Lecture 12 Linkage disequilibrium and the evolution of sex
The Evolution of Sex
1. The cost of sex
Sexual species Asexual species
Female Female Male
AA AA BB
AA BB AA AA
AA BB AA AA AA AA The Evolution of Sex
2. Life without sex
Unisexual species
Poeciliopsis, Amazon mollies Unisexual species
Amazon mollies
Hybridogenetic Gynogenetic Parthenogenetic
AX BB AA BB AA
B B A AA AA
AB CC AA CC AA
C C A AA AA Unisexuals
Poeciliopsis
Rivulus marmoratus The Evolution of Sex
a. Simultaneous hermaphrodites b. Sequential hermaphrodites The Evolution of Sex
3. Hermaphrodites b. Sequential hermaphrodites
b1. Protogynous b2. Protandrous
Amphiprion, Semicossyphus pulcher Clownfish California sheephead 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 Female
2N 2N
Linkage disequilibrium and the evolution of sex
Q: What distinguishes sexual from asexual reproduction?
A: Meiosis and Syngamy
Male Female
2N 2N
Meiosis ↓ ↓
N N
Linkage disequilibrium and the evolution of sex
Q: What distinguishes sexual from asexual reproduction?
A: Meiosis and Syngamy
Male Female
2N 2N
Meiosis ↓ ↓
N N
Syngamy Ø ×
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 Gamete type (M) size (G)
+/- Small (S)/Large (L) A model for the evolution of two sexes
Mating Gamete type (M) size (G)
+/- Small (S)/Large (L)
Ü Linkage disequilibrium MG A model for the evolution of two sexes
Mating Gamete type (M) size (G)
+/- Small (S)/Large (L)
Ü Linkage disequilibrium MG
ß MG + S ♂ A model for the evolution of two sexes
Mating Gamete type (M) size (G)
+/- Small (S)/Large (L)
Ü Linkage disequilibrium MG
ß à MG MG + S - L ♂ ♀ MG MG + S - L ♂ ♀ MG MG + S - L ♂ ♀
Recombinants: MG MG + S - L ♂ ♀
Recombinants:
MG ↓ fitness due to + L low sperm number MG MG + S - L ♂ ♀
Recombinants:
MG ↓ fitness due to + L low sperm number
MG ↓ fitness due to - S inviable eggs MG MG + S - L ♂ ♀
Recombinants:
MG ↓ fitness due to + L low sperm number
MG ↓ fitness due to - S 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? Q: What causes linkage disequilibrium?
Q: What causes linkage disequilibrium?
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
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
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 at 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?
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 (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 Abcdª ª ª ª ª ª ª ª ª ªAbcd’ ª ª ª ª ª ª ª ª
ª ª ª ª ª ª ª ª ª ª ª ª ª ª ª ª ª ª ª ª ª ª ª
ª ª ª ª ª ª ª ª ª ª ª ª ª ª ª ª ªAb’cd’ ª ª 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 ª ª ª Abc’d
x ª Abc’d’ ª ª
Abcd’ ª ª ªAbcd’ 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
• 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
x “Enemies” (parasites, predators, competitors) The Red Queen process is an evolutionary arms race
Target species {
Counter- Adaptation adaptation
x “Enemies” (parasites, predators, competitors) Muller’s ratchet
Hermann Muller (1890 – 1967) A simple ratchet
pawl â crank à
pawl à
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