1. 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?

2. 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

3. Biological species concept
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

4. 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

5. 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:

6. 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

7. The Jordan/Mayr pie diagram for mechanisms producing reproductive isolation
Premating barriers in sympatry
Post-mating barriers in sympatry
Ecogeographic
The speciation engine is powered primarily by divergent adaptive evolution

8. 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

9. Bumblebee-pollinated
Hummingbird-pollinated
Pink
Red
Wide corolla opening
Narrow, tubular corolla
Inserted stigma/anther
Exserted stigma/anther
1-2ml nectar
40-100ml nectar
Mid-high elevation
Low-mid elevation

10. Components of reproductive isolation between M. lewisii and M
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:

11. Mimulus section Erythranthe (7-8 spp.)51
M cardinalis OR 01
M cardinalis CA 02
M cardinalis CA 03
M cardinalis CA 04
cardinalis 60
M cardinalis CA 11
M cardinalis Mx 13
M cardinalis CA 14 80 60
M cardinalis CA 05
100
M cardinalis CA 06
M cardinalis CA 07
M cardinalis CA 15
M cardinalis CA 10
M cardinalis CA 09 85 93
M lewisii WA 1
lewisii
Rockies; Cascades
M lewisii WA 3 89
M lewisii OR 4 1
100 78
M lewisii OR 4 2 69
M lewisii MT 6
M lewisii OR 5
100
M lewisii N CA 7 1
M lewisii N CA 7 2 66
M lewisii N CA 8
M lewisii CA 1 1
M lewisii CA 1 2
lewisii
Sierra Nevada
M lewisii CA 3
M lewisii CA 4 78 69
M lewisii CA 5 1 58 64
M lewisii CA 5 3
100
M lewisii CA 5 2
M lewisii CA 2
M lewisii CA 6
M lewisii CA 7
M lewisii WA 2 97 95
M eastwoodiae CO 2 97
M eastwoodiae UT 4 99 77
M eastwoodiae UT 3 94
M verbenaceus AZ 2 79
M verbenaceus UT 3
M verbenaceus UT 4 87
M nelsonii Mx 1
M rupestris Mx 1 72
M parishii CA 2
100 96
M parishii CA 5
M parishii CA 3
Paul Beardsley
Neighbor-joining
478 AFLPs
M parishii CA 6 76
M bicolor CA 2
M filicaulis CA 2
0.01 changes

13. Timberline 3050m White Wolf 2200m Mather 1400m Jamestown lewisii 450m
cardinalis m

14. (lo = cardinalis habitat)
Relative Fitness of Parents and Hybrids
Jamestown
(lo = cardinalis habitat)
White Wolf
(hi = lewisii habitat)
1.0
1.0
0.8
0.8
0.6
0.6
Relative fitness
0.4
0.4
0.2
0.2
0.0
0.0
cardinalis F3
lewisii
cardinalis F3
lewisii

16. F2 progeny Locus 1 Locus 2 Nectar volume Genotype LL Genotype LC
Genotype CC 1
Locus 1 2 3 4
Locus 2 5
Nectar volume

17. 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

18. Components of reproductive isolation between M. lewisii and M
Components of reproductive isolation between M. lewisii and M. cardinalis
QTL5
Pollinator
40.3%
QTL6
QTL4
QTL7
Post-mating
0.9%
QTL3
Geography and ecology
58.8%
QTL2
QTL1
Ramsey, J., Bradshaw, H.D., Jr., & Schemske, D.W. (2003) Evolution 57:

20. Genetic marker (RFLP) dataH

21. (lo = cardinalis habitat)
Relative fitness of F3 genotypes at MgSTS46
Jamestown
(lo = cardinalis habitat)
White Wolf
(hi = lewisii habitat)
1.0
1.0
0.8
0.8
0.6
0.6
Relative fitness
0.4
0.4
0.2
0.2
0.0
0.0 CC CL LL CC CL LL
Genotype
Genotype

22. 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 genome-wide scans for Dp in large segregating populations experiencing natural selection, determines most of this differential adaptation

24. Major QTLs in Mimulus Trait Linkage group PVE Mode of action
Carotenoids (yellow) DC
83%
L > C
Anthocyanins (red/purple)
21%
Petal width EL
42%
Corolla width AL
32%
Corolla projected area CC
41%
C > L
Petal reflexing
69%
Nectar volume B
33%
add
Stamen length
47%
Pistil length
50%

26. YUP
Mimulus map
Can a single QTL have a large effect on pollinator choice in sympatry?

27. Near-isogenic lines (NILs)
lewisii F1 F2
NIL1
cardinalis xL xL xL

28. Bumblebees Hummingbirds N=1090 N=201
Bradshaw & Schemske (2003) Nature 426:

29. Components of reproductive isolation between M. lewisii and M
Components of reproductive isolation between M. lewisii and M. cardinalis
QTL5 = YUP
Pollinator
40.3%
QTL6
QTL4
QTL7
Post-mating
0.9%
QTL3
QTL2
Geography and ecology
58.8%
QTL1 = EL SALTO
Ramsey, J., Bradshaw, H.D., Jr., & Schemske, D.W. (2003) Evolution 57:

30. Bumblevision

31. 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?