilliant synthesis on the role infectious disease has played in the unfolding of world history. Slide 73 Further reading: For some great papers on the role of parasites in the evolution of sex and sexual selection Slide 74 Further reading: For a nice introduction to some of the best primary literature in evolutionary biology, including the Haldane paper on disease