Natural selection and speciation.

A paper by Korol et al. (1) in this issue demonstrates significant premating reproductive divergence between Drosophila melanogaster populations adapted to distinct, but closely adjacent, habitats in ‘‘Evolution Canyon’’ on Mt. Carmel, Israel. The authors suggest that reproductive isolation has evolved in situ as a result of adaptive divergence in response to the contrasting environments of northand south-facing slopes in Evolution Canyon despite the fact that the populations are within easy ‘‘cruising range’’ (2) of each other. The authors suggest that the divergence of Drosophila occupying distinct habitats in Evolution Canyon represents an early stage in ecological speciation in which divergent natural selection drives the accumulation of genetic differences among populations, resulting in reproductive isolation. The paper by Korol et al. (1) addresses one of the most persistent questions in evolutionary biology: How do new species arise? As with so many apparently simple questions, there is no simple answer, only complex answers to a number of interrelated questions. How do sexually reproducing organisms become reproductively isolated? How do environment and ecological interactions influence the formation of new species? Are the processes of local adaptation and the evolution of reproductive isolation the same (i.e., both resulting from the accumulation of small, adaptive genetic changes) or are the genetic changes leading to reproductive isolation fundamentally different (i.e., large and rapid genetic changes such as chromosomal rearrangements, genetic revolutions, transilience, or founder events)? Is the disruption of gene flow necessary? What are the relative roles of chance events (e.g., genetic drift) and selection in speciation? The short answer to all of the above questions is that reproductive divergence can evolve in a number of ways. Both drift and selection can be important depending on the number, degree of interaction, and magnitude of effect of genes involved in reproductive isolation; on the relationship between genes controlling reproductive compatibility and phenotypic characters that may be under ecological selection; and on the historical effective population size of the diverging populations. Reproductive isolation may evolve as a consequence of genetic drift in populations of small effective size (see, e.g., refs. 3–5 for recent treatments), or as a byproduct of adaptive divergence or genetic drift in large populations in allopatry [the classic allopatric divergence model of Mayr (6)]. Reproductive isolation may also evolve in sympatry because of disruptive or divergent selection. For example, natural selection on characters important in both ecological function and mate recognition [such as bill size in Darwin’s finches (7) or body size and shape in sticklebacks (8–10)] can lead to premating reproductive isolation without geographic isolation. Rapid chromosomal changes (as in the origin of polyploid plants) can result in instantaneous reproductive isolation, as can changes in genes of large effect that result in rapid evolution of phenotypic characters important in reproduction (e.g., ref. 11). Host shifts in phytophagous insects are wellknown to result in essentially instantaneous reproductive isolation (e.g., refs. 12–14). The challenge is to distinguish among alternative hypotheses for diversification in natural populations and to determine the relative roles of selection and drift in speciation. Natural selection has always been considered a key component of adaptive divergence and speciation (2, 15–17), but the importance of selection has been eclipsed in recent decades by a strong focus on the geography of speciation and on the purely genetic mechanisms by which reproductive isolation evolves (see refs. 18–20 for reviews). Even though selection was seen as critically important in sympatric speciation, sympatric divergence was thought to be rare, and the role of ecology and the environment in diversification received little emphasis. Currently, there is resurgent interest in the role of ecology in speciation. Several recent studies (9, 21–28) have emphasized the importance of ecology and selection in speciation, regardless of the geographic context in which populations diverge, and the term ‘‘ecological speciation’’ has become an important part of the modern lexicon. In a review of 40 years of laboratory experiments on speciation in Drosophila, Rice and Hostert (29) concluded that founder events, drift, and isolation played little role in speciation (but see ref. 20 for critique). On the other hand, diversifying selection was found to contribute substantially to the evolution of reproductive isolation, even when populations were not isolated [see also Barton and Charlesworth (30) who reached a similar conclusion]. This finding bolstered earlier theoretical studies that showed how premating reproductive isolation could evolve as a consequence of ecological selection on characters involved directly in mate recognition or as a consequence of pleiotropy or genetic hitchhiking of genes controlling ecological and reproductive characters (31–33). The paper by Korol et al. in this issue (1) is important in that it demonstrates significant premating reproductive isolation among populations of D. melanogaster experiencing divergent selection between habitats, whereas there is no reproductive isolation among populations occupying similar habitats. This result is consistent with the evolution of reproductive divergence as a consequence of ecological selection (ecological speciation). However, a key question remains unanswered, namely, did reproductive isolation evolve in situ in response to selection or is the presence of reproductive isolation among populations a result of secondary contact between divergent populations whose ecologies differ and whose ranges abut in Evolution Canyon? This question is important because it bears on the mechanisms by which reproductive isolation has evolved. If the populations are historically divergent, then a degree of reproductive isolation may have evolved because of drift or as a byproduct of adaptive divergence in allopatry before their meeting in Evolution Canyon. If premating reproductive isolation has evolved in situ as a result of local adaptation, then traits under ecological selection must be either directly involved in mate choice, or genetically correlated (via pleiotropy or linkage) with phenotypic characters important in mate choice. History, and the relative roles of drift and selection, are general issues for empirical studies of speciation in natural populations.