The genetics of speciation - 1
The Dobzhansky-Muller model
Haldane's rule
SPECIATION / EVA KISDI / 2014 FALL / LECTURE 12
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Genetic incompatibilities
n
Allopatric speciation:
genetic differences accumulate
hybrids are inviable or sterile = intrinsic postzygotic isolation
n
Single gene speciation – very unlikely
AA
aa
left-right coiling of Lymnaea peregra;
chromosomal mutations!
W22
W11
aa
Aa = inferior hybrid
W12
W12
0
p
1
Assuming constant fitnesses, A cannot spread if Aa is inferior
(cf Wright model of natural selection)
SPECIATION / EVA KISDI / 2014 FALL / LECTURE 12
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Dobzhansky-Muller model
n
Dobzhansky-Muller model: between-locus incompatibilities
aaBB
AAbb
Aabb
aaBb
A is selected to work with b
B is selected to work with a
A and B are not tested together:
on average, they work less well
aabb
substitutions may be due to selection or genetic drift
SPECIATION / EVA KISDI / 2014 FALL / LECTURE 12
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Dobzhansky-Muller model
Holey adaptive landscapes (Gavrilets 1999, 2004)
aaBB
Aabb
aaBb
aa
AABB
aabb
aaBB
fitness
aabb
aa
aabb
bb
Bb
Aa
AA BB
fitness
AAbb
fitness
n
bb
Bb
Aa
AA BB
nearly neutral evolution
on fitness ridges
SPECIATION / EVA KISDI / 2014 FALL / LECTURE 12
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Dobzhansky-Muller model
n
Many loci evolve: the number of incompatibilities
“snowballs”
N substitutions in the two lineages:
d
D
C
0 + 1 + 2 + ... + (N-1) = (N-1)N/2
possible incompatibilities
c
b
B
a
A
aabbccdd
q
q
derived alleles are more often involved
asymmetry: the derived allele introgressed to
the alternative sp can have more incompatibilities
than the ancestral allele – empirically confirmed
SPECIATION / EVA KISDI / 2014 FALL / LECTURE 12
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Dobzhansky-Muller model
n
Genic incompatibility:
gene A1 of species 1 does not work well with gene B2 of species 2
dominant-dominant (H0) incompatibility:
A1_B2_ hybrids are affected, no homo/hemizygous locus required
(classic F1 autosomal inviability/sterility)
dominant-recessive (H1) incompatibility:
A1_B2B2 hybrids are affected (B2 acts recessively)
(F1 x sp2 backcross affected)
"hybrid breakdown"
(not in F1 but later)
recessive-recessive (H2) incompatibility:
only A1A1B2B2 hybrids are affected (some of F2)
SPECIATION / EVA KISDI / 2014 FALL / LECTURE 12
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Dobzhansky-Muller model
n
First incompatibility gene known: Xiphophorus hybrid melanoma
X. maculatus (platy, with spots) mother x X. helleri (swordtail) father
F1 strong black spots
F1 x X. helleri backcross: 50% no spots, 25% lethal melanoma
X. maculatus: Tu complex (dominant, X-linked) causes tumour
RR (dominant, autosomal) suppressor
X. helleri: no Tu, no suppressor
dominant-recessive incompatibility (Tu_rr is lethal)
SPECIATION / EVA KISDI / 2014 FALL / LECTURE 12
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Dobzhansky-Muller model
X. helleri
X. maculatus
++,rr
TuTu,RR
Tu+,RR
++,RR
++,Rr
Tu was never tested with r
++,rr
SPECIATION / EVA KISDI / 2014 FALL / LECTURE 12
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Genic incompatibilities
n
Mapping recessive-recessive incompatibilities:
D. simulans x melanogaster hybrid inviability genes (Presgraves 2003)
Df autosome with small deletion
Bal balancer (dominant marker + no recomb.)
(Lhr rescues from male hybrid inviability without Df)
Df male hybrids hemizygous for a bit of sim autosome
AND the mel X-chromosome
All Df hybrids die: recessive-dominant incompatibility between sim and mel OR
simply a recessive lethal on the sim chromosome – discard
Only Df males die: recessive-recessive incompatibility between sim autosome
and mel X-chromosome (all rescued when sim X is present)
SPECIATION / EVA KISDI / 2014 FALL / LECTURE 12
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Genic incompatibilities
20 recessive hybrid lethals + 3 nearly lethals (+ 17 semilethals) found
on the two major autosomes:
+ regions not covered by deletions + incompatibilities with chromosomes
other than X = ca 170 recessive-recessive incompatibilities
no dominant-dominant and only 22 dominant-recessive incompatibilities
(known from F1 and F1 x sp2 backcross)
SPECIATION / EVA KISDI / 2014 FALL / LECTURE 12
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Haldane's rule
n
When only one hybrid sex is intrinsically inviable or
sterile, then it is usually the heterogametic (XY, ZW) sex
one sex affected Haldane's rule
XY males
Drosophila
mammals
ZW females
Lepidoptera
birds
sterility
inviability
sterility
inviability
114
17
25
1
98 %
76 %
100 %
100 %
sterility
inviability
sterility
inviability
11
34
23
30
100 %
85 %
91 %
100 %
SPECIATION / EVA KISDI / 2014 FALL / LECTURE 12
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Haldane's rule
n
Haldane's rule seems to be a transitory state
Comparative analysis of Drosophila speciation (see lecture 4):
1 My
male inviability
and sterility
SPECIATION / EVA KISDI / 2014 FALL / LECTURE 12
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Haldane's rule
n
Dominance theory: dominant-recessive incompatibilities
explain Haldane's rule
dominant-dominant incompatibilities affect both sexes but are rare
recessive-recessive incompatibilities do not appear in F1
dominant autosomal - recessive X-linked incompatibilities appear
when X is hemizygous = in the heterogametic sex
dominant-recessive incompatibilities accumulate faster
than dominant-dominant incompatibilities
+ enhancement from "faster-X"?
favourable recessive mutations on X spread faster within a species
than recessive mutations on autosomes
= X diverges faster
has a disproportionally large effect
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