Experimental evidence for the genetic-transilience model of speciation.
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 genetic-revolution 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 age-specific 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 at major loci that are induced by the initial founder event and that subsequently interact with genetic architectures characterized by much gene-action level epistasis and with recombination to produce an expanding founding population that has enhanced responsiveness to selection (just the opposite of the genetic revolution model) and is thereby subject to rapid evolutionary change.
In contrast, the founder-flush model regards the phase of rapid population growth as being one of relaxed selection but during which recombination will produce new combinations of genes that would normally be selected against because of their epistatic interactions under the prefounder environmental conditions. When selection is reimposed upon the population as it reaches its new carrying capacity, selection will now be operating upon new gene combinations, thereby allowing novel evolutionary pathways to be explored. Note that the demographic and basic genetic conditions (the roles of epistasis and recombination) of the genetic transilience and founder-flush models are mechanistically compatible and that these models differ primarily in the timing and triggering agent of selection. Thus, a single bottleneck event can be affected by both genetic transilience and founder flush. However, these two models of bottleneck speciation are mechanistically incompatible with genetic revolution because both of them require a founding population that has in some sense enhanced - not depleted - genetic variability. Because most of the experiments reviewed by Rice and Hostert (1993) at least attempted to satisfy the demographic conditions of the genetic transilience and founder-flush models (although, as will be pointed out later, many of these experiments ignored other explicit conditions of these models), the remainder of this note will substitute the term "genetic transilience" for Rice and Hostert's "bottleneck" speciation, although in this context genetic transilience is not distinguished from the founder-flush model.
Rice and Hostert (1993) begin their discussion of genetic transilience speciation by dismissing my experimental studies on D. mercatorum (Templeton 1979a) in light of a criticism made by Charlesworth et al. (1982) that this work is irrelevant to sexual speciation processes because it used parthenogenesis to induce an extreme bottleneck effect. Much of this uneasiness about parthenogenesis is based upon some fundamental misconceptions about parthenogenesis in Drosophila and its genetic consequences. First, there is the misconception that because D. mercatorum, a normally sexually reproducing species, has facultative parthenogenesis, it must be a genetically odd species with an unusual genetic system. However, almost all species of Drosophila have facultative parthenogenesis (27 out of 29 species surveyed, Templeton 1983), so if species with this capacity are to be excluded because they are odd, virtually every experiment reviewed by Rice and Hostert (1993) must also be excluded as they also use species with this capacity (including Drosophila melanogaster, Fuyama 1986). The fact is that all Drosophila have a genetic system that is preadapted to automictic, diploid parthenogenesis (Templeton 1983). Completion of meiosis in the egg does not generally depend upon fertilization, mitosis activating factors reside in the central part of the egg, and all early mitotic divisions occur in a syncytium with no cytological barriers separating the nuclei. All of these features preadapt Drosophila to automixis, a form of parthenogenesis in which normal meiosis is retained. Moreover, most parthenogenetic reproduction in Drosophila, and all in D. mercatorum, restores the normal state of diploidy by some sort of postmeiotic fusion of nuclei that is facilitated by the lack of cytological barriers in the egg. Automictic diploidy, by retaining a completely normal meiosis and restoring diploidy, represents a form of parthenogenesis that deviates the least from normal sexual reproduction; and indeed parthenogenetic females are fully capable of reproducing either sexually or parthenogenetically by using exactly the same meiotic and early developmental system as used in sexual reproduction. Hence, there is no unusual or odd genetic system at work here. Finally, there is the concern that the gene complexes revealed by these experiments were really the result of murational accumulation and clonal selection over many generations of parthenogenetic reproduction rather than the result of founder effects. This is a valid concern for the initial work on coadapted gene complexes in long-established parthenogenetic strains (Templeton et al. 1976) but is irrelevant to the subsequent studies that used newly established parthenogenetic lines that were isolated directly from sexual reproducing, natural populations (Templeton 1979a).
What is true is that these experiments (Templeton 1979a) were done prior to the formulation of the genetic-transilience model of speciation (Templeton 1980) and hence were obviously not performed to test or validate that theory. However, these experiments were the primary inspiration of the genetic-transilience model, as pointed out by Carson and Templeton (1984). Given that these experimental results were incorporated into the genetic-transilience model at the most fundamental level, their relevancy to bottleneck-induced models of speciation is augmented, not diminished.
These early experiments using parthenogenesis suggested that extreme founder effects could result in rapid and radical shifts in coadapted gene complexes affecting viability, fecundity, and other life-history characteristics (Templeton et al. 1976; Annest and Templeton 1978; Templeton 1979a). A second round of experiments was then initiated with this sexual/parthenogenetic system of reproduction (Templeton 1989). Drosophila mercatorum, along with most Drosophila, normally reproduces sexually, but both laboratory and natural populations have the ability to reproduce parthenogenetically under automictic diploidy (Templeton 1979b, 1983). Diploidy is usually restored after meiosis by the fusion of two mitotic products of a single pronucleus, thereby producing a doubled haploid. Hence, this system induces an extreme genetic bottleneck. Genetic variation will still exist among the parthenogenetic progeny of a single virgin female extracted from the sexual population because of meiosis, so there is much opportunity for selection to operate in this single generation of an extreme bottleneck. Moreover, because the parthenogenetic females are diploid and retain meiosis, it is possible to create a sexual population that is genetically identical to a parthenogenetic stock (save for the introduction of a Y chromosome in the males of the sexual population) by using an isogenic laboratory stock with visible markers on its autosomes and exploiting the lack of recombination in male meiosis (Templeton 1983). In the experiments of Templeton (1989), the source population for the founders is the first generation of laboratory reared offspring of inseminated females captured in nature. Hence, the source of genetic variability in these experiments is derived from matings in the wild. A generation of parthenogenesis is then used to induce an extreme bottleneck effect. Next, sexual crosses were used to study the same types of pre- and postisolating mechanisms that occur in sexual populations (Mayr 1970). The rationale for using parthenogenesis in this design is to "push the essence of the founder-speciation models to their absolute extremes in the hope of speeding up the evolutionary process to the point where empirical study would be more feasible" (Templeton 1989, p. 139). This design obviously intensifies and simplifies the natural phenomenon to be studied; but that is the essence of any experiment and the same criticism can be applied to every experiment cited by Rice and Hostert (1993) in favor of the "allopatric model." (Note, the genetic-transilience and founder-flush models are also allopatric models of speciation, so Rice and Hostert's use of the word "allopatric" is neither standard nor consistent. From the context of their paper, their "allopatric model" is equivalent to the speciation mechanism of "adaptive divergence" in the terminology of Templeton . To avoid perpetuating this confusion, the term "adaptive divergence" will be used in the remainder of this note to refer to those uses of "allopattic" by Rice and Hostert that clearly relate to the adaptive divergence mechanism and not to genetic transilience.) These adaptive divergence experiments usually used stocks that had been in the laboratory for many generations, and hence began with an "unnatural" source of genetic variation. In these adaptive divergence experiments, selection was manipulated to be intense and consistent over many generations and usually directed at only one or, rarely, a handful of traits at a time - a situation that differs considerably from selection in natural populations in which intensities vary dramatically over both space and time and in which multiple traits are being simultaneously selected, often with complex fitness trade-offs (Templeton et al. 1989, 1990, 1993; Hollocher and Templeton 1994). These facts are not being raised to undermine the conclusions drawn from these experiments, only to show that all experiments intensify and simplify the phenomena under study in order to obtain interpretable and more easily measurable results.
This second round of experiments using the sexual/parthenogenetic system found in D. mercatorum resulted in virtually 100% premating isolation, complete male sterility, and a strong [F.sub.2] viability breakdown (Templeton 1989): isolating barriers far stronger than those described in any of the experiments cited by Rice and Hostert (1993) in favor of the adaptive divergence model. Moreover, the genetic bases of these isolating mechanisms involved multilocus systems with strong epistasis among major and modifying loci with much recombination (Templeton 1989), as predicted by the genetic-transilience model (Templeton 1980). These results are highly supportive of genetic transilience, but of course they do not prove that the less extreme founder effects found in nature would have the same effects (Templeton, 1989); but neither do the experiments cited by Rice and Hostert (1993) prove that natural selection operating upon natural gene pools would have the same effects as highly artificial selective regimes operating upon laboratory altered gene pools. However, there is no doubt that parthenogenesis does indeed induce a genetic bottleneck. Hence, the one thing that is not open to alternative interpretations is that bottlenecks can produce strong to complete pre- and postzygotic isolation.
Rice and Hostert (1993) are internally inconsistent in their use of statistics to examine the validity of the various speciation models. With regard to the work of Powell (1978) and Dodd and Powell (1985), Rice and Hostert (1993, p. 1646) noted that two of the eight lines showed "persistent and statistically significant, prezygotic isolation," but then added that the quantitative degree of isolation was "low." However, the degree of isolation found in these two lines is comparable quantitatively to that found in the references they cite on prezygotic isolation in favor of the adaptive divergence model (the references in Part A of their Table 1). Rice and Hostert (1993) then claimed that the results of Dodd and Powell (1985) lacked significance by noting that two out of eight experimental lines evolved significant isolation, but neither of the two controls lines did, and this results in a non-significant 2 x 2 contingency test. Similarly, the bottleneck experiment of Ringo et al. (1985) was also subjected to this contingency analysis of experimentals versus controls. However, the purpose of control lines in these (and most) experiments is not to provide multiple replicates for a higher-ordered meta-analysis, but rather to provide a baseline for monitoring the treatment effects. If the same type of statistical analyses were applied to the experiments that Rice and Hostert (1993) cite in favor of other speciation models, all of them would be dismissed as insignificant (including the work of Rice and Salt 1990, which had only two treatments and one control lines and hence could not possibly yield a significant result with this contingency analysis). Obviously, to dismiss all of this work as insignificant is inappropriate and represents a fundamental abuse of statistics in the context of a treatment/control experimental design. The experiments of Powell (1978) and Dodd and Powell (1985) do indeed support the genetic-transilience model in a way comparable statistically and quantitatively to the references cited as supporting the adaptive divergence and "gene flow" ("habitat divergence" in the terminology of Templeton 1981) models.
Contingency meta-analyses do have a legitimate role in evaluating experimental results. Typically, they are not used to contrast treatments versus controls within an individual experiment but rather are used to look for and examine trends found over several different experiments (Hedges and Olkin 1985). Following is a more standard use of a contingency meta-analysis of the works of Powell (1978), Dodd and Powell (1985), Ringo et al. (1985) and Galiana et al. (1993) that all dealt with bottlenecks (treatments) and controls and the evolution of prezygotic reproductive isolation. Two out of eight treatments and zero of two controls resulted in significant isolation in the experiments of Dodd and Powell (1985), and one out of eight treatments and zero out of eight controls resulted in isolation in Ringo et al. (1985). Galiana et al. (1993) report no evolution of isolation in 12 controls and give the results for 45 experimental lines. However, most of these experimental contrasts violate the conditions required for genetic transilience (Templeton 1980; Carson and Templeton 1984), as will be discussed in more detail shortly. The legitimate tests of genetic transilience are the "BCA" lines with three or fewer founder pairs. The isolation indices, along with significance levels, are given in Table 6 for these lines in Galiana et al. (1993). Some of these test results represent multiple measurements on the same lines taken at different times during the course of the experiment. Such results are not independent (Templeton 1974), so only the final test for a given line is considered. These restrictions limit the tests of genetic transilience to only ten of the lines given in Table 6 of Galiana et al. (1993), and seven evolved significant prezygotic isolation. Hence, combining all of these experiments, bottlenecked populations resulted in significant pre-zygotic isolation in 10 cases out of 26, whereas the controls resulted in significant isolation 0 times out of 22. This result is significant at the 0.1% level using a two-tailed Fisher's exact test. Hence, when used properly, a contingency meta-analysis provides strong support of the hypothesis that bottlenecks facilitate the evolution of reproductive isolation.
The reason why many of the experimental lines described in Galiana et al. (1993) were excluded from the meta-analysis is that genetic transilience is likely to occur only when many conditions in addition to a bottleneck are satisfied (Templeton 1980). Because other factors are necessary for genetic transilience, an experiment using bottlenecks is not automatically an experiment of genetic transilience speciation. Indeed, the model of genetic transilience predicts that most founder effects do not lead to speciation (Templeton 1980). This predicted rarity of founder-induced speciation events was misinterpreted by Rice and Hostert (1993) as meaning that the model is "virtually impossible to reject experimentally." This would be a valid argument if the transilience model made no specifications as to what types of founder events would be predisposed to speciation events and which not, but this is not the case. The conditions that both augment and diminish the likelihood of speciation were specified in great detail in terms of the attributes of the ancestral population (Templeton 1980, p. 1016-1020), the nature of the sampling event that produces the founders (p. 1020-1023), the attributes of the founder population after its establishment (p. 1024-1030), and many other basic biological attributes (e.g., chromosome number, system of mating, and so on; see Table 2 of Templeton 1980). Indeed, I know of no other model of speciation that has made so many detailed predictions about factors that both augment and diminish the likelihood of speciation. These specific predictions make this model testable with respect to both positive and negative results (Templeton 1980, p. 1031).
These predictions will now be used to reevaluate the set of experiments performed by Galiana et al. (1993) with Drosophila pseudoobscura, the same species used by Powell (1978) and Dodd and Powell (1985). Galiana et al. (1993) examined 45 experimental lines that differed in their ancestral source population, founder numbers, and number of founder-flush events. When examined over all 45 lines, the evolution of reproductive isolation appears sporadic and weak, particularly in contrast to the earlier work by Powell (1978). Galiana et al. (1993) were surprised by these differences, stating that "we have no obvious explanation for these differences between Powell's and our experiments" (p. 441). However, these differences are readily explained by the other conditions that I had published long before these experiments were performed; particularly since I had discussed these predictions specifically in terms of the D. pseudoobscura experimental system (Templeton 1980, p. 1030-1031) relative to Powell's (1978) work. One of the critical features of Powell's design relative to the predictions of the genetic-transilience model was that Powell selected as founders those lines derived from his base population that were most homokaryotypic. Recall that both the genetic transilience and founder-flush models place great importance on recombination as a source of genetic variation in the founding population. Paracentric inversions in Drosophila suppress recombination, and given the small genome size in this genus, even a single inversion polymorphism will commonly suppress recombination in a substantial (up to around 20%) portion of the genome. Hence, inversion polymorphisms in the founders are predicted to reduce substantially the chances of genetic transilience (Templeton 1980). Galiana et al. (1993) used two different sources for their lines; the BCA strains that were chromosomally monomorphic and the MA lines that were extremely polymorphic for inversion arrangements. According to the explicit predictions for D. pseudoobscura (Templeton 1980), this extensive inversion polymorphism should substantially decrease the chances for genetic transilience. Hence, when looking for positive results, the MA strains should be excluded.
The genetic-transilience model also requires that the in-breeding effective size of the founder or bottleneck population be extremely small relative to the inbreeding effective size of the ancestral population (Templeton 1980). There is no direct information about inbreeding effective sizes in these experiments, but the BCA population was started with 204 adult flies, and the bottlenecks consisted of from two adult flies (one pair) to 18 (nine pairs). Assuming that the inbreeding effective sizes are roughly comparable to the adult sizes, the change of inbreeding effective size is only an order of magnitude for the higher pair numbers. Moreover, there has been much work about the genetic consequences of founder effects relative to founder number, mostly in the context of conservation genetics. Most of the genetic consequences of founder effects are highly nonlinear with founder number when the founder number is fewer than 10 (five pairs), but the effects are very modest at 10 or more (e.g., see Senner 1980). For example, the triggering event under genetic transilience is a severe alteration of allele frequency at a major locus due to the initial founding event. Consider for example, an allele at a major locus with a frequency of 0.5 (as is the case, for example, for abnormal abdomen in some natural populations, Templeton et al. 1989, 1990). Consider now a founder event that would lead to fixation of an allele at this major locus, thereby instantly converting almost all epistatic interactions of other loci with this major locus into additive genetic variance. For an autosomal major locus, the probability of fixation is [(0.5).sup.2N], where N is the founder size. Given that the major elements in genetic transilience are often predicted to be X-linked (Templeton 1987), consider now an X-linked major locus in which the number of founder males is twice that of the females (an expected situation in Drosophila in which wild-caught females are frequently multiply inseminated). Now the probability of fixation is [(0.5).sup.4N/3] (note, this equation ignores the fact that the number of males and females must be an integer, so the actual probabilities of fixation in real populations will fluctuate above and below this equation). Figure 1 shows a plot of these two equations. As can be seen, there is virtually no chance of fixation at a major autosomal locus when the founder size is greater than five, or for the X-linked locus when the founder size is greater than eight. Accordingly, founder events involving ten or more individuals are unlikely to serve as a trigger for genetic transilience. In terms of positive results, only those lines in Galiana et al. (1993) that use fewer than five founder pairs are therefore relevant (which turns out to be three or fewer pairs in their experimental design). When one restricts the evidence for genetic transilience to these lines, seven out of 10 evolved significant prezygotic reproductive isolation, as noted earlier. Hence, the results of Galiana et al. (1993) are actually stronger than those of Powell's (two out of eight) when one excludes the diluting effects of lines that were predicted to result in no or weak isolation long before this experiment was implemented. The results of Galiana et al. (1993) are strongly concordant with the predictions made by Templeton (1980), both with respect to positive and negative results. The work of Galiana et al. (1993), therefore, represents a major empirical confirmation of the genetic-transilience theory.
Relative to positive versus negative results, Carson and Templeton (1984) also pointed out that some of the strongest experimental evidence for genetic transilience comes from experiments using organisms that have more of the attributes facilitating genetic transilience as given in Table 2 of Templeton (1980) than are possessed by most standard laboratory organisms, such as D. melanogaster. Yet, none of the papers cited by Carson and Templeton (1984) in this regard were considered as evidence for founder-induced speciation by Rice and Hostert (1993). First, the papers dealing with D. mercatorum were not even considered, as discussed above.
Second, Carson and Templeton (1984) cited experiments performed with Hawaiian pictured-winged Drosophila, which have the attributes most likely to facilitate founder-induced speciation among the Drosophila (Templeton 1980). Not many experiments have been done with Hawaiian picture-winged Drosophila because these species are so difficult to rear and maintain in the laboratory. However, two such experiments have been performed, both of which showed that laboratory founder-flush events lead to the rapid evolution of premating isolation. One is the work of Arita and Kaneshiro (1979), which was not included in the literature review of Rice and Hostert (1993). The other was the work of Ahearn (1980), which was included in their review, but not in the section on bottleneck-induced speciation. Moreover, the work of Ahearn (1980) was dismissed by Rice and Hostert (1993) on the basis of a reanalysis indicating a lack of statistical significance using an unspecified 2 x 2 contingency test. There is only one data table in Ahearn (1980), and it is in the form of a 2 x 2 table. The Pearson [[Chi].sup.2] statistic for this table is 19.92 with 1 df (P [less than] 0.0005), a Yates corrected [[Chi].sup.2] is 17.63 (P [less than] 0.0005), and a two-tailed Fisher exact test yields a P [less than] 0.0005. These highly significant results clearly document a rapid evolution of mating asymmetries that mimic exactly the same type of asymmetries found in natural speciation events for this group of Drosophila. Mating asymmetries are not a general feature of speciation (Giddings and Templeton 1983; DeSalle and Templeton 1987), but their validity in Hawaiian picture wings is well established (Kaneshiro 1976, 1980, 1990; Kaneshiro and Kurihara 1981). Hence, it is inappropriate both statistically and biologically to pool across the sexes when looking at reproductive isolation in this group. Accordingly, Ahearn (1980) did not pool, but rather documented strong reproductive isolation in the only crosses predicted to show such isolation; namely, derived males with ancestral females. The Stalker index of isolation in this case was 0.78 (-1 corresponds to complete disassortative mating, 0 to random mating, and +1 to complete assortative mating or isolation). Ahearn reported that this isolation index was significant at the 0.01 level. In light of Rice and Hostert's claims of no significant isolation, I recalculated this index and its statistical test from the raw data and obtained Ahearn's original results. A Stalker index of 0.78 represents strong premating isolation that is comparable quantitatively to that seen in natural speciation events in this group (Kaneshiro 1976). Hence, Ahearn's experiments mimic both qualitatively and quantitatively the alterations of mating behavior that are observed in cases of natural speciation associated with trans-island founding events in Hawaiian Drosophila.
Third, Carson and Templeton (1984) cited work performed on captive populations of endangered species, which are often founded by small numbers of individuals. Since the publication of Carson and Templeton (1984), additional work with the captive herd of Speke's gazelle (founded with one male and three females) has provided strong support for an interaction among selection, recombination, and founder effects (Templeton and Read 1994) and for the prediction that founder effects under the conditions described by the founder-flush and genetic-transilience models do not result in a major reduction of nuclear DNA variation although they can have a drastic effect on mitochondrial DNA (mtDNA) variation (Templeton et al. 1987). This confirms major predictions of the genetic transilience theory (Templeton 1980, 1987).
The literature that Rice and Hostert (1993) cite in favor of selection facilitating speciation via pleiotropy and/or hitchhiking is also germane to genetic transilience speciation. It is well known that genetic bottlenecks induce linkage disequilibrium and hence accentuate hitchhiking effects, but one of the counterintuitive predictions of the genetic-transilience theory (Templeton 1980, p. 1015-1016) was that the founder effect would cause epistatic interactions (in the gene action sense, not the quantitative genetic concept of epistatic variance) to make many gene loci more responsive to selection after the founder effect (that is, the gene action epistasis is converted into increased additive genetic variance by the founder effect). Given that this is the major genetic mechanism put forward to explain genetic transilience (Templeton 1980) and, as mentioned earlier, has supporting quantitative genetic theory (Goodnight 1988; Wagner et al. 1994), the experimental evidence for this prediction should not be ignored. The weaker experimental support for this counterintuitive prediction is found in the extensive literature on isofemale stocks, particularly in the Drosophila literature. Most females collected from nature are already inseminated, and isofemale stocks are established from a large number of offspring from a single wild-caught female. This mimics the role of single gravid females and the subsequent population flush in genetic transilience and founder-flush speciation models (Carson and Templeton 1984). Unfortunately, most of this literature deals with standard laboratory organisms that are not expected to yield drastic evolutionary changes (Templeton 1980; Carson and Templeton 1984). Nevertheless, an amazing amount of genetic variability for virtually every character or trait that has been studied has been documented by these experiments (see the following articles and books for reviews of this extensive literature: Parsons 1980; Ehrman and Parsons 1981a; Hoffmann and Parsons 1993), including the trait of reproductive isolation (Ehrman and Parsons 1981b). Although this literature documents that founder events can reveal large amounts of genetic variation for virtually any trait even when that variation is not apparent in the ancestral populations, it did not directly quantify the amount of additive variance before and after the bottleneck. However, a large number of experiments have now shown directly that bottlenecks do indeed increase additive genetic variation for a wide variety of traits (Lints and Bourgois 1984; Bryant et al. 1986a,b; Bryant and Meffert 1990, 1991, 1992; Carson and Wisotzkey 1989; Terzian and Biemont 1988). None of these papers were cited by Rice and Hostert (1993), but they provide repeated experimental confirmation for the major theoretical underpinning of the genetic-transilience model.
This body of experimental evidence implies that bottlenecks can induce and accentuate selective response and hitchhiking effects, precisely the same microevolutionary processes that Rice and Hostert (1993) feel are strongly documented as being necessary and sufficient for speciation. There is no obvious mechanism for why these processes would not lead to speciation when they are accentuated or triggered by founder effects but would lead to speciation in the absence of such an accentuating/triggering effect. Rice and Hostert (1993) do acknowledge that "bottlenecks may facilitate ... but not cause the speciation process" (p. 1647). However, no criteria are given for discriminating between mechanisms that "facilitate" versus mechanisms that "cause" speciation. Such a distinction probably cannot be made and is misleading because it equates speciation mechanisms with speciation processes. As pointed out by Templeton (1981), mechanisms are distinct from processes. For example, the shifting-balance theory of Wright attempts to explain the process of adaptation by combining the effects and interactions of several distinct microevolutionary mechanisms; namely, natural selection, genetic drift, and differential gene flow (Templeton 1982). Similarly, a single process of speciation could be affected by a variety of speciation mechanisms and their interactions (Templeton 1981). This mechanistic approach avoids the sterile debate about facilitation versus cause.
In summary, the strong statements made by Rice and Hostert (1993) about the absence of experimental evidence for genetic transilience are not justified by a more thorough examination of the relevant literature, by using uniform criteria for evaluation, and by discriminating between founder events that should facilitate speciation versus those that should not (using criteria that were published prior to most of the experimental investigations). Quite the contrary, the experimental evidence for genetic transilience and its critical mechanistic predictions and underpinnings is strong and extensive. The common assertion that there is little or no support for the genetic transilience model of speciation is no longer tenable.
This work was supported by grant R01 GM31571 from the National Institutes of Health. I wish to thank A. Larson and D. Futuyma for their excellent comments and suggestions on an earlier version of this note.
AHEARN, J. N. 1980. Evolution of behavioral reproductive isolation in a laboratory stock of Drosophila silvestris. Experientia 36:63-64.
ANNEST, J. L., AND A. R. TEMPLETON. 1978. Genetic recombination and clonal selection in Drosophila mercatorum. Genetics 89:193-210.
ARITA, L. H., AND K. Y. KANESHIRO. 1979. Ethological isolation between two stocks of Drosophila adiastola Hardy. Proceedings of the Hawaiian Entomological Society 12:31-34.
BRYANT, E. H., AND C. M. MEFFERT. 1990. Multivariate phenotypic differentiation among bottleneck lines of the housefly. Evolution 44:660-668.
-----. 1991. The effects of bottlenecks on genetic variation, fitness, and quantitative traits in the housefly. Pp. 591-601 in E. C. Dudley, eds. The unity of evolutionary biology. Dioscorides Press, Portland, OR.
-----. 1992. The effect of serial founder-flush cycles on quantitative genetic variation in the housefly. Heredity 70:122-129.
BRYANT, E. H., L. M. COMBS, AND S. A. McCOMMAS. 1986a. Morphometric differentiation among experimental lines of the housefly in relation to a bottleneck. Genetics 114:1213-1223.
BRYANT, E. H., S. A. McCOMMAS, AND L. M. COMBS. 1986b. The effect of an experimental bottleneck upon quantitative genetic variation in the housefly. Genetics 114:1191-1211.
CARSON, H. L., AND A. R. TEMPLETON. 1984. Genetic revolutions in relation to speciation phenomena: The founding of new populations. Ann. Rev. Ecol. Syst. 15:97-131.
CARSON, H. L., AND R. G. WISOXZKEY. 1989. Increase in genetic variance following a population bottleneck. Am. Nat. 134:668-671.
CHARLESWORTH, B., R. LANDE, AND M. SLATKIN. 1982. A neo-Darwinian commentary on macroevolution. Evolution 36:474-498.
DESALLE, R., AND A. R. TEMPLETON. 1987. Comments on "The significance of asymmetrical sexual isolation." Evol. Biol. 21:2127.
DODD, D. M. B., AND J. R. POWELL. 1985. Founder-flush speciation: An update of experimental results with Drosophila. Evolution 39: 1388-1392.
EHRMAN, L., AND P. A. PARSONS. 1981a. Behavior genetics and evolution. McGraw-Hill, New York.
-----. 1981b. Sexual isolation among isofemale strains within a population of Drosophila immigrans. Behav. Genet. 11:127-133.
FUYAMA, Y. 1986. Genetics of parthenogenesis in Drosophila melanogaster. I. The modes of diploidization in the gynogenesis induced by a male sterile mutant, ms(3)K81. Genetics 112:237-248.
GALIANA, A., A. MOYA, AND F. J. AYALA. 1993. Founder-flush speciation in Drosophila pseudoobscura - a large-scale experiment. Evolution 47:432-444.
GIDDINGS, L. V., AND A. R. TEMPLETON. 1983. Behavioral phylogenies and the direction of evolution. Science 220:372-378.
GOODNIGHT, C. J. 1988. Epistasis and the effect of founder events on the additive genetic variance. Evolution 42:441-454.
HEDGES, L. V., AND I. OLKIN. 1985. Statistical methods for meta-analysis. Academic Press, Orlando, FL.
HOFFMANN, A. A., AND P. A. PARSONS. 1993. Evolutionary genetics and environmental stress. Oxford University Press, Oxford.
HOLLOCHER, H., AND A. R. TEMPLETON. 1994. The molecular through ecological genetics of abnormal abdomen in Drosophila mercatorum VI. The nonneutrality of the Y-chromosome rDNA polymorphism. Genetics 136:1373-1384.
HOLLOCHER, H., A. R. TEMPLETON, R. DESALLE, AND J. S. JOHNSTON. 1992. The molecular through ecological genetics of abnormal abdomen. IV. Components of genetic variation in a natural population of Drosophila mercatorum. Genetics 130:355-366.
KANESHIRO, K. Y. 1976. Ethological isolation and phylogeny in the planitibia subgroup of Hawaiian Drosophila. Evolution 30:740-745.
-----. 1980. Sexual isolation, speciation and the direction of evolution. Evolution 34:437-444.
-----. 1990. Natural hybridization in Drosophila, with special reference to species from Hawaii. Can. J. Zool. 68:1800-1805.
KANESHIRO, K. Y., AND J. S. KURIHARA. 1981. Sequential differentiation of sexual behavior among populations of Drosophila silvestris. Pac. Sci. 35:177-183.
LINTS, F. A., AND M. BOURGOIS. 1984. Population crash, population flush and genetic variability in cage populations of Drosophila melanogaster. Genet., Sel., Evol. 16:45-56.
MAYR, E. 1970. Populations, species, and evolution. The Belknap Press of Harvard University Press, Cambridge, MA.
-----. 1982. Processes of speciation in animals. Pp. 1-19 in C. Barigozzi, ed. Mechanisms of speciation. Alan R. Liss, New York.
PARSONS, P. A. 1980. Isofemale strains and evolutionary strategies in natural populations. Evol. Biol. 13:175-217.
POWELL, J. R. 1978. The founder-flush speciation theory: An experimental approach. Evolution 32:465-474.
RICE, W. R., AND E. E. HOSTERT. 1993. Laboratory experiments on speciation: What have we learned in 40 years? Evolution 47:1637-1653.
RICE, W. R., AND G. W. SALT. 1990. The evolution of reproductive isolation as a correlated character under sympatric conditions: Experimental evidence. Evolution 44:1140-1152.
RINGO, J., D. WOOD, R. ROCKWELL, AND H. DOWSE. 1985. An experiment testing two hypotheses of speciation. Am. Nat. 126:642-661.
SENNER, J. W. 1980. Inbreeding depression and the survival of zoo populations. Pp. 209-224 in M. E. Soule and B. A. Wilcox, eds. Conservation biology: An evolutionary-ecological perspective. Sinauer, Sunderland, MA.
TEMPLETON, A. R. 1974. Analysis of selection in populations observed over a sequence of consecutive generations. I. Some one locus models with a single, constant fitness component per genotype. Theor. Appl. Genet. 45:179-191.
-----. 1979a. The unit of selection in Drosophila mercatorum. II. Genetic revolution and the origin of coadapted genomes in parthenogenetic strains. Genetics 92:1265-1282.
-----. 1979b. The parthenogenetic capacities and genetic structures of sympatric populations of Drosophila mercatorum and Drosophila hydei. Genetics 92:1283-1293.
-----. 1980. The theory of speciation via the founder principle. Genetics 94:1011-1038.
-----. 1981. Mechanisms of speciation - A population genetic approach. Ann. Rev. Ecol. Syst. 12:23-48.
-----. 1982. Adaptation and the integration of evolutionary forces. Pp. 15-31 in R. Milkman, ed. Perspectives on evolution. Sinauer, Sunderland, MA.
-----. 1983. Natural and experimental parthenogenesis. Pp. 343-398 in M. Ashburner, H. L. Carson, and J. N. Thompson, eds. The genetics and biology of Drosophila. Academic Press, London.
-----. 1987. Genetic systems and evolutionary rates. Pp. 218-234 in K. S. W. Campbell and M. F. Day, eds. Rates of evolution. Allen and Unwin, London.
-----. 1989. Founder effects and the evolution of reproductive isolation. Pp. 329-344 in L. V. Giddings, K. Y. Kaneshiro, and W. W. Anderson, eds. Genetics, speciation, and the founder principle. Oxford University Press, Oxford.
TEMPLETON, A. R., AND B. READ. 1994. Inbreeding: One word, several meanings, much confusion. Pp. 91-106 in V. Loeschcke, J. Tomiuk, and S. K. Jain, eds. Conservation genetics. Birkhauser-Verlag, Basel, Switzerland.
TEMPLETON, A. R., C. F. SING, AND B. BROKAW. 1976. The unit of selection in Drosophila mercatorum. I. The interaction of selection and meiosis in parthenogenetic strains. Genetics 82:349-376.
TEMPLETON, A. R., T. J. CREASE, AND F. SHAH. 1985. The molecular through ecological genetics of abnormal abdomen in Drosophila mercatorum. I. Basic genetics. Genetics 111:805-818.
TEMPLETON, A. R., S. K. DAVIS, AND B. READ. 1987. Genetic variability in a captive herd of Speke's gazelle (Gazella spekei). Zoo Biol. 6:305-313.
TEMPLETON, A. R., H. HOLLOCHER, S. LAWLER, AND J. S. JOHNSTON. 1989. Natural selection and ribosomal DNA in Drosophila. Genome 31:296-303.
-----. 1990. The ecological genetics of abnormal abdomen in Drosophila mercatorum. Pp. 17-35 in J. S. F. Barker, eds. Ecological and evolutionary genetics of Drosophila. Plenum Press, New York.
TEMPLETON, A. R., H. HOLLOCHER, AND J. S. JOHNSTON. 1993a. The molecular through ecological genetics of abnormal abdomen in Drosophila mercatorum. V. Female phenotypic expression on natural genetic backgrounds and in natural environments. Genetics 134:475-485.
-----. 1993b. The molecular through ecological genetics of abnormal abdomen in Drosophila mercatorum. V. Female phenotypic expression on natural genetic backgrounds and in natural environments. Genetics 134:475-485.
TERZIAN, C., AND C. BIEMONT. 1988. The founder effect theory: Quantitative variation and the MDG-1 mobile element polymorphism in experimental populations of Drosophila melanogaster. Genetica 76:53-63.
WAGNER, A., G. P. WAGNER, AND P. SIMILION. 1994. Epistasis can facilitate the evolution of reproductive isolation by peak shifts: A two-locus two-allele model. Genetics 138:533-545.
|Printer friendly Cite/link Email Feedback|
|Title Annotation:||Brief Communications; comment on W.R. Rice and E.E. Hostert, Evolution, v. 47, p. 1637|
|Author:||Templeton, Alan R.|
|Date:||Apr 1, 1996|
|Previous Article:||Mating system and asymmetric hybridization in a mixed stand of European oaks.|
|Next Article:||Transmission rates and the evolution of HIV virulence.|