PLANT OF THE DAY!

•Tamarix (salt cedar)• 50-60 species •Family Tamaricaceae•native to dry areas of Eurasia and Africa.

•Introduced to North America as ornamental shrub in 19th century•Planted extensively during great depression to prevent soil erosion

•Second worst invasive species in USA•Colonizes riparian habitats, displacing native vegetation and consume precious water resources

•Most common invasive in USA is a hybrid of two species that do not grow in the same areas of Asia

Hybrid Speciation

Kinds of Hybrid Speciation

Homoploid Hybrid Speciation•Rare•Reproductive isolation difficult to achieve

2x 2x

2x

X

Polyploid Hybrid Speciation(Allopolyploidy)•Common•Reproductive isolation byproduct of genome doubling

2x 2x

4x

X

reproductive isolation

reproductive isolation

Model for Homoploid Hybrid Speciation

Interspecific hybridization

Fertility / viability selection

Stabilization of fertile & viable hybrid segregates

Reproductive isolation facilitated by karyotypic divergence (recombinational model) hybrid trait causes ecological divergence hybrid trait causes assortative mating spatial isolation

Recombinational Model

New homokaryotype confers partial isolation with parentals

Frequency of Hybrid Speciation (open habitat available for hybrids)

•Fertility controlled by two underdominant loci

•Ecological performance controlled by two loci with additive effects

•Three different habitats and ecological selection occurred at seedling stage

Heredity (2000) 84, 441–4510.1 0.3 0.5 0.7 0.9

0.1

0.3

0.5

0.7

0.9

0

0.1

0.2

0.3

0.4

0.5

prop

ortio

n of

rep

licat

es

ecological selection

fertilityof F1 hybrid

Hybrid speciation

Alex Buerkle

Hybrid Speciation Model (open habitat available for hybrids)

Decay of genetic distance (Gst) between hybrid species and one of its parental species

Eco

logi

cal S

elec

tion

Hybrid speciationFrequency of Hybrid Speciation (no open habitat available for hybrids)

0.9

0.7

0.5

0.3

0.1

0.1 0.3 0.5 0.7 0.9

F1 Hybrid Fertility

Ec

olo

gic

al S

ele

cti

on

Stable Hybrid Zone

Adaptive Introgression

Hybrid SpeciationBuerkle et al. (2003)

Alex Buerkle

CONDITIONS FAVORING HOMOPLOID HYBRID SPECIATION

•Little spatial isolation between parental species, but substantial isolation of hybrid species.

•Open habitat for hybrid species.

•Strong ecological selection favoring hybrid lineage in new habitat.

•Weak postzygotic isolation between parental species, but strong isolation of hybrid species.

•Hybrid trait causes assortative mating (not modeled)

EMPIRICAL EVIDENCE: SPATIAL ISOLATION(allopatric origin of oxford ragwort, Senecio squalidus (Abbott, 2000, 2002)

EMPIRICAL EVIDENCE: SPATIAL ISOLATION

Allopatric:Gila seminude (DeMarais et al., 1992)Paeonia sinjiangensis (Sang and Zhang, 1999)Senecio squalidus (Abbott et al., 2000)

Parapatric:Argyranthemum sundingii (Brochmann, 1987) Helianthus anomalus (Rieseberg, 1991)Helianthus deserticola (Rieseberg, 1991)Helianthus paradoxus (Rieseberg et al., 1990)Invasive sculpin (Nolte et al. 2005)Lycaeides butterflies (Gompert et al. 2006)Iris nelsonii (Arnold, 1993)Pinus densata (Song et al., 2003)Penstemon clevelandii (Wolfe et al., 1998)

Sympatric:Daphnia mendotae (Taylor et al., 1996)Lonicera fly (Schwartz et al., 2005)Pungu maclareni (Schliewen & Klee, 2004)Heliconius heurippa (Mavarez et al. 2006)

H. deserticoladesert floor

H

x

Helianthus annuusmesic soils

H. petiolaris sandy soils

H. anomalussand dune

H. paradoxus salt marsh

P

P

H

H

EMPIRICAL EVIDENCE: ECOLOGICAL ISOLATION

Reciprocal transplant experiments indicate that synthetic and natural hybrids favored in hybrid habitats.

TESTING THE IMPORTANCE OF ECOLOGY IN HYBRID SPECIATION

•Are the stabilized hybrid species ecologically divergent from their parents?

•Are the hybrid species favored in the hybrid habitats?

•Is there evidence of parallel hybrid speciation?

YES - for all but one species tested

YES - for Helianthus

YES - for Argyranthemum, Helianthus, Pinus

HYBRID TRAITS CAUSE ASSORTATIVE MATING

Helianthus deserticola (flowering time)Rieseberg 1991

Heliconius heurippa (wing pattern)Maverez et al. 2006

Iris nelsonii (flower color)Arnold 1993

Penstemon clevelandii (flower color)Wolf et al. 1998

Xiphorus clemenciae (swordtail)Meyer et al. 2006

H. deserticoladesert floor

H

EMPIRICAL EVIDENCE: KARYOTYPIC EVOLUTIONDistribution of hybrid and parental Helianthus species

H. deserticola

H. paradoxus

H. annuus

H. anomalus

H. petiolaris

1.6%

18.5%

2.2%

1.6%

1.5%

2.1%

0.18%

0.78%

0.96%

13.8%

Line thickness proportional to % seed set

Crossing relationships among hybrid and parental Helianthus species

annuus

deserticola

paradoxus

petiolaris

anomalus

LG2

LG2

LG2A

LG2B

LG2-8 LG2-8

Comparative mappingof linkage group 2In Helianthus

1152229

1282

925279

10657081011

423

1035

333

1152

333

332

1065249

1035

120

332229279

1011

984

1065

249

1028

377120

996

996

229

1147984

7083771035423E-12

103

16

328

1065

229

11471028925

671671423E-12103

16

328

Parents

H. annuus x H. petiolaris: 8 translocations / 3 inversions

collinear with collinear with novel gene both parents one parent order

H. anomalus: 6 linkages 3 linkages 8 linkagesH. deserticola: 6 5 6H. paradoxus: 6 4 7

24 of 29 new chromosomal changes in hybrid species associated with linkage groups already rearranged in parents (P = 0.009)

Hybrids

Origins of rearrangements

1/3 sorting of pre-existing rearrangements2/3 novel rearrangements

Comparative Linkage Mapping - summary

Conclusions - Homoploid Hybrid Speciation

•Generally good match between theory & empirical data

•spatial isolation of hybrid species predicted & 12/16 hybrid species parapatric or allopatric with parents

•Ecological divergence of hybrid species predicted & all but one hybrid species exhibit some degree of ecological divergence

•Karyotypic evolution predicted to contribute to reproductive independence of hybrid lineage & 6/14 hybrid species exhibit karyotypic divergence

•Hybrid traits frequently cause assortative mating

How does hybridization create novel or extreme phenotypes?

•Natural populations of organisms often contain cryptic variation that cannot be predicted from the phenotype of the population.•Cryptic variation is released in crosses through the expression of extreme or “transgressive” phenotypes

Mechanism = complementary gene action

H. deserticoladesert floor

H

x

Helianthus annuusmesic soils

H. petiolarissandy soils

H. anomalussand dune

H. paradoxus salt marsh

P

P

H

H

Field Experiments:

Hybrid species favored in hybrid habitats

Empirical Evidence: Ecological Divergence

Most extreme traits could be re-created in experimental hybrids

1% of experimental hybrids classified as H. anomalus

6.5% of experimental hybrids classified as H. deserticola

0.2% of experimental hybrids classified as H. paradoxus

Re-creating the birth of a new species in the greenhouse

Conclusions - Transgressive Segregation

• Crosses between genetically divergent populations frequently release cryptic phenotypic variation, referred to as transgressive variation

• Transgressive segregation may provide a means for large or difficult evolutionary transitions requiring simultaneous changes at multiple genes or traits.

• This possibility is illustrated by the ecological divergence of several sunflower species.

• Hybridization’s role in adaptation is probably under-estimated.