Conflict

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Wolbachia microbial manipulator of insect
reproduction
Wolbachia microbial manipulator of insect
reproduction
T. WenseleersUniversity of Sheffield2002
Selfishness
Altruism course
T. WenseleersUniversity of Sheffield2002
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Conflicts in societies
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Intragenomic conflict

• Similar conflicts occur among genes within
  individual organisms
• Intragenomic conflict
• E.g. conflict
• between genes on homologous chromosomes over
  transmission to gametes (meiotic drive)
• between nucleus and cytoplasm over optimal
  sex-ratio (cytoplasmic sex-ratio distorters)
• between cells over who ends up in the germ-line

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Meiotic drive
section through sperm bundle
normal Mendeliansituationeach homologue
transmittedto half of the gametes
meiotic drive gene transmitted to all gametes
(but only half as much sperm produced)
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(No Transcript)
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Cytoplasmic sex-ratio distorters

• Cytoplasmic symbionts that manipulate their host
  into producing a female-biased brood
• Benefits their transmission to future generations
  because of their exclusively maternal inheritance
• Mechanisms
• Selective killing of male offspring / function
• Feminisation of genetic males
• Induction of parthenogenesis
• Increasing the fertilisation frequency in
  male-haploids

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W.D. Hamilton (1936-2000)Extraordinary
sex-ratios, Science 1967
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Wolbachia

• Example of a Cytoplasmic Sex-Ratio Distorter
• Alpha-proteobacterium
• Occurs in 15-75 of all insects in crustacea,
  spiders and nematodes
• Biases sex-ratio via
• Male killing
• Feminisation
• Parthenogenesis induction
• May cause mating incompatibilities
• High temperature or tetracycline cure the host

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First observed by Hertig Wolbach (1924)

• Intracellular rickettsial bacterium in ovaries of
  mosquito Culex pipiens
• Wolbachia pipientis

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The DNA revolution

• Amplification of Wolbachia DNA up to detectable
  levels has become possible using PCR-techniques
• Cloning and sequencing of various genes (16S
  rRNA, ftsZ, wsp) allows detailed analysis

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EUBACTERIA
ARCHAEBACTERIA
mitochondria
Riftia
Haloferax
E. coli
Wolbachia
Chromatium
Methanospirillum
Methanosarcina
Chlorobium
Cytophaga
Sulfolobus
Methanobacterium
Epulopiscium
Thermoproteus
Methanococcus
Bacilllus
Thermofilum
chloroplast
pSL 50
Thermococcus
Synechococcus
Methanopyrus
pSL 4
Thermus
pSL 22
Thermomicrobium
pSL 12
Thermotoga
Aquifex
origin
marinegroup1
pJP 27
EM 17
pJP 78
EUCARYA
macroscopicorganisms
Tritrichomonas
Zea
Homo
Coprinus
Paramecium
Giardia
Porphyra
Hexamita
Dictyostelium
Vairimorpha
Physarum
Naegleria
Entamoeba
Euglena
Encephalitozoon
Trypanosoma
0.1 changes per nt
C. Woese
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Jack Werren,University of Rochester
Gregory Hurst,UCL, London
Richard StouthamerUniversity of
California,Riverside
Scott ONeillUniversity of Queensland, AU
Ary Hoffmann,La Trobe, AU
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Phylogeny
Other alpha proteobacteria
Gamma proteobacteria
Wolbachia
0.1
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No match with host phylogeny
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• Male killing
• Selective killing of males
• In Tribolium and ladybird beetles, Drosophila
  and Acraea butterflies
• Increases the survival of sisters in the same
  brood, who carry copies of the maternal element
• Kin selected benefit

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Male killing in ladybird beetle
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• Male killing
• Causes cost at population/species level(dearth
  of males, decreased female mating success)
• E.g. in Acraea encedana 96 of all wild-caught
  butterflies are female
• Still male killing remains selected for since
  even at high frequency a sex-ratio distorter
  transmits more of its genes to future generations
  than a symbiont not distorting the sex-ratio

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Feminisation

• In woodlice
• Causes genetic males (ZZ) to develop as ZW
  females
• Works by suppressing the androgenic gland
• Also causes cost at population/species
  level(dearth of males, decreased female mating
  success)

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Induction of parthenogenesis

• Induction of asexual reproduction, resulting in
  an all-female brood
• Sex-ratio benefit avoids cost of sex
• Occurs in various parasitoid waspse.g.
  Trichogramma, Muscidifurax, Aphytis, Diplolepis
• Restoration of diploidy via gamete duplication

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Other Examples

• Feminization
• microsporidia in Amphipods
• Male killing
• Spiroplasma and Rickettsia in Drosophila and
  ladybird beetle
• Arsenophonus nasoniae in Nasonia vitripennis
  (parasitoid jewel wasp)
• microsporidia in mosquitoes

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Other Sex Ratio Distorter Types

• Cytoplasmic male sterility
• cf. male killing, but in plants
• male function inhibited
• Increased fertilization frequency
• in haplo-diploids fertilized eggs females
• maternal sex-ratio

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• Cytoplasmic male sterility
• in approx. 4 of all hermophrodite plants
• determined by mitochondrial gene
• mitochondria kill themselves when they find
  themselves in tissue of male function
• nuclear genes may suppress CMS

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• Maternal sex-ratio
• manipulates her host (Nasonia) to fertilise more
  eggs than she is selected to
• Nasonia is haplodiploid, so fertilised eggs
  develop as females.
• exact nature unknown

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Cytoplasmic incompatibility
Inviable

-

• Reduces fitness of Uninfected Female x Infected
  Male Crosses
• Gives an advantage to infected females
• Sterility in diploids, but production of males
  only in haplo-diploids

NormalOffspringProduction
-

-
-
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Mechanism

• Condensation of paternal genome in infected
  male
• Rescue by Wolbachia in egg upon fertilisation
  of infected oocyte

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CI may drive speciation

• Unidirectional incompatibility
• UNINFECTED FEMALE x INFECTED MALEincompatible
• other crosses unaffected
• Bidirectional incompatibility
• A STRAIN INFECTED FEMALE x B strain INFECTED
  MALEincompatible and vice versa
• may drive sympatric speciation

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Wolbachia in nematodes

• Mutualistic
• Wolbachia required for nematode reproduction
• Nematodes die when treated with tetracycline
• Strict host-parasite coevolution(concordant
  phylogenies)
• Offers new avenues for treatment of filarial
  diseases

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Concluding remarks

• Two ways for Wolbachia to increase its fitness
• Increase host fecundity (cf. nematodes)
• Manipulation
• How are conflicting genetic interests
  resolved? Parliament of the Genes? (E.
  Leigh) Majority Interests Prevail
• small Wolbachia genome powerless against a large
  autosome ?

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Take-home questions

1. Meiotic drive genes often do not go to fixation
   because drive/drive homozygotes tend to be
   near-sterile. If k is the fraction of drive
   gametes produced by a drive/wild type
   heterozygote and H is the fitness of a
   drive/drive homozygote, what is the equilibrium
   frequency of the drive allele in the population?
2. Are male killing elements selected to kill just
   as many males in large as in small populations?
   In the limit where on would have a population of
   only one female, what should the male-killing
   symbiont do?

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Maynard Smith Price 1973
Game theory(hawk-dove game)
PLAYER 2
DOVE
HAWK
DOVE
0 -B
PLAYER 1
HAWK
B -C
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Solving for an ESS
- SYNERGY

• Fitness player 1 w1 B.z1-B.z2-C.z1.z2 z1 en
  z2 phenotypes of players 1 2 (hawk1,
  dove0)
• Personal benefit of playing hawk influence of
  own behaviour on own fitness dw1/dz1 B-C.z2
  (depends on what other player does)
• At equilibrium benefit B-C.z2 0, and the ESS
  is to play hawk with a probability of zB/C

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Meiotic drive
HOMOLOGUE 2
COOPERATE
DRIVE
COOPERATE
(1-k)
1/2
HOMOLOGUE 1
DRIVE
k
H.(1/2)
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Solution problem 1
If z1 and z2 are the probabilities that genes on
chromosomal homologue 1 and 2 play as drive
alleles, we can write the fitness of the gene on
homologue 1 as w1 (1-z1).(1-z2).(1/2) (neither
of them drive, hom. 1 gets half of the gametes)
z1.(1-z2).k (homologue 1 shows drive, the
other hom. does not,
hom. 1 then gets a share k gt 1/2
of the gametes) (1-z1).z2.(1-k) (homologue 1
is mendelian, the other hom. shows drive)
z1.z2.(H/2) (both drive, each get half of the
gametes, but drive/drive type only produces a
fraction H of the gametes of the normal wild
type) The benefit for homologue 1 to drive with a
probability z1 is Dw1,z1 (where D stands
for a partial derivative - the idea is to
calculate how your behaviour influences your
reproduction) -(1-z2).(1/2)k.(1-z2)-(1-k).z2z2
.H/2
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Solution problem 1
As one can see, in a population where all
chromosomes play the fair Mendelian strategy
(z20), drive confers a benefit (when z20 the
benefitk-1/2). This benefit reduces as drive
becomes more common, however, because of the cost
that arises in drive/drive pairs. The selective
pressure to drive with higher probability stops
when the Dw1,z1 drops to zero. At that point
the ESS (evolutionary stable state) is
reached. So at the ESS we have
-(1-z2).(1/2)k.(1-z2)-(1-k).z2z2.H/2 0 from
which we can solve for the ESS strategy,
z(2k-1)/(1-H), i.e. if a gene drives with this
probability it cannot be invaded by any other
gene that drives with a another (higher)
probability.
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Solution problem 1
Technically we have now derived what is known as
a mixed strategy ESS, that is the situation
whereby the players adopt a probabilistic
strategy, e.g. drive or play hawk with a
particular probability. Alternatively, we could
also have derived what is known as a pure
strategy ESS where players play fixed strategies.
The ESS will then be reached when these different
types (genotypes) of players occur in some
equilibrium mix in the population. Fortunately,
it has been shown that for 2-player games the
mixed and pure ESS always coincide so that the
above result also describes the equilibrium
frequency of a drive allele in a population
(assuming that driving and non-driving alleles
have a different genetic constitution, which is
indeed the case). A more orthodox way to
calculate this result would be to construct a
genetic model and write down a recurrence
equation that describes how a drive allele
increases in frequency from one generation to the
next. The equilibrium frequency is then reached
when the frequency of the drive allele does not
change between generations. Hartl Clark (1997)
has a simple derivation. Hartl, D. L. Clark, A.
G. 1997. Principles of population genetics.
Sunderland, MA Sinauer Ass. The result is the
same though, and which approach to use is a
matter of taste.For a general overview of game
theory as applied to problems in biology
see Maynard Smith, J. 1982. Evolution and the
Theory of Games. New York Cambridge University
Press.
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Solution problem 2
In a large population the best strategy for a
cytoplasmic male killer is to kill all males in a
brood so as to bias the brood sex ratio to a
maximum extent. In a very small population,
however, biasing the sex ratio will also have
costs to the females in the same brood, because
they will be unable to find a male to mate with,
and the Wolbachia will die with them. In a large
population this wouldnt matter since this cost
would be carried by females in the population at
large, which contain Wolbachia unrelated to
actual male killing Wolbachia in the focal brood.
In a small population, however, this is no longer
true because it will be females of the very same
brood that will have a reduced mating success as
a result of the male killing. In the limit where
we would have a population of only one female,
that produces offspring that mate among
themselves, the best strategy for the Wolbachia
would be to kill no males at all, and have the
host produce an equal sex ratio (this assumes
that one male is needed to fertilise one female).