Speciation Genes

1
Speciation Genes
April 17, 2008
What sorts of genes promote reproductive
isolation? How do we find and characterize them
? How many changes does it take to make a new
species?
2
Darwins problem
LONG before having arrived at this part of my
work, a crowd of difficulties will have occurred
to the reader. Some of them are so grave that to
this day I can never reflect on them without
being staggered how can we account for species,
when crossed, being sterile and producing sterile
offspring, whereas, when varieties are crossed,
their fertility is unimpaired?
The Origin of Species (1859)
3
Chromosomal Speciation

• Inversion heterozygotes often have reduced
  fitness (meiosis malfunction -- fewer viable
  gametes)
  
• Many species pairs have fixed inversion
  differences, which cause hybrid problems
  
• But how does a new inversion mutation spread???

4
Is single-gene speciation possible?
Ueshima Asami 2003
5
The problem What happens to the first
opposite-coiled individual??
aa
aa
Aa
aa
aa
aa
aa
aa
aa
Ueshima Asami 2003
6
The solution Maternal effects!

• Small (subdivided) populations would help a rare
  allele drift to high frequencies
  
• Imagine that offsprings phenotype is determined
  by mothers genotype (not by its own genotype!)
  
• The mutant allele is recessive and drifts to
  moderate frequency in heterozygous form

7
The solution Maternal effects!
Aa
AA
¼ aa
Aa
AA
STILL right- handed!
Aa
AA
AA
AA
AA
Aa
AA
AA
Aa
AA
AA
Right-handed
8
The solution Maternal effects!
Aa
AA
Aa
AA
aa
aa
Aa
Aa
AA
AA
LEFT-handed!
AA
aa
AA
Aa
aa
AA
aa
aa
aa
Aa
AA
LEFT-handed!
AA
Right-handed
9
Dobzhansky-Muller Incompatibilities
Bateson (1909), Dobzhansky (1936, 1937), Muller
(1942)
3 criteria of D-Ms
10
Incompatibility alleles can be dominant
Ancestor
aa bb
Species 1
Species 2
AA bb
aa BB
Hybrid
Aa bB
x
x
11
or recessive!
Ancestor
AA BB
Species 1
Species 2
aa BB
AA bb
Hybrid
aA Bb
12
Recessive D-Ms act in the F2
Aa Bb x Aa Bb
F1 hybrid
3 B _
3 A _
F2s
1 bb
1
3 B _
1 aa
1 bb
13

• Theory predicts that interacting gene pairs
  should cause reproductive isolation between
  species.
  
• How can we test that?

• Find the genetic basis of reproductive
  isolation!
  
• Crosses Look for problems in the F1, or in a
  fraction of the F2s
  
• Map these problems Do they involve pairs of
  interacting loci?

14
Xiphophorus Hybrid lethality with a simple
genetic basis
Platyfish Swordtail
xiphophorus.org
15
Xiphophorus Hybrid lethality with a simple
genetic basis
Backcross
xiphophorus.org
16
The genetic basis of spots (T)
Backcross
xiphophorus.org
17
The Tumor locus interacts w/ a Repressor
locus
t/t r/r
T/T R/R
1/4 1/4 1/4 1/4
x
x
xiphophorus.org
18

• Is the Xiphophorus incompatibility dominant or
  recessive?
  
• Does it cause complete reproductive isolation?
• Does it reduce gene flow?
• What would the reciprocal backcross (to X.
  maculatus) look like?
  
• What was the ancestral genotype, according to the
  D-M model?

19
Many D-M incompatibilities are known to exist
Drosophila Cabot et al (1994) Two D. sechellia
loci, when introgressed together into a D.
simulans genome, cause hybrid male sterility.
Ting et al (1998) A D. mauritiana allele causes
hybrid male sterility in a D. simulans genomic
background. Monkeyflowers (Mimulus) Sweigart
et al (2006) 2 loci interact to cause hybrid
male sterility in a M. nasutus x M. guttatus
cross. Arabidopsis Bomblies et al (2007) Mul
tiple pairs of loci from different populations of
A. thaliana can interact to cause hybrid death.
20
But only one complete D-M pair has ever been
cloned!
D. melanogaster D. simulans
Two loci Hmr Lhr
21
What is the genetic basis of this incompatibility?
Cross 2 sim ? x mel ? Daughters Fine Sons
Dead
22
What is the genetic basis of this incompatibility?
Cross 1 sim ? x mel ? XAXA BB x __Y
____
Cross 2 sim ? x mel ?
XAY BB x ____ ____
23
Part II Prezygotic Speciation Genes
24
Genes for plant mating behavior in Mimulus
M. lewisii F1 hybrid M. cardinalis
Schemske Bradshaw 1999
25
Hybrid F2s recombine parental shape, color, and
nectar traits
QTL mapping identifies genomic regions associated
with these phenotypes
26
Yellow pigment and nectar volume Genotype at 1
locus affects pollinator preference
27
(No Transcript)
28
Reinforcement
Definition The enhancement of prezygotic isolat
ion, in sympatry, by natural selection
29
Reinforcement

• Heres how it happens
• Hybrids are unfit (postzygotic isolation)
• Individuals that dont hybridize have higher
  fitness
  
• Selection favors mechanisms that reduce or
  prevent hybridization (prezygotic isolation)

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History of Reinforcement Research

• 1930s - 1970s
• Dobzhansky (1937) proposes the idea.
• Rampant enthusiasm for reinforcement!!
• 1980s
• Theoretical models show that reinforcement may be
  very difficult to achieve.
  
• Rampant rejection of reinforcement!!
• 1990s - today
• Actual data collected from actual populations!!
• Refined theory and modeling

31
Two major questions

• Can reinforcement happen?
• Theoretical models
• Experimental evolution
• Does reinforcement happen?
• Survey natural systems
• What patterns should you see, if reinforcement
  occurred?

32
Experimental tests of reinforcement

33
Destroy-the-hybrid Strong selection against
hybridization
Parents
Offspring

Start of experiment No isolation between red-
and blue-marked individuals
34
Destroy-the-hybrid Strong selection against
hybridization
Parents
Offspring

Question After many generations of intense
selection, do red- and blue-marked individuals
mate less frequently than they used to?
35

• Answer Sometimes, yes.
• Koopman (1950) Drosophila
• Generation 1 Up to 50 of crosses
  hybridization
  
• Generation 6
• Paterniani (1969) Zea (corn)
• Generation 1 35-45 hybridization
• Generation 6 3-5 hybridization
• But This scenario invokes a hybrid fitness of 0
  (speciation is already complete!)
  
• When hybrid fitness is 0, reinforcement rarely
  evolves.

36
Reinforcement in natural populations
What patterns should we see in a species pair
affected by reinforcement?
A
A
S
Ranges Species 1 Species 2
37
Many species pairs show stronger reproductive
isolation in sympatry than in allopatry
Hawaiian crickets Otte (1989)
Abalone Lee et al (1995) Mussels Springer a
nd Crespi (2004) Toads Pfennig (2000) Stick
leback fish Rundle Schluter (1998)
Gilia plants Grant (1966) Drosophila Many,
many studies
Otte 1989
pond.dnr.cornell.edu
photobucket.com
38
Spadefoot toads Reinforcement observed over 27
years!
39
Evidence for reinforcement in many Drosophila
species pairs
40
Answers to Xiphophorus questions

• What would the reciprocal backcross (to X.
  maculatus) look like?
  
• T/t R/r x T/T R/R -- All progeny are T_ R_
  , so there are no hybrid problems in this
  direction of the cross!
  
• What was the ancestral genotype, according to the
  D-M model?
  
• The alleles that interact badly are T and r.
  Under a typical D-M scenario, those are derived
  and the ancestor was tt RR. One population then
  fixed a T and the other fixed an r. But
  In this case, it may be more biologically
  realistic to envision a tt rr ancestor, with X.
  maculatus fixing a T by drift and then an R
  by selection. How could you use a phylogeny to
  decide between these hypotheses?