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Hybrid Fitness, Adaptation and Evolutionary Diversification: Lessons

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Hybrid Fitness, Adaptation and Evolutionary Diversification: Lessons Heredity (2012) 108, 159–166 & 2012 Macmillan Publishers Limited All rights reserved 0018-067X/12 www.nature.com/hdy REVIEW Hybrid fitness, adaptation and evolutionary diversification: lessons learned from Louisiana Irises ML Arnold, ES Ballerini and AN Brothers 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 genotypeÂenvironment 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. Heredity (2012) 108, 159–166; doi:10.1038/hdy.2011.65; published online 27 July 2011 Keywords: natural hybridization; habitat selection; hybrid fitness INTRODUCTION process (Anderson, 1949; Anderson and Stebbins, 1954; Mayr, 1963; ‘Considering the several rules now given, which govern the fertility of Lewontin and Birch, 1966; Grant, 1981; Barton and Hewitt, 1985; first crosses and of hybrids, we see that when forms, which must be Arnold, 1992, 1997, 2006, 2008; Grant and Grant, 1992, 2010; considered as good and distinct species, are united, their fertility Dowling and DeMarais, 1993; Rieseberg, 1997; Rieseberg et al., graduates from zero to perfect fertility, or even to fertility under 2003; Seehausen, 2004; Seehausen et al., 2008; Anderson et al., certain conditions to excess. That their fertility, besides being emi- 2009). Significantly, there are now numerous studies that have inferred nently susceptible to favorable and unfavorable conditions, is innately a causal link between natural hybridization and adaptive evolution variableyit is by no means always the same in degree in the first cross and/or diversification (Grant and Grant, 2002; Salzburger et al., and in the hybrids produced from this cross’ (Darwin, 1859). 2002; Rieseberg et al., 2003; Seehausen, 2004; Schwarz et al., 2005; The above quote demonstrates that Darwin observed variation in Martin et al., 2006; Anderson et al., 2009; Johnson et al., 2010). fertility within and among species and considered its importance for Many examples of diversification and adaptation as the result of understanding evolutionary processes. Notwithstanding this clarity, reticulate evolution have come to light, leading to the formation of Darwin indicated throughout The Origin his concept that reticulate several related hypotheses. These include: (1) hybrid genotypes with evolution had a relatively unimportant role during descent with high relative fitness are produced more often than previously assumed modification (for example, see the only figure included in this (Arnold and Hodges, 1995); (2) even hybrids with low relative fitness book). Yet, his description of a wide range of hybrid fitness, and the may act as a conduit for genetic exchange, given that they have some influence of interactions between individuals in response to a given level of fertility (Arnold and Hodges, 1995; Arnold, 1997, 2006); and environment in determining this range, begs an alternative conclusion. (3) for many taxonomic groups, allopatric divergence is not as Thus, relatively fit hybrids, like other ‘more fit’ genotypes might be frequent as divergence accompanied by some level of at least inter- expected to contribute significantly to adaptation and diversification. mittent gene flow (that is, parapatric or sympatric divergence; Pinho Since Darwin’s time, many researchers have reported on the relative and Hey (2010)). Numerous authors including Darwin himself—see fitness of hybrids and have found that in many cases, hybrids are as fit, above quote—contributed to the formulation of the first hypothesis or fitter than their pure species counterparts (see Arnold and Hodges (relating to the production of relatively fit hybrid genotypes). Since (1995); Arnold (2006, 2008) and Arnold and Martin (2010) for Darwin, numerous reviews and books have addressed the concept reviews). Many have debated what these estimates might mean with of hybrid fitness, with some addressing the relative importance or regard to the impact of genetic exchange on evolutionary pattern and unimportance of hybrid genotypes in the evolutionary and ecological Department of Genetics, University of Georgia, Athens, GA, USA Correspondence: Professor ML Arnold, Department of Genetics, University of Georgia, Athens, GA 30602 USA. E-mail: [email protected] Received 9 December 2010; revised 19 May 2011; accepted 31 May 2011; published online 27 July 2011 Hybrid fitness and evolution in Louisiana Irises ML Arnold et al 160 trajectories of plant and animal lineages (Dobzhansky, 1937; Mayr, known as the Louisiana Irises. In particular, we wish to emphasize the 1963; Endler, 1977; Moore, 1977; Barton and Hewitt, 1985; Howard, development of this plant species complex into a model for identifying 1993; Arnold and Hodges, 1995; Arnold, 1997, 2006, 2008; Arnold some of the genetic and ecological components that affect hybrid and Martin, 2010; Grant and Grant, 2010). The data available for fitness. This definition of components affecting the fitness of these reviews (particularly those deriving from genomic information) Louisiana Iris hybrid genotypes has allowed us to make comparisons have multiplied exponentially over the past decade due largely to the with other reticulate complexes and thus to test whether different advances in methodologies for collecting and analyzing DNA hybrid genotypes vary in fitness across environments and whether sequences (Green et al., 2010) and for deciphering the function of hybrid genotypes with either elevated or lowered fitness have con- the underlying genes (Rosas et al., 2010). However, the species tributed to genetic exchange during the diversification of lineages and complexes that have provided the most rigorous and detailed descrip- species complexes. tions of hybrid fitness have done so because of the availability of both genetic and ecological information (Grant and Grant, 1992, 2010; HYBRID FITNESS VARIES: TESTING A TRUISM? Rieseberg et al., 2003; Martin et al., 2005, 2006; Arnold et al., 2010; One of the hallmarks of research into genetic exchange during and see Arnold and Martin (2010) for a review). These various evolutionary diversification has been the assumption of either creative catalogs of hybrid fitness estimates have demonstrated that ‘all hybrids or destructive consequences. Within the creative paradigm, hybridiza- are not created equal’ in terms of their fitness. As Darwin recognized, tion (or lateral exchange or viral recombination) is ascribed the hybrid genotypes can demonstrate lower, equivalent or higher fitness potential role of a catalyst for the formation of novel lineages and/ relative to progenitor and other hybrid genotypes, and this variation or adaptations. For example, Rieseberg et al. (2003) and Seehausen can reflect genotypeÂenvironment interactions. (2004) inferred a primary causality for hybridization between diver- The observation of relatively high fitness of some hybrid genotypes gent lineages of sunflowers and cichlid fish, respectively, to the suggests one causal factor by which both parapatric and sympatric origin of novel adaptations and adaptive radiations. Similarly, Grant divergence are accompanied by introgression. In particular, as lineages and Grant (2008, 2010) have documented the adaptive evolutionary diverge, some genetic exchange can be the result of selection favoring impact of low levels of gene flow between various Darwin finch the incorporation of foreign alleles, and thus the formation of species. admixed genotypes (Grant and Grant, 2002; Rieseberg et al., 2003; In contrast to the concept of genetic exchange as a novelty- Martin et al., 2006). However, as suggested by hypothesis 2, this generating process, is the perception of hybridization and lateral selective incorporation can be accomplished through relatively unfit exchange as disruptive of the natural order of diversification. hybrid genotypes as well. This is possible because a hybrid with lower Classically, Mayr (1963) stated, ‘The total weight of the available overall fitness (for example, one that has low, but not zero, fertility) by evidence contradicts the assumption that hybridization plays a major definition produces gametes that are viable
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