Hybrid fitness, adaptation and evolutionary diversification: lessons learned from Louisiana Irises

Abstract

Estimates of hybrid fitness have been used as either a platform for testing the potential role of natural hybridization in the evolution of species and species complexes or, alternatively, as a rationale for dismissing hybridization events as being of any evolutionary significance. From the time of Darwin's publication of The Origin, through the neo-Darwinian synthesis, to the present day, the observation of variability in hybrid fitness has remained a challenge for some models of speciation. Yet, Darwin and others have reported the elevated fitness of hybrid genotypes under certain environmental conditions. In modern scientific terminology, this observation reflects the fact that hybrid genotypes can demonstrate genotype × environment interactions. In the current review, we illustrate the development of one plant species complex, namely the Louisiana Irises, into a 'model system' for investigating hybrid fitness and the role of genetic exchange in adaptive evolution and diversification. In particular, we will argue that a multitude of approaches, involving both experimental and natural environments, and incorporating both manipulative analyses and surveys of natural populations, are necessary to adequately test for the evolutionary significance of introgressive hybridization. An appreciation of the variability of hybrid fitness leads to the conclusion that certain genetic signatures reflect adaptive evolution. Furthermore, tests of the frequency of allopatric versus sympatric/parapatric divergence (that is, divergence with ongoing gene flow) support hybrid genotypes as a mechanism of evolutionary diversification in numerous species complexes.

Figure 1

Hybrid fitness varies by genotype and by environment. (a) Individuals (represented by linkage groups; the different colored regions reflect genetic material from hybridizing species) may suffer from reduced fitness as the result of genetic incompatibilities regardless of the environment. These hybrid genotypes are then lost from the population (indicated by a red ‘X'). (b) The fitness of the remaining individuals can then be tested in different environmental conditions (such as wet and sunny versus dry and shady).

Figure 2

(a) The typical natural distribution of Iris brevicaulis and Iris fulva. I. brevicaulis and I. fulva often occur in sympatry near bayous and waterways in southern Louisiana. Although plants from each species may grow within a meter of one another, elevational gradients along bayou edges and differences in microhabitats provide distinct growth environments for each species. I. brevicaulis is generally found in mixed hardwood forest at slightly higher elevations that do not experience flooding, whereas I. fulva is found at lower elevations in soils that are often submerged in water. (b) Results of experiments on I. brevicaulis and I. fulva backcross individuals. Genetic clones from two backcross populations, one toward I. brevicaulis and one toward I. fulva, were grown in both a greenhouse common garden and in a common garden in a natural Louisiana Iris setting. In the drier greenhouse common garden, backcross genotypes toward I. brevicaulis survived at a higher frequency than did those in the direction of I. fulva. Three QTLs introgressed from I. brevicaulis increased survivorship of I. fulva backcrosses. Interestingly, some alleles from wet-adapted I. fulva increased the fitness of I. brevicaulis backcross genotypes even in these dry conditions. The natural common garden experienced higher water levels than usual, resulting in prolonged flooding across the site. A cline in survivorship was seen with I. fulva parents showing the highest percentage survival (27%), followed by individuals backcrossed to I. fulva (9%), and then individuals backcrossed to I. brevicaulis (5.5%). I. brevicaulis parents had no survivors. Although individuals composed primarily of the dry-adapted I. brevicaulis alleles were generally less fit in the flooded environment, a QTL from I. brevicaulis was associated with higher survival of certain I. fulva BC₁ individuals in the flooded conditions.