Re‐creating Ancient Hybrid Species’ Complex Phenotypes from Early‐Generation Synthetic Hybrids: Three Examples Using Wild Sunflowers

Abstract

Can the complex phenotypes that characterize naturally occurring hybrid species be re-created in early-generation artificial hybrids? We address this question with three homoploid hybrid species (Helianthus anomalus, Helianthus deserticola, Helianthus paradoxus) and their ancestral parents (Helianthus annuus, Helianthus petiolaris) that are phenotypically distinct and ecologically differentiated. These species, and two synthetic hybrid populations of the ancestral parents, were characterized for morphological, physiological, and life-history traits in greenhouse studies. Among the synthetic hybrids, discriminant analysis identified a few individuals with the multitrait phenotype of the natural hybrid species: 0.7%-1.1% were H. anomalus-like, 0.5%-13% were H. deserticolalike, and only 0.4% were H. paradoxus-like. These relative frequencies mirror previous findings that genetic correlations are favorable for generating the hybrid species' phenotypes, and they correspond well with phylogeographic evidence that demonstrates multiple natural origins of H. deserticola and H. anomalus but a single origin for H. paradoxus. Even though synthetic hybrids with hybrid species phenotypes are rare, their phenotypic correlation matrices share most of the same principal components (eigenvectors), setting the stage for predictable recovery of hybrid species' phenotypes from different hybrid populations. Our results demonstrate past hybridization could have generated hybrid species-like multitrait phenotypes suitable for persistence in their respective environments in just three generations after initial hybridization. Keywordshybridization; constraints; niche differentiation; adaptive evolution; speciation; Fleury hierarchy There are two contrasting mechanisms by which a new plant species can arise by hybridization (Grant 1981): allolyploid and homoploid hybrid speciation. Because hybridization must be initiated in sympatry, both forms of hybrid speciation require that reproductive barriers arise in the presence of gene flow. Allopolyploid speciation is straightforward because reproductive isolation is an instantaneous by-product of genome doubling. However, there is no assured means by which homoploid hybrid lineages become isolated from their parental species. Early authors (Stebbins 1957;Grant 1958;Templeton 1980) (McCarthy et al. 1995;Buerkle et al. 2000). Karyotypic divergence and spatial isolation are well documented in natural hybrid species (Gallez and Gottlieb 1982;Rieseberg 1991;Rieseberg et al. 1995;Hirai et al. 2000), and most hybrid species occupy habitats that are different or extreme compared with the parental species (Abbott 1992; Arnold 1997;Rieseberg 1997;Schwarzbach et al. 2001;Rosenthal et al. 2005).The simulation models above assume that habitat differentiation must occur early in the speciation process (Buerkle et al. 2000). Hybridization provides a plausible mechanism for rapid niche differentiation between the parental species and neohybrids. Recombinant hybrids are expected to have more phenotypi...

Molecular genetic and quantitative trait divergence associated with recent homoploid hybrid speciation: a study of Senecio squalidus (Asteraceae)

“…S. squalidus was also distinct from Sicilian hybrids on the basis of six QTs, including the three transgressive traits (Table 2). These findings are in accordance with observations of other homoploid hybrid species, such as H. anomalus and H. deserticola, which showed that the hybrid species were distinct from earlygeneration hybrids and exhibit particular QTs that are transgressive relative to their parents H. annuus and H. petiolaris (Schwarzbach et al, 2001;Rosenthal et al, 2002Rosenthal et al, , 2005. Transgressive QT expression can be spontaneously generated in new hybrids when QTLs with fixed but opposing directions of effects within species segregate in heterozygous hybrids and also by interaction of divergent gene expression mechanisms in hybrids (Rieseberg et al, 1999;Hegarty and Hiscock, 2008).…”

“…However, the population sampling approach of our study does not permit adequate partitioning of genetic and environmental contributions to quantitative variance, preventing Q st estimates that, validly, can be directly compared with molecular genetic estimates. Therefore, we chose instead to focus on multivariate analysis of QTs that have been successfully applied in other hybrid studies (for example, Brochmann et al, 2000;Rosenthal et al, 2002Rosenthal et al, , 2005.…”

Phenotypic selection on leaf water use efficiency and related ecophysiological traits for natural populations of desert sunflowers

“…The active dune habitat of H. anomalus has higher water availability and lower N than the adjacent stabilized dune habitats of H. deserticola (Rosenthal et al 2005a). Phenologically, H. anomalus generally Xowers and sets seed later than H. deserticola , Rosenthal et al 2005b. Previous comparisons of leaf ecophysiological traits in greenhouse studies and Weld experimental gardens have demonstrated that H. anomalus is always more succulent and tends to have larger leaves with lower N concentration, but that the species do not consistently diVer in WUE (Schwarzbach et al 2001;Rosenthal et al 2002;Rieseberg et al 2003;Brouillette et al 2006).…”

Reconstructing the History of Selection during Homoploid Hybrid Speciation

“…Because this type of speciation appears to occur rapidly (Ungerer et al 1998), it is sometimes possible to experimentally replicate the early stages of the hybrid speciation process. Comparison of experimental hybrid lineages with those that originated naturally has provided a powerful means for reconstructing the speciation process (Rieseberg et al 1996a;Lexer et al 2003;Gross et al 2004;Ludwig et al 2004;Gross and Rieseberg 2005;Hegarty and Hiscock 2005;Rosenthal et al 2005).Three of the best-investigated examples of homoploid hybrid species are annual sunflowers. Molecular evidence indicates that independent hybridization events between the annual sunflowers Helianthus annuus and Helianthus petiolaris, both widespread throughout North America, gave rise to three hybrid species, Helianthus anomalus, Helianthus deserticola, and Helianthus paradoxus (Rieseberg 1991), all with restricted geographical distributions in the southwestern United States.…”

“…Because this type of speciation appears to occur rapidly (Ungerer et al 1998), it is sometimes possible to experimentally replicate the early stages of the hybrid speciation process. Comparison of experimental hybrid lineages with those that originated naturally has provided a powerful means for reconstructing the speciation process (Rieseberg et al 1996a;Lexer et al 2003;Gross et al 2004;Ludwig et al 2004;Gross and Rieseberg 2005;Hegarty and Hiscock 2005;Rosenthal et al 2005).…”