Download Monkeyflowers (Mimulus) as a model for evolutionary genetics

The origin of species
• Are species real biological entities, or
are they just a consequence of human
attempts to find order in the natural
world?
• How are species defined?
• How are new species formed?
• Does macroevolution follow a different
set of rules than microevolution?
Are species real?
“… the living world is not a
formless mass of
randomly combining
genes and traits, but a
great array of … gene
combinations, which are
clustered on a large but
finite number of adaptive
peaks.” – Theodosius
Dobzhansky
Speciation
Biological species concept
• “Groups of actually or potentially
interbreeding populations reproductively
isolated from all other such groups.”
– Ernst Mayr
“When we understand the origin of
reproductive isolation, we understand
the origin of species.” – Jerry Coyne
Reproductive isolation
Pre-mating barriers to gene flow
•
•
•
•
•
Geographic
Ecological
Phenological
Behavioral
Mechanical
Post-mating barriers to gene flow
•
•
•
•
•
Gamete incompatibility
Sperm competition
Hybrid inviability
Hybrid sterility
Hybrid breakdown
Jordan’s law
“Given any species in any
region, the nearest related
species is not likely to be
found in the same region nor
in a remote region, but in a
neighboring district separated
from the first by a barrier of
some sort.” -- David Starr
Jordan (1905) Science 22: 545562.
The origin of reproductive isolation
by ecogeography
“... not a single
geographic race is
known that is not also
an ecological race; nor
is there an ecological
race that is not at the
same time at least a
microgeographic race.”
-- Ernst Mayr (1963)
Animal Species and
Evolution
The Jordan/Mayr pie diagram for mechanisms
producing reproductive isolation
Premating barriers
in sympatry
Ecogeographic
Post-mating
barriers in
sympatry
The speciation engine is
powered primarily by
divergent adaptive evolution
Why use plant systems to study the
genetic architecture of adaptation?
Sessile
• Common garden/reciprocal transplant in natural
habitat
Prolific
• Thousands of progeny per cross
• Easily replicated as clones or inbred lines
Agent of natural selection often obvious
• Elevation, soil chemistry, water availability
Photogenic
Good enough for Mendel
Bumblebee-pollinated
Pink
Wide corolla opening
Inserted stigma/anther
1-2ml nectar
Mid-high elevation
Hummingbird-pollinated
Red
Narrow, tubular corolla
Exserted stigma/anther
40-100ml nectar
Low-mid elevation
Components of reproductive isolation
between M. lewisii and M. cardinalis
Pollinator
40.3%
Post-mating
0.9%
Geography and ecology
58.8%
Ramsey, J., Bradshaw, H.D., Jr., & Schemske, D.W.
(2003) Evolution 57: 1520-1534.
Mimulus section
Erythranthe (7-8 spp.)
51
M cardinalis CA 04
M cardinalis CA 11
M cardinalis Mx 13
M cardinalis CA 14
80
M cardinalis CA 05
60
M cardinalis CA 06
M cardinalis CA 07
M cardinalis CA 15
M cardinalis CA 10
M cardinalis CA 09
M lewisii WA 1
85
93
M lewisii WA 3
M lewisii OR 4 1
89
M lewisii OR 4 2
100
78
M lewisii MT 6
M lewisii OR 5
100
M lewisii N CA 7 1
M lewisii N CA 7 2
66M lewisii N CA 8
M lewisii CA 1 1
M lewisii CA 1 2
M lewisii CA 3
M lewisii CA 4
M lewisii CA 5 1
78 69
M lewisii CA 5 3
M lewisii CA 5 2
100
M lewisii CA 2
M lewisii CA 6
M lewisii CA 7
M lewisii WA 2
97
M eastwoodiae CO 2
95
M eastwoodiae UT 4
M eastwoodiae UT 3
77
M verbenaceus AZ 2
94
M verbenaceus UT 3
M verbenaceus UT 4
M nelsonii Mx 1
M rupestris Mx 1
72
M parishii CA 2
96
M parishii CA 5
M parishii CA 3
M parishii CA 6
M bicolor CA 2
M filicaulis CA 2
60
100
M cardinalis OR 01
M cardinalis CA 02
M cardinalis CA 03
cardinalis
lewisii
Rockies;
Cascades
69
lewisii
Sierra Nevada
64
58
99
97
79
87
100
76
0.01 changes
Paul Beardsley
Neighbor-joining
478 AFLPs
White Wolf
2200m
Mather
1400m
lewisii
1200-3100m
Jamestown
450m
cardinalis
30-1400m
Timberline
3050m
Relative Fitness of Parents and Hybrids
Relative fitness
Jamestown
(lo = cardinalis habitat)
White Wolf
(hi = lewisii habitat)
1.0
1.0
0.8
0.8
0.6
0.6
0.4
0.4
0.2
0.2
0.0
0.0
cardinalis F3
lewisii
cardinalis F3
lewisii
F2 progeny
Genotype LL
Genotype LC
Genotype CC
1
Locus 1
2
3
4
Locus 2
5
Nectar volume
What does a QTL mapping experiment
tell us about an adaptive trait?
•
•
•
•
Number of loci
Genetic map position of each QTL
Magnitude of effect (‘major’ or ‘minor’)
Mode of action (dominant, recessive,
additive, epistatic)
What a QTL mapping experiment does
not tell us:
• Gene identity
Components of reproductive isolation
between M. lewisii and M. cardinalis
QTL5
QTL4
Pollinator
40.3%
QTL6
QTL7
QTL3
Post-mating
0.9%
Geography and ecology
58.8%
QTL2
QTL1
Ramsey, J., Bradshaw, H.D., Jr., & Schemske, D.W.
(2003) Evolution 57: 1520-1534.
Genetic marker (RFLP) data
C
L
H
Relative fitness of F3 genotypes at
JamestownMgSTS46 White Wolf
Relative fitness
(lo = cardinalis habitat)
(hi = lewisii habitat)
1.0
1.0
0.8
0.8
0.6
0.6
0.4
0.4
0.2
0.2
0.0
0.0
CC
CL
LL
Genotype
CC
CL
LL
Genotype
Conclusions
• Differential adaptation is responsible
for most of the reproductive isolation
between M. lewisii and M. cardinalis
(and, according to Jordan’s rule, most
other pairs of sister taxa)
• A single locus, mapped by genomewide scans for Dp in large segregating
populations experiencing natural
selection, determines most of this
differential adaptation
Major QTLs in Mimulus
Trait
Linkage
group
PVE
Mode of
action
Carotenoids (yellow)
DC
83%
L>C
Anthocyanins (red/purple)
DC
21%
L>C
Petal width
EL
42%
L>C
Corolla width
AL
32%
L>C
Corolla projected area
CC
41%
C>L
Petal reflexing
AL
69%
L>C
Nectar volume
B
33%
add
Stamen length
AL
47%
add
Pistil length
EL
50%
add
YUP
Mimulus map
Can a single QTL have a large effect
on pollinator choice in sympatry?
Near-isogenic lines (NILs)
lewisii
F1
F2
NIL1
cardinalis
xL
xL
xL
yup
YUP
yup
YUP
N=1090
N=201
Bumblebees
Hummingbirds
Bradshaw & Schemske (2003) Nature 426: 176-178.
Components of reproductive isolation
between M. lewisii and M. cardinalis
QTL5 = YUP
QTL4
Pollinator
40.3%
QTL6
QTL7
QTL3
Post-mating
0.9%
QTL2
Geography and ecology
58.8%
QTL1 = EL SALTO
Ramsey, J., Bradshaw, H.D., Jr., & Schemske, D.W.
(2003) Evolution 57: 1520-1534.
Bumblevision
Future directions
• Which environmental factors are the
agents of natural selection?
• What are the underlying physiological
mechanisms of adaptation to high and low
elevation?
• Are major QTLs composed of single
genes, or multiple linked genes?
• Which gene(s) is(are) responsible for
reproductive isolation in allopatry and in
sympatry?