1. 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 19 th 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

2. Hybrid Speciation

3. Kinds of Hybrid Speciation Homoploid Hybrid Speciation Rare Reproductive isolation difficult to achieve 2x X Polyploid Hybrid Speciation (Allopolyploidy) Common Reproductive isolation byproduct of genome doubling 2x 4x X reproductive isolation

4. 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

5. Recombinational Model New homokaryotype confers partial isolation with parentals

6. 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, 441–451 0.1 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 proportion of replicates ecological selection fertility of F1 hybrid Hybrid speciation AlexBuerkle Hybrid Speciation Model (open habitat available for hybrids)

7. Decay of genetic distance (Gst) between hybrid species and one of its parental species Ecological Selection

8. Hybrid speciation Frequency 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 Ecological Selection Stable Hybrid Zone Adaptive Introgression Hybrid Speciation Buerkle et al. (2003) AlexBuerkle

9. 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)

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

11. 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)

12. H. deserticola desert floor H x Helianthus annuus mesic soils H. petiolaris sandy soils H. anomalus sand 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.

13. 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

14. 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. deserticola desert floor H

15. EMPIRICAL EVIDENCE: KARYOTYPIC EVOLUTION Distribution of hybrid and parental Helianthus species

16. 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

18. Parents H. annuus x H. petiolaris: 8 translocations / 3 inversions collinear withcollinear with novel gene both parentsone parentorder H. anomalus: 6 linkages3 linkages 8 linkages H. deserticola:656 H. paradoxus:647 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 rearrangements 2/3 novel rearrangements Comparative Linkage Mapping - summary

19. 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

20. 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

21. H. deserticola desert floor H x Helianthus annuus mesic soils H. petiolaris sandy soils H. anomalus sand dune H. paradoxus salt marsh P P H H Field Experiments: Hybrid species favored in hybrid habitats Empirical Evidence: Ecological Divergence

22. 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

23. 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.