EXPERIMENTAL EVIDENCE FOR THE GENETIC-TRANSILIENCE MODEL OF SPECIATION.

Rice and Hostert (1993) recently presented a literature review of laboratory experiments on speciation and concluded that there was little or no support for the "bottleneck model of speciation." This conclusion is flawed because the most relevant papers in the experimental literature on this topic are not cited by Rice and Hostert (1993), internally inconsistent criteria for evaluation are used in the contrast of bottleneck models versus the other speciation models, and the predictions of the genetic-transilience model of speciation are inaccurately portrayed. Before discussing the above issues, it is first necessary to clarify the modes of speciation being discussed. Although Rice and Hostert (1993) acknowledge that three different models of founder-induced speciation have been presented (Carson and Templeton 1984), they still proceed to equate the "bottleneck model of speciation" to genetic revolution (p. 1638). A discussion of the distinction of the geneticrevolution model from the alternatives of genetic transilience and founder flush can be found in Carson and Templeton (1984), so only a brief distinction will be presented here. Genetic revolution occurs after an extreme founder event and subsequent small population size has eroded virtually all genetic variability from the founding population's gene pool. This is likely to occur only in a peripheral population that remains isolated from the ancestral population for many generations with persistent small variance effective size; hence, this mechanism is also called peripatric speciation (Mayr 1982). None of the experimental protocols reviewed by Rice and Hostert (1993) tried to approximate this genetic situation, so the genetic-revolution model is irrelevant to their review. In contrast, both the genetic-transilience and founder-flush models stipulate that the founder event is followed by a large increase in population size; for example, colonization of a new territory with an open ecological niche for the founding population. Both of these models are also predicated upon the assumption that much nuclear genetic variability is retained in the founding population; and indeed both models actually predict an increase of certain classes of genetic variability in the founding population. However, the genetic-transilience and founder-flush models do differ in the type of genetic variability that is used in the speciation process and in its selective impact. The genetic-transilience model focuses on polymorphic systems in the ancestral population that have a genetic architecture characterized by at most a few major "segregating units" (thereby including both genic and chromosomal variants as discussed in Templeton 1981, although for ease of presentation, the words "allele" and "locus" will be used hereafter) that have large phenotypic effects on syndromes with many pleiotropic effects on fitness-related traits. These pleiotropic effects in turn can be altered by modifying loci. Hence, there is at most a few major "loci" with many epistatically modifying loci. An example of this type of polymorphic system is provided by abnormal abdomen, as found in natural populations of Drosophila mercatorum. The major "loci" in this case are the ribosomal DNA (rDNA) multigene family complex on the X chromosome and a second X-linked locus that controls the pattern of somatic underreplication of rDNA in polytene tissues. These two loci are closely linked but separable through recombination, but due to linkage disequilibrium they form a supergene complex in natural populations (Hollocher et al. 1992). The abnormal-abdomen syndrome affects egg-to-adult developmental time, female agespecific fecundity, adult longevity, male reproductive maturity rates, male mating success, system of mating, and several morphological features. These pleiotropic effects are under intense natural selection (Templeton et al. 1989, 1990) and are subject to genetic modification in a trait specific fashion via epistatic loci scattered throughout the D. mercatorum genome (Templeton et al. 1985, 1993; Hollocher and Templeton 1994). Under genetic transilience, there is no radical overall reduction in levels of genetic variation in the founding population as in the genetic revolution model, but the initial founder effect can occasionally induce severe allele frequency alterations at one or more of the major loci, including fixation. Such a frequency alteration at the major locus then induces a cascading selective response at the modifier loci that are extremely responsive to selection in the founding population (Templeton 1980). The theoretical prediction of increased responsiveness to selection at the modifier loci has been elaborated and confirmed by subsequent theoretical work showing that founder events can indeed convert epistatic variance into additive genetic variance, thereby increasing-not diminishing-the overall levels of additive genetic variance and hence selective responsiveness immediately after the founder event (Goodnight 1988; Wagner et al. 1994). This responsiveness is also predicted to be enhanced by recombination through the creation of novel, selectively important allelic combinations (Templeton 1980); such as recombination between the major X-linked elements in the abnormal-abdomen syndrome. Thus, genetic transilience is triggered by drift effects