Thoughts about the relative importance of interspecific hybridization in plant evolution have switched back and forth over time. In the middle of the last century, the role of hybridization was considered to be substantial, based on a number of morphological studies of native and crop species (Anderson, 1949). In the 1970s, enthusiasm waned (Heiser, 1973), but with the advent of molecular markers in the 1980s support grew dramatically (Rieseberg, 1995; Rieseberg et al., 2000). Most plant systematists now believe that hybrid speciation is at least common, with estimates of the percentages of hybrid species in different floras ranging from 25% to 80% (Whitman et al., 1991; Abbott, 1992; Masterson, 1994). Ellstrand et al. (1996) found 16–34% of the families in five biosystematic floras to have at least one pair of species that hybridized locally, and 6–16% of the genera.
Hybridizations between native and introduced species have often led to the development of new taxa and have even been implicated in the evolution of a number of new invasive species. Abbott (1992) estimated that 45% of the British flora was alien, and 7% of those introduced species were involved in the production of hybrids now prominent in the native flora. One of the most widespread examples is Senecio vulgaris var. hibernicus, a hybrid of native S. vulgaris var. vulgaris and introduced Senecio squalidus, which escaped from the Oxford Botanical Garden in 1794 (Abbott, 1992). Highly invasive thistles from Europe have widely hybridized in Australia (O’Hanlon et al., 1999). Ellstrand and Schierenbeck (2000) found 28 examples ‘where invasiveness was preceded by hybridization’ and at least half of these hybrid lineages were the product of native non-native hybridizations.
As we have discussed previously in this chapter, many plant species retain the ability to hybridize with their relatives, even when they are quite distinct and have relatively strong RIBs. Numerous hybrid populations or
‘hybrid swarms’ have been identified where closely related species come into contact. These hybrid zones are often narrow and stable when hybrid fitness is low or the species are adapted to very distinct habitats (Levin and Schmidt, 1985; Campbell and Waser, 2001); however, interspecies hybridization can act as the nucleus for evolution if hybrids are at least partially viable and suit- able habitats exist to support them (Buerkle et al., 2000).
Hybridization can stimulate evolutionary change in two ways: (i) the adaptive potential of one or both parents might be increased through back-crossing, or ‘introgressive hybridization’ (Fig. 5.10; Anderson,
Species A
Species B F1
I II III IV V VI VII
Generations
Subsequent back-crosses Back-
cross
Fig. 5.10.Cartoon illustrating introgression between two species. Back-crossing of the F1hybrid to species B ultimately results in the absorption of some genes from species A into at least some individuals of species B. (Used with permission from D. Briggs and S.M. Walters, © 1984,Plant Variation and Evolution, Cambridge University Press, New York.)
1949); this trickle of genes might expand the adaptive potential of the recipient population; or (ii) the hybrid population itself may evolve unique adaptations through genetic differentiation and genomic reorgani- zation, or ‘recombinational speciation’ (Stebbins, 1957; Grant, 1958).
The latter process is generally thought to occur over a number of genera- tions, although Rieseberg and Ellstrand (1993) have identified many examples where F1 hybrids had unique phenotypes that could be a nucleus for speciation. Most hybrids are less fit than their progenitors, but several cases have been found where hybrids had higher fitness and unique adaptations (Emms and Arnold, 1997; Burke and Arnold, 2001;
Johnston et al., 2001).
Most hybrid species are polyploid, but speciation via homoploid hybridization has also been documented in several instances (Gallez and Gottleib, 1982; Crawford and Ornduff, 1989; Wolf and Elisens, 1993). In one of the earliest studies of hybridization, Riley (1938) described natural hybridization between Iris fulva and Iris hexagona in Louisiana, USA, using a ‘hybrid index’. He compiled a list of differences between the two species and one was arbitrarily selected at the low end (Fig. 5.11). Plants in the natural environment were then scored for each character and the
Hybrid index values
0 5 10 15
F G
H1 Character scoring
Character scoring
Sepal Exertion
Tube blade Sepal Petal of Stylar
colour colour length shape stamens appendage Crest
Like I. fulva 0 0 0 0 0 0 0
Intermediates 1 1, 2 or 3 1, 2 1 1 1 1
Like I. hexagona 2 4 3 2 2 2 2
Fig. 5.11.Hybridization between Iris fulvaand Iris hexagonain Louisiana, USA. Two relatively pure (F and G) and one hybrid population are shown. (From Riley, 1938.)
grand total was calculated for each individual. Many populations con- tained individuals with intermediate scores, suggesting that they were indeed hybrids. Randolph (1966) later identified a population of Iriscalled
‘Abbeville Reds’ that had a bright red-purple colour distinct from that of any other Iris species, different shaped capsules and a unique habitat of deep shade and high water. He gave it a new species name, Iris nelsonii, and speculated that it was derived from the hybridization of I. fulva and other local species.
Arnold (1993) used a broad array of nuclear and cytoplasmic markers to confirm that the Louisiana irises were indeed hybridizing. He found indi- viduals with many different combinations of the cytoplasmic DNA (cpDNA) and nuclear genes of three species, I. fulva, I. hexagona and Iris brevicaulis (Fig. 5.12). He also found that I. nelsonii carried markers from all three species, although every individual had the I. fulvacytotype and only a few individuals carried species-specific randomly amplified polymorphic DNAs (RAPDs) from the other two species. This suggested that the taxon was the product of repeated back-crossing of the original F1 hybrid to I. fulva, a likely scenario, as the appearance of hybrids in nature is rare and the species have several prezygotic and postzygotic RIBs (Carney et al., 1994;
Carney and Arnold, 1997; Emms and Arnold, 2000).
BAYOU TECHE BAYOU TECHE
RAPD LOCI
A A
B B
I. fulva I. brevicaulis I. hexagona
cpDNA I. fulva I. brevicaulis I. hexagona 10m 10m
A A
B B
Fig. 5.12. Combinations of cpDNA and nuclear markers (RAPDs) in a hybrid swarm of Iris at Bayou Teche, Louisiana. The relative proportion of Iris fulva, Iris hexagona and Iris brevicaulismarkers in each plant is represented by the pie charts. (Used with permission from Arnold, 1993, American Journal of Botany80, 577–583.)
Using morphological and cytological data, Heiser (1947, 1949, 1951, 1958) documented widespread hybridization and introgression among Helianthus taxa in the south-eastern USA. He proposed two instances of introgression, Helianthus annuussubsp. texanus arising due to hybridiza- tion with Helianthus debilis subsp. cucumerifolius and a weedy race of Helianthus bolanderi being the product of introgression with H. annuus.
He also suggested that three species, Helianthus paradoxus, Helianthus anamolus and Helianthus neglectus, were the stabilized products of hybridization between H. annuusand Helianthus petiolaris. Later molec- ular work by Rieseberg and associates (1988, 1990a,b, 1991) verified Heiser’s prediction of a hybrid origin for H. paradoxus and H. anamolus, and the proposed introgression between H. annuus and H. debilis. They also found evidence of the introgression of cpDNA from H. annuus into southern California populations of H. petiolaris (Dorado et al., 1992).
However, the hybrid origin of H. neglectus was not supported, nor was any evidence found of gene transfer between H. annuus and H.
bolanderi.
Rieseberg et al. (1995) went on to show how the genomes of H.
annuus and H. petiolaris were rearranged to produce H. anamolus. They developed a molecular linkage map of the two progenitor species and then compared it with the proposed derivative. They discovered six linkage groups that were conserved across all three species (collinear), and another 11 chromosomal regions whose gene order differed across taxa. Of these 11, H. anamolus shared four of them with one or the other parent, while the other seven were distinct from either parent, suggesting that substantial reorganization had occurred within these linkages (Fig. 5.13).
To determine if particular gene assemblages were maintained by selec- tion during the formation of H. anamolus, Rieseberg et al.(1996) produced three hybrid lineages through artificial crosses and compared them with the ancient hybrid species, using a map-based approach. The genomic compo- sition of the ancient and synthesized genomes were highly concordant, indi- cating that the particular gene assemblages maintained in the hybrids were probably under selection. Some parts of the genome were less subject to introgression than others, suggesting that there was coadaptation between blocks of parental species genes. Jiang et al.(2000) also found introgression to be confined to specific chromosomal regions in interspecific populations of polyploid Gossypium.
To further confirm the role of coadapted complexes in hybrid species formation, Rieseberg et al.(1999) examined 88 markers across 17 chromo- somes in three natural hybrid zones of H. petiolaris and H. annuus. They found patterns of introgression to be quite similar across all three hybrid zones, with 26 chromosomal locations having significantly lower levels of introgression than according to neutral expectations. They were even able to link pollen sterility with 16 of these segments.