A Motor of Evolution Sexually Selected Intersexual Conflict

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A Motor of Evolution - Sexually Selected
Intersexual Conflict
-Brett Holland -Bill Rice
Why am I so pretty?
2
1. Physical environment
Arctic pack-ice
Polar bear
Ursus arctos
Terrestrial
Brown bear
(grizzly)
Ursus savini Prehistoric ancestor
Ursus maritimus
3
2. Biotic environment
Adaptation
Mutualism
Counter-adaptation
4
3. Biotic environment
Adaptation
Focal species
Enemies
Predators Pathogens Competitors
Conflict (Red Queen)
(VanValen 1973)
Counter-adaptation
5
Today
Sexual environment
Adaptation
Conflict and/or Mutualism?
Counter-adaptation
6
Sexual selection

• Hypothesis 1 Mutualism / benefits

it appears that the strongest and most vigorous
males have prevailed under nature and have led
to the improvement of the natural breed or
species. (Darwin, 1871, p. 258)
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Hypothesis 1 Mutualism

• What Darwin implied

Adaptation to physical biotic environment
Sexually selected males
8
The model organism

Experimental Power

Drosophila melanogaster
Courtship dance, wing song, hydrocarbons
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Drosophila Experiments
Random monogamy (no opportunity for sexual
selection)
Partridge 1980
Reduced, D. melanogaster
Juvenile survival
No difference, D. melanogaster No difference, D.
psuedoobscura
Schaeffer et al. 1984

No difference, D. melanogaster
Promislow et al. 1998
Adult female survival
Unclear1, D. melanogaster
Promislow et al. 1998
1no difference during period to which females are
selected
10
What is needed for progress?

• Measure net RS

Fitness components may negatively covary
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2. Increase variation in fitness

Additive
genetic
neutral low frequency
variation
selected
New stressful environment
Stable

environment
12
2. Increase variation in fitness
13
3. Increase the number of generations of
selection
14
Experimental design
Replicate

Experimental

samples
populations
Treatments
1
Y

Monogamy
MA
1
X

A
N133
X

Drosophila

4
Y

melanogaster
Polyandry
PA
1
X
Starting

N133
X

population
......
Monogamy
MB
N
gt5,000
e
B
CB
......
PB
Polyandry
CA
Thermal control A
N133
X

CB
CB
Thermal control B
N133
X

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Thermal regime
16
Thermal regime
Productivity (total offspring) Development rate
17
Substantial adaptation through both productivity
and development rate
20
15
C
RS
10
M
5
0
35
46
Generations of selection
18
No difference in rate of adaptation between
monogamous and promiscuous populations
M
Polyandrous mating environment
Monogamous mating environment
P
15
20
P 0.4
P 0.9
P 0.6
15
10
Net
reproductive
RS
RS
10
rate
5
5
0
0
36
37
38
49
50
51
Generations of selection
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Why is sexual selection not facilitating
adaptation?
1. Heritable variation in thermal stress
tolerance?

6 standard deviations of adaptation
2. Is the thermal regime relevant to adaptive
sexual selection?
a. D. melanogaster in nature experience
temperatures within this range (Feder et
al.1997)
b. Natural clines of thermal adaptation exist
(James and Partridge 1995)
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No evidence that sexual selection is reinforcing
selection outside of the context of sexual
selection in D. melanogaster


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Sexual selection

• Hypothesis 2 Conflict

Sexual selection generates conflict Arms races
between and among the sexes
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Seminal fluid proteins
Male benefit
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Seminal fluid proteins
Male benefit
Female cost?
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Seminal fluid proteins
Female cost?
Male benefit
female Optimum
male Optimum

Female lifetime reproductive success

Female reproductive rate

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Courtship
Male benefit
Female cost?
Male mating rate
Female lifespan
(Partridge Fowler 1990)
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The Intraspecific Red Queen
(Rice Holland 1997)
Adaptation also reduces female survival
Sperm competition
A
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The Intraspecific Red Queen
(Rice Holland 1997)
Adaptation also reduces female survival
Sperm competition
B
A
disables protein A
Counter-adaptation reduces male fertilization
success
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The Intraspecific Red Queen
(Rice Holland 1997)
Adaptation also reduces female survival
Sperm competition
B
A
disables protein A
Counter-adaptation reduces male fertilization
success
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The Intraspecific Red Queen
(Rice Holland 1997)
Adaptation also reduces female survival
Sperm competition
B
A
disables protein A
Counter-adaptation reduces male fertilization
success
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Removing the conflict
Monogamy (with random mate assignment) RS between
mates is identical no sexually selected
conflict (developmental conflict retained)
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Experimental design
Replicates
Treatments
Experimental populations
Monogamous A
Monogamous
n114 Vials
A
3 Males 1 Female
Promiscuous A
Promiscuous

n114 Vials
Monogamous B
.....................
B
Promiscuous B
.....................
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After 34 generations of divergence
Assays
1. Male effects 2. Female effects 3. Combined
Specific traits predicted to change by each
hypothesis
Assayed flies reared Identical
environment Density controlled
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1. Monogamous male harm to test females is
diminished
2. Monogamous male seminal fluid appears less
toxic
Females continuously exposed
Females mated once, males removed
1.3
(N.S.)

1.2
1.1
Relative

1
value
0.9
0.8
0.7
Female reproductive success
Female survival
Female lifetime fecundity




All data shown (no error bars)
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Monogamous males court less
Promiscuous males
Monogamy males
100
75
Courtship
50
bouts
25
0
A
B
Replicate
35
Consistent with reduction in sexual conflict
Mutualistic adaptation
Counter-adaptation?
36

Monogamous females die quickly with ancestral
males
1
0.9
0.8
Promiscuous females
0.7
0.6
Surviving females
Monogamous females
0.5
0.4
0.3
0.2
0.1
0
0
10
20
30
40
50
Time (days)
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Monogamous females are less fecund with
ancestral males
Promiscuous females
Monogamous females
3
2
1
0
A
B
Replicate
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Inbreeding depression?

• It also predicts the presented results
• Effective population size is slightly smaller
  under monogamy

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Reproductive Success
Predicted reproductive success
Hypothesis
Promiscuity gt Monogamy Promiscuity lt Monogamy
Inbreeding Sexual conflict
mutualism/benefits hypothesis predicts same
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Reproductive Success
Generation
Measure
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Monogamous populations reproductive rate gt
Promiscuous
Reproductive success
50
40
30
Percent
20
difference
10
0
-10
45
46
47
Generation
42
Reproductive success
Total adult progeny (N.S.)
50
40
30
Percent
20
difference
10
0
-10
45
46
47
45
46
47
Generation
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Monogamous populations development rate gt
Promiscuous
Reproductive success
Total adult progeny (N.S.)
Development rate
50
40
30
Percent Difference
20
10
0
-10
45
46
47
45
46
47
45
46
47
Generation
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Conclusions

• Specific traits hypothesized to mediate sexual
  conflict evolved in response to the removal of
  sexual selection.
• This resulted in a rapid increase in net
  reproductive success.
• Sexual selection is a net load on these
  populations.

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What about the pretty traits?
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Chase-away Sexual Selection

• Hypothesis the result of sexual conflict
• Three lines of evidence
• Intersexual conflict (shown previously)
• Sensory bias
• Reduction in bias

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Incidental preference (sensory bias)
Eurasian oystercatcher
Tinbergen 1951
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Females prefer longer sworded males
Xiphophorus
800


600

Time (s)

400
Basolo 1995


200


0
20

25

30

35

40

45

50
Sword length (mm)
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Phylogeny
Basolo 1995
Other
Xiphophorus
P
riapella
Poeciliids
male
ornament
Time
50
Artificial swords
P
riapella
800


600

Time (s)

400
Basolo 1995


200


0
20

25

30

35

40

45

50
Sword length (mm)
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Sensory bias results in sensory exploitation
Basolo 1995
Other
Xiphophorus
P
riapella
Poeciliids
male o
rnament
Female preference
Time
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Sensory exploitation
Tungara frogs (

Ryan Rand 1993)
Sword tailed fishes
(Basolo 1990 1995)
Wolf spiders
(McClintock and Uetz 1996)
Sp B
Sp A
O
rnament
Female bias
Time
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Chase-away ornament evolution
(Holland Rice 1998)
!
Incidental


S
ensory bias
preference
Direct f
emale
costs
Diminished effectiveness
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Unique Prediction
Female preference (bias) should decline after
the evolution of the male ornament
decreased
female bias
male o
rnament
female bias
(Benefits hypotheses make the opposite prediction)
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Relative f
emale bias for swords
Basolo 1998
Priapella

800
m1.3


600
Xiphophorus


m0.8

Time (s)
400


40 reduction in bias(slope)
200


0
20

25

30

35

40

45

50
Sword length (mm)
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Other
Xiphophorus
P
riapella
Poeciliids
decreased
female bias
male o
rnament
female bias
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Wolf spiders
Schizocosa
sp.

McClintock and Uetz 1996
S. ocreata
S. rovneri
m
ale ornament?
f
emale bias?
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N
on
tufted sp.

McClintock Uetz 1996
Female bias

Blank
C
ontrol



Tufts
V
ideo image
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McClintock Uetz 1996
T
ufted sp.
N.S.
Female bias
-

Tufts

Control Tufts exaggerated
Blank
V
ideo image
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S. ocreata
S. rovneri
f
emale bias
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Chase-away Sexual Selection

• Three lines of evidence
• Intersexual conflict (e.g., over mating rate).
• Sensory bias female preference evolves before
  the male ornament.
• Reduction in female bias following the
  evolution of male ornaments (sensory
  exploitation) females appear to evolve decreased
  preference (bias) for ornaments in the only
  species for which we have phylogenetic data.
• Conclusion Chase-away sexual selection can occur
  between male-benefit genes that make ornaments
  and female-benefit genes that mediate sensory
  systems.

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Leftovers
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Intersexual conflict
S
ex-specific optima
R
elative
optimum
Low
High
X
Y
Mating rate
Seminal fluid
toxicity
X
Y
Y
(mate)
(non-mate)
Female
remating rate
Y
X
Female
fecundity
X
Y
Female age at
first copulation
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population
individual
locus alleles (A, a, etc.)
A
a
a
A
A
mutation
Natural selection
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Mutualism The empirical evidence
Reproductive Success
Fecundity
Survival
Development rate
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Measuring adaptation
M
M
C
Acclimation
Net reproductive rate
0.......................................35 46
2 generations

Productivity
Generations of selection

Development rate
n133 females/population
All populations under monogamy environment
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Why males usually compete for females
Obligate parental investment
Reproductive rate limited by
Low
Fertilizations
High
Material resources
egg
(Trivers 1972)
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Evolutionary Experiment
Divergence
Trait value
Time
Time 32-47 generations
Assays