Sept2_Lecture3

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Lecture 3The central role of parasites in
evolution
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The central role of parasites in
evolution J.B.S. Haldane (1892-1964)
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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.
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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

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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?

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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

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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?

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Disease and Evolution, 1949
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Disease and Evolution, 1949
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Disease and Evolution, 1949

• Huge difference between developed and developing
  world
• Infectious disease still kills gt 1/3 of people
  worldwide
• Mostly in developing countries (big populations)
  and mostly kids

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Disease and Evolution, 1949

• How do you think infectious disease has impacted
  the human population through history (and
  pre-history)?

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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

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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/grafs/demos/15.html
  

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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

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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)

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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.

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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?

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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?

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

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Disease and Evolution, 1949

• http//www.gi.alaska.edu/ScienceForum/ASF9/977.htm
  l
• 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.

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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.

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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.

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Case study I Parasites and the advantage of sex
Which reproductive mode is better sexual or
asexual?

• JMS died recently
• Student of Haldane
• Aircraft engineer in WWII, came to biology later
  in life
• Leading thinker on the evolutionary scandal of
  sex

• John Maynard Smith

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• 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?

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Case study I Parasites and the advantage of sex
Which reproductive mode is better sexual or
asexual?

• Null model (what a null model?)
• A females reproductive mode does not affect the
  number of offspring she can make
• A females reproductive mode does not affect the
  probability that her offspring will survive
• (John Maynard Smith, 1978)

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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?

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In a population conforming to JMSs assumptions,
asexual females produce twice as many
grandchildren as sexuals, and fraction of
asexuals climbs
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• Asexuals should take over. And yet the vast
  majority of multicellular species are sexual.
• Whats going on?
• JMSs model illustrates, as he intended it to,
  that these facts represent a paradox for
  evolutionary theory
• Its an evolutionary scandal!

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• 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.

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

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• 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

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• 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
• (its a double-edged sword.Why?

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• 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)

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• 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.

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• 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, "It 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. 

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• 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)

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• 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)

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• 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.  

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• 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.

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• 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.

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•   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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• 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.

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"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!"
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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
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Case study IISexual selection, parasites and the
Hamilton Zuk hypothesis
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• 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? 

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• 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

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• 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?

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• 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

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• 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

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• 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.  

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• 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  

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• 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  

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Further reading
For a readable introduction to the Red Queen and
its links to human behavior
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Further reading
For a brilliant synthesis on the role infectious
disease has played in the unfolding of world
history.
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Further reading
For some great papers on the role of parasites in
the evolution of sex and sexual selection
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Further reading
For a nice introduction to some of the best
primary literature in evolutionary biology,
including the Haldane paper on disease