Mimulus as a model for speciation
• Long history of ecological genetic studies
• Small genome (comparable to rice)
• Short generation time (~2 months)
• Easy to cultivate
• Highly speciose genus
• Diversity in mating system, floral form and habitat

Frontiers in Biological Research:
Integrated Ecological and Genomic
Analysis of Speciation in Mimulus
Michigan State Univ.
Doug Schemske
Univ. of Washington
Toby Bradshaw
Duke Univ.
John Willis
Univ. of Montana
Lila Fishman
Andrea Sweigart
Andrea Case
Fred Dietrich
CUGI
Jeffery Tomkins
UNC Chapel Hill
Todd Vision

Selfing has evolved several times in the Mimulus guttatus complex
Mimulus guttatus
Mimulus platycalyx Mimulus laciniatus Mimulus nasutus

Reproductive isolation between
M. guttatus and M. nasutus
• Largely allopatric
• Sympatry in some ephemeral habitats
• Natural hybrids are observed in the field
M. guttatus
M. guttatus + M. nasutus
M. guttatus M. nasutus

Isolating mechanisms
• Premating barriers
– Microhabitat
– Flowering time
– Cleistogamy
– Pollen tube competition
• Postmating barriers
– Partial male and female sterility of F1 and F2 hybrids

Quantitative trait loci (QTL)
P1 (+) P2 (-)
F1 (0)
F2
LOD
0
-
+
+

M. guttatus x nasutus map
• 600 F2 plants
• 174 markers over 1780 cM
• ~85% coverage
• 14 linkage groups
Fishman, Kelly and Willis (2002) Evolution 56, 2138-2155.

QTL for species differentiation
• Prezygotic isolation
– Many minor QTL underly floral morphological differences
• Postzygotic isolation
– Hybrid sterility due to two interacting nuclear loci
– Cytonuclear incompatibility
– Meiotic drive

Dobzhansky-Muller loci and hybrid sterility/inviability
AABB aaBB AAbb

DM factors in M. guttatus x nasutus?
G N
+
G
F1
Bg F2 Bn
Male sterile: 0 3/16 1/4
N

Model: sterility requires aaB- genotype
Genotype
AABB
AABb
AAbb
AaBB
AaBb
Aabb aaBB aaBb aabb
0
0
0
0
0
0
0
1
F1
0
F2 Bg
1/16 1/4
2/16 1/4
1/16 0
2/16 1/4
4/16 1/4
2/16 0
1/16 0
2/16 0
1/16 0
Total Steriles 0 3/16 0
* Using male steriles as dams
1/4
0
0
1/4
1/4
Bn
0
0
0
1/4
0
0
0
1/2
1/2
0
0
0
ABn* Male_sterile
0 no no no no no no yes yes no
1/4 1/2

Fine mapping the A locus
• Analysis of linkage to A in aaBB x AaBB
• ~1000 plants screened with markers from all over the genome
• Mapped to a ~15 cM interval
MgSTS45 MgSTS11
A
MgSTS104

Fine mapping the B locus
• Analysis of linkage to B in aaBb x aabb
• 2900 plants screened with markers from all over genome
• Only 4 recombinants with MgSTS28
– If region is typical, this implies ~30 kb distance
0.14 cM 0.7 cM
B
MgSTS28 MgSTS606

What happens in the opposite cross?
G
+
N
F1
Male sterile:
F2
1/4

Cytoplasmic male sterility
• Common in hermaphroditic plants and animals
• The mechanism is typically a mitochondrial fusion protein
• Evolutionary dynamics
– Maternally transmitted organelles that increase female fitness at the expense of male fitness spread rapidly
– Nuclear restorers arise that suppress CMS
– CMS can be uncovered when wide crosses separate CMS cytoplasm from its restorer

Evolutionary dynamics of
CMS
+
CMS
+ +
+
F2
CMS
+
CMS
+
R

Isolating CMS factors
• Model: M. guttatus has male sterilizing cytoplasm and a dominant restorer (R)
• Restorer being mapped in Rr x rr
– On linkage group 4, 20 cM from MgSTS34
• Mitochondrial factor being isolated by looking for fusion proteins

Segregation distortion
• In F2, 50% of alleles should be from each parent
• Eleven regions of severe segregation distortion in guttatus x nasutus cross
– Nine in favor of guttatus
• Occurs during gamete formation in females

Female gametogenesis in angiosperms
• Only one of the four meiotic products leads to an egg
• Potential for conflict between alleles

Evolutionary dynamics of meiotic drive
• Distorter locus spreads due to its transmission advantage
– Linked suppressor locus can arise to prevent drive against itself
• Once both are fixed, the system is quiescent until revealed by a wide cross
• May contribute to pericentromeric heterochromatin tracts in mammals, plants
• Question: do distorters map to centromeres in guttatus ?

Are speciation genes fixed by genetic drift or natural selection?
x B y
Neutrality
Population bottleneck
Selection

Some closing thoughts
• Genomic conflicts should be stronger in outcrossers than selfers
– CMS in guttatus
– Meiotic drive in guttatus
• Genetic incompatibilities may be accelerated by a shift in mating system
• Not something that can be studied in
Drosophila , the predominant model for the genetics of speciation