Lecture 12
Linkage disequilibrium and the
evolution of sex
The Evolution of Sex
1. The cost of sex
Sexual species
Female
Asexual species
Female
Male
AA
BB
AA
BB
AA
BB
AA
AA
AA
AA
AA
AA
AA
The Evolution of Sex
2.
Life without sex
Unisexual species
Poeciliopsis, Amazon mollies
Unisexual species
Amazon mollies
Hybridogenetic
AX
A
BB
B
AB
A
AA
AA
CC
C
Gynogenetic
BB
B
AA
AA
AA
AA
CC
C
Parthenogenetic
AA
AA
Unisexuals
Poeciliopsis
Rivulus marmoratus
The Evolution of Sex
3. Hermaphrodites
a.  Simultaneous hermaphrodites
b.  Sequential hermaphrodites
The Evolution of Sex
3. Hermaphrodites
b.
Sequential hermaphrodites
b1. Protogynous
Semicossyphus pulcher
California sheephead
b2. Protandrous
Amphiprion,
Clownfish
Simultaneous Hermaphrodites
Hamlets
Hypoplectrus
The Evolution of Sex
4.1: Environmental Sex Determination (ESD)
The Evolution of Sex
4.1: Environmental Sex Determination (ESD)
Atherina boyeri, Silverside
Linkage disequilibrium and the evolution
of sex
Linkage disequilibrium and the evolution
of sex
Q: What distinguishes sexual from asexual
reproduction?
Linkage disequilibrium and the evolution
of sex
Q: What distinguishes sexual from asexual
reproduction?
A: Meiosis and Syngamy
Linkage disequilibrium and the evolution
of sex
Q: What distinguishes sexual from asexual
reproduction?
A: Meiosis and Syngamy
Male
2N
Female
2N
Linkage disequilibrium and the evolution
of sex
Q: What distinguishes sexual from asexual
reproduction?
A: Meiosis and Syngamy
Male
Meiosis
Female
2N
2N
↓
↓
N
N
Linkage disequilibrium and the evolution
of sex
Q: What distinguishes sexual from asexual
reproduction?
A: Meiosis and Syngamy
Male
Meiosis
Syngamy
Female
2N
2N
↓
↓
N
N


2N
A model for the evolution of two sexes
A model for the evolution of two sexes
• in many species, sexual reproduction has entailed a
shift from isogamy to anisogamy.
A model for the evolution of two sexes
• in many species, sexual reproduction has entailed a
shift from isogamy to anisogamy.
Isogamy
+
-
A model for the evolution of two sexes
• in many species, sexual reproduction has entailed a
shift from isogamy to anisogamy.
Isogamy
-
+
Anisogamy
♀
♂
A model for the evolution of two sexes
Mating
type (M)
+/-
A model for the evolution of two sexes
Mating
type (M)
+/-
Gamete
size (G)
Small (S)/Large (L)
A model for the evolution of two sexes
Mating
type (M)
+/-
Gamete
size (G)
Small (S)/Large (L)

MG
Linkage disequilibrium
A model for the evolution of two sexes
Mating
type (M)
+/-
Gamete
size (G)
Small (S)/Large (L)

MG

MG
+S
♂
Linkage disequilibrium
A model for the evolution of two sexes
Mating
type (M)
+/-
Gamete
size (G)
Small (S)/Large (L)

Linkage disequilibrium
MG


MG
+S
MG
-L
♂
♀
MG
MG
+S
-L
♂
♀
MG
MG
+S
-L
♂
♀
Recombinants:
MG
MG
+S
-L
♂
♀
Recombinants:
MG
+L
↓ fitness due to
low sperm number
MG
MG
+S
-L
♂
♀
Recombinants:
MG
+L
↓ fitness due to
low sperm number
MG
-S
↓ fitness due to
inviable eggs
MG
MG
+S
-L
♂
♀
Recombinants:
MG
+L
↓ fitness due to
low sperm number
MG
-S
↓ fitness due to
inviable eggs
The system is stable (i.e., cannot be invaded)
What is linkage disequilibrium?
What is linkage disequilibrium?
Linkage equilibrium occurs when the
genotypes present at one locus are
independent of the genotypes present at a
second locus.
What is linkage disequilibrium?
Linkage equilibrium occurs when the
genotypes present at one locus are
independent of the genotypes present at a
second locus.
Linkage disequilibrium occurs when
genotypes at the two loci are not independent
of each other.
What is linkage disequilibrium?
What is linkage disequilibrium?
What is linkage disequilibrium?
Q: What causes linkage disequilibrium?
Q: What causes linkage disequilibrium?
1. Natural selection
Q: What causes linkage disequilibrium?
1. Natural selection
• can be produced by selective sweeps or by
epistatic selection
Q: What causes linkage disequilibrium?
1. Natural selection
• can be produced by selective sweeps or by
epistatic selection
• epistasis occurs when the fitness of a genotype
at one locus depends on its genotype at another
locus
What is linkage disequilibrium?
Q: What causes linkage disequilibrium?
1. Natural selection
• can be produced by selective sweeps or by
epistatic selection
• epistasis occurs when the fitness of a genotype
a one locus depends on its genotype at another
locus
2. Random genetic drift
Q: What causes linkage disequilibrium?
1. Natural selection
• can be produced by selective sweeps or by
epistatic selection
• epistasis occurs when the fitness of a genotype
a one locus depends on its genotype at another
locus
2. Random genetic drift
• weaker than selection in creating disequilibrium.
Q: What causes linkage disequilibrium?
3. Population admixture
Q: What causes linkage disequilibrium?
3. Population admixture
• can be as important as selection in creating
disequilibrium.
Q: What causes linkage disequilibrium?
3. Population admixture
• can be as important as selection in creating
disequilibrium.
Q: What eliminates linkage disequilibrium?
Q: What causes linkage disequilibrium?
3. Population admixture
• can be as important as selection in creating
disequilibrium.
Q: What eliminates linkage disequilibrium?
A: Recombination!
The decay of disequilibrium depends on
the rate of recombination (r)
How and why did sex evolve?
How and why did sex evolve?
or… how is sexual reproduction maintained in the
face of so many alternative strategies?
How and why did sex evolve?
or… how is sexual reproduction maintained in the
face of so many alternative strategies?
Some alternatives:
1. Parthenogenesis (both mitotic and sexual forms)
How and why did sex evolve?
or… how is sexual reproduction maintained in the
face of so many alternative strategies?
Some alternatives:
1. Parthenogenesis (both mitotic and sexual forms)
• organisms develop from unfertilized eggs.
Examples: some lizards, aphids, many plants
New Mexico whiptail lizard (Cnemidophorus neomexicanus)
↑
C. neomexicanus
How and why did sex evolve?
or… how is sexual reproduction maintained in the
face of so many alternative strategies?
Some alternatives:
1. Parthenogenesis (both mitotic and sexual forms)
• organisms develop from unfertilized eggs.
Examples: some lizards, aphids, many plants
2. Hermaphroditism (obligate or sequential)
How and why did sex evolve?
or… how is sexual reproduction maintained in the
face of so many alternative strategies?
Some alternatives:
1. Parthenogenesis (both mitotic and sexual forms)
• organisms develop from unfertilized eggs.
Examples: some lizards, aphids, many plants
2. Hermaphroditism (obligate or sequential)
• organisms possess both male and female reproductive
organs, or change sex at some point in their lives.
How and why did sex evolve?
or… how is sexual reproduction maintained in the
face of so many alternative strategies?
Some alternatives:
1. Parthenogenesis (both mitotic and sexual forms)
• organisms develop from unfertilized eggs.
Examples: some lizards, aphids, many plants
2. Hermaphroditism (obligate or sequential)
• organisms possess both male and female reproductive
organs, or change sex at some point in their lives.
Examples: many fishes, snails, worms
How and why did sex evolve?
or… how is sexual reproduction maintained in the
face of so many alternative strategies?
3. Haplodiploidy
How and why did sex evolve?
or… how is sexual reproduction maintained in the
face of so many alternative strategies?
3. Haplodiploidy
• haploid males develop from unfertilized
eggs,diploid females from fertilized eggs.
How and why did sex evolve?
or… how is sexual reproduction maintained in the
face of so many alternative strategies?
3. Haplodiploidy
• haploid males develop from unfertilized
eggs,diploid females from fertilized eggs.
Examples: ants, bees, wasps
How and why did sex evolve?
or… how is sexual reproduction maintained in the
face of so many alternative strategies?
3. Haplodiploidy
• haploid males develop from unfertilized
eggs,diploid females from fertilized eggs.
Examples: ants, bees, wasps
4. Pseudogamy (Gynogenesis)
How and why did sex evolve?
or… how is sexual reproduction maintained in the
face of so many alternative strategies?
3. Haplodiploidy
• haploid males develop from unfertilized
eggs,diploid females from fertilized eggs.
Examples: ants, bees, wasps
4. Pseudogamy (Gynogenesis)
• contact with sperm stimulates development from
unfertilized eggs.
How and why did sex evolve?
or… how is sexual reproduction maintained in the
face of so many alternative strategies?
3. Haplodiploidy
• haploid males develop from unfertilized
eggs,diploid females from fertilized eggs.
Examples: ants, bees, wasps
4. Pseudogamy (Gynogenesis)
• contact with sperm stimulates development from
unfertilized eggs.
Example: some nematodes and freshwater fishes
Amazon molly (Poecilia formosa)
But… of the world’s ~2 million named
species less than ~2,000 are totally
asexual…
But… of the world’s ~2 million named
species less than ~2,000 are totally
asexual…
… and they don’t appear to persist very long
Asexual species are typically found at the
tips of phylogenetic trees
Asexual species are typically found at the
tips of phylogenetic trees
S
A S
S S A S
A S
S
S = sexual species
A = asexual species
The exception: bdelloid rotifers – no sex for
40 million years!
The “costs” of sex
The “costs” of sex
1. The cost of producing males (or, the “two-fold
cost of sex”).
The “costs” of sex
1. The cost of producing males (the “two-fold
cost of sex”).
The “costs” of sex
1. The cost of producing males (the “two-fold
cost of sex”).
The “costs” of sex
1. The cost of producing males (the “two-fold
cost of sex”).
The “costs” of sex
2. The cost of finding mates
The “costs” of sex
2. The cost of finding mates
• exacerbated by low population density.
The “costs” of sex
2. The cost of finding mates
• exacerbated by low population density.
3. The costs of mating
The “costs” of sex
2. The cost of finding mates
• exacerbated by low population density.
3. The costs of mating
• mating is a risky business!
The “costs” of sex
2. The cost of finding mates
• exacerbated by low population density.
3. The costs of mating
• mating is a risky business!
• also vulnerable to sexually transmitted diseases.
The “costs” of sex
2. The cost of finding mates
• exacerbated by low population density.
3. The costs of mating
• mating is a risky business!
• also vulnerable to sexually transmitted diseases.
4. The cost of recombination
The “costs” of sex
2. The cost of finding mates
• exacerbated by low population density.
3. The costs of mating
• mating is a risky business!
• also vulnerable to sexually transmitted diseases.
4. The cost of recombination
• recombination creates superb combinations of
genes then quickly breaks them apart.
Why then does sexual reproduction
persist?
Why then does sexual reproduction
persist?
1. Adaptive evolution is enhanced
Why then does sexual reproduction
persist?
1. Adaptive evolution is enhanced
• in asexual species, advantageous mutations must occur in
the same lineage:
Why then does sexual reproduction
persist?
1. Adaptive evolution is enhanced
• in asexual species, advantageous mutations must occur in
the same lineage:
advantageous mutation

Abcd         Abcd’        

                Ab’cd’  

advantageous mutation
Why then does sexual reproduction
persist?
1. Adaptive evolution is enhanced
• in asexual species, advantageous mutations must occur in
the same lineage.
• in sexual populations, advantageous mutations can be
combined across lineages (through meiosis and syngamy).
Why then does sexual reproduction
persist?
1. Adaptive evolution is enhanced
• in sexual populations, advantageous mutations can be
combined across lineages (through meiosis and syngamy):
advantageous mutation

Abcd    Abc’d
 Abc’d’  
x
Abcd’   Abcd’

advantageous mutation
Why then does sexual reproduction
persist?
2. The Red Queen hypothesis
Why then does sexual reproduction
persist?
2. The Red Queen hypothesis
• originally proposed by Leigh Van Valen in 1973.
Why then does sexual reproduction
persist?
2. The Red Queen hypothesis
Why then does sexual reproduction
persist?
2. The Red Queen hypothesis
• originally proposed by Van Valen in 1973.
• species must continuously “run” (evolve) to track changing
environments.
Why then does sexual reproduction
persist?
2. The Red Queen hypothesis
• originally proposed by Van Valen in 1973.
• species must continuously “run” (evolve) to track changing
environments.
• if species fail to adapt, they may go extinct.
Why then does sexual reproduction
persist?
2. The Red Queen hypothesis
• originally proposed by Van Valen in 1973.
• species must continuously “run” (evolve) to track changing
environments.
• if species fail to adapt, they may go extinct
• sexual reproduction facilitates this process.
The Red Queen process is an
evolutionary arms race
The Red Queen process is an
evolutionary arms race
Target species
“Enemies”
(parasites, predators, competitors)
The Red Queen process is an
evolutionary arms race
Target species
Adaptation

“Enemies”
(parasites, predators, competitors)
The Red Queen process is an
evolutionary arms race

Target species
Counteradaptation
Adaptation

“Enemies”
(parasites, predators, competitors)
Muller’s ratchet
Hermann Muller (1890 – 1967)
A simple ratchet
pawl

crank 
pawl 
Muller’s ratchet


 

Mutation


Muller’s ratchet
• deleterious mutations occur in
asexual lineages…


 

Mutation


Muller’s ratchet
• deleterious mutations occur in
asexual lineages…
• … causing the least mutated class to
dwindle…



 

Mutation


Muller’s ratchet
• deleterious mutations occur in
asexual lineages…
• … causing the least mutated class to
dwindle…


 



• … and be lost by random drift

Mutation

?


Mutation



Muller’s ratchet
• deleterious mutations occur in
asexual lineages…
• … causing the least mutated class to
dwindle…
• … and be lost by random drift
• now the ratchet has “clicked” forward
once.


 

Mutation




?


Mutation



Muller’s ratchet
• deleterious mutations occur in
asexual lineages…
• … causing the least mutated class to
dwindle…
• … and be lost by random drift


 

Mutation




?


Mutation



• now the ratchet has “clicked” forward
once.

• now the ratchet has “clicked” forward
again.
? ?



Mutation

Muller’s ratchet
Asexual populations can only evolve towards ever
greater loads of deleterious mutations!
Muller’s ratchet
Asexual populations can only evolve towards ever
greater loads of deleterious mutations!
Does Muller’s ratchet occur in sexual populations?
Muller’s ratchet
Asexual populations can only evolve towards ever
greater loads of deleterious mutations!
Does Muller’s ratchet occur in sexual populations?
NO! Sex breaks the ratchet.
Muller’s ratchet
Asexual populations can only evolve towards ever
greater loads of deleterious mutations!
Does Muller’s ratchet occur in sexual populations?
NO! Sex breaks the ratchet.
How? By reconstituting the least mutated classes (by
recombination).
Muller’s ratchet
Asexual populations can only evolve towards ever
greater loads of deleterious mutations!
Does Muller’s ratchet occur in sexual populations?
NO! Sex breaks the ratchet.
How? By reconstituting the least mutated classes (by
recombination).
SEX IS RECOMBINATION!
Q: So why are asexual species at the tips of
phylogenetic trees?
S
A S
S S A S
A S
S
S = sexual species
A = asexual species
Q: So why are asexual species at the tips of
phylogenetic trees?
A: Because the short-term benefit of asexual
reproduction is countered by the long-term
advantage of sex.
S
A S
S S A S
A S
S
S = sexual species
A = asexual species