How genes causing unfit hybrids evolve within populations: a review of models of postzygotic isolation

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1 Popul Ecol (2002) 44: The Society of Population Ecology and Springer-Verlag Tokyo 2002 SPECIAL FEATURE: REVIEW Takehiko I. Hayashi Masakado Kawata How genes causing unfit hybrids evolve within populations: a review of models of postzygotic isolation Received: February 7, 2002 / Accepted: October 17, 2002 Abstract The main subject for models of postzygotic isolation has been how reproductive isolation genes (RI genes) which cause hybrid inviability or sterility spread within populations despite their deleterious effects. The models are divided into three categories according to the withinpopulation effect of RI genes in their fixation process. (1) The beneficial effect model, where RI genes are assumed to spread within populations by a positive selective force via natural or sexual selection. (2) The neutral effect model, where RI genes are assumed not to affect the fitness of individuals in their fixation process and to be spread by genetic drift. (3) The deleterious effect model, where RI genes are assumed to exhibit some (slightly) deleterious effects in their fixation process and to be spread by genetic drift. Factors that affect the applicability of these models are discussed. If a selective force such as sexual conflict or natural selection facilitates the evolution of RI genes, the beneficial effect model should be applied. Many empirical studies have suggested that positive selection plays an important role in the evolution of hybrid male sterility. If the mutation rates of RI genes are low, and the specificity of epistatic interaction causing hybrid inviability or sterility is high, the neutral effect model should be applied. However, if the opposite condition applies, the deleterious effect model should be applied. Key words Speciation Reproductive isolation Mathematical model Postmating isolation Genetics of speciation T.I. Hayashi (*) Department of Ecology and Evolutionary Biology, Biological Institute, Graduate School of Science, Tohoku University, Sendai , Japan Tel ; Fax takehiko@biology.tohoku.ac.jp M. Kawata Division of Ecology and Evolutionary Biology, Graduate School of Life Sciences, Tohoku University, Sendai, Japan Introduction Speciation is completed by reproductive isolation (RI) that prevents gene flow between populations. Once genetically isolated, those populations can evolve as independent evolutionary units. Thus, reproductive isolation plays an important role in the creation of irrevocable genetic subdivisions, which lead to biodiversity. Reproductive isolation is effective either (a) before fertilization or zygote formation (prezygotic isolation) due to barriers such as courtship differences, or (b) after fertilization or zygote formation (postzygotic isolation) due to barriers such as hybrid inviability or sterility. Traits causing prezygotic isolation can often be adaptive, because such isolation can reduce or avoid the risk of a mating that would produce unfit offspring. Thus, natural selection can create prezygotic isolation, which is known as reinforcement (Dobzhansky 1937; Bush 1994; Liou and Price 1994; Butlin 1995; Kelly and Noor 1996; Servedio and Kirkpatrick 1997; Partridge and Parker 1999; Cain et al. 1999; Noor 1999; Kirkpatrick 2000; Servedio 2000). On the other hand, traits causing postzygotic isolation rarely reduce costs. This implies that postzygotic isolation generally has no adaptive advantage; an exception is the case when hybrid inviability reduces the cost of parental investment (Coyne 1976). Thus, prezygotic isolation would be more important than postzygotic isolation in sympatric and parapatric speciation in which prezygotic isolation can evolve through natural selection. However, postzygotic isolation, which is involved in most speciation events, is also important when considering speciation. Coyne and Orr (1989, 1997) have shown that prezygotic and postzygotic isolation increase at about the same rate between allopatric populations. Several recent analyses suggest that many speciation events are allopatric (e.g., Barraclough and Vogler 2000). Even if sympatry and parapatry are the result of secondary contact, the possibility of reinforcement strongly depends on the degree of postzygotic isolation that has evolved in the allopatric stage (e.g., Liou and Price 1994; Servedio and Kirkpatrick 1997).

2 158 The basic idea of a postzygotic isolation model was proposed in the foundation of the modern synthesis. Bateson (1909), Dobzhansky (1937), and Muller (1942) expressed the idea that speciation arises as a by-product of independent divergence between populations (the Dobzhansky Muller model; see next section). However, subsequent to their proposals, many theoretical studies focused more on speciation by the founder effect or by peak shift than on the Dobzhansky Muller model. These studies have shown that the range of conditions that can give rise to speciation by the founder effect or peak shift is generally limited (for a review, see Barton and Charlesworth 1984). Recently, stimulated by progress in empirical genetic studies, many theoretical models elaborating the Dobzahnsky Muller model have been proposed (Table 1). Although the history of genetic studies on postzygotic isolation can be traced back to Dobzhansky s pioneering work (Dobzhansky 1936), detailed genetic analysis of postzygotic isolation has been made possible by recent progress in molecular biological techniques. We now have considerable information on the location and interaction of genes involved in hybrid incompatibility (Wu and Hollocher 1998; Naveira and Maside 1998; Sawamura 1999, 2000; Orr and Presgraves 2000). This article reviews an issue in modeling postzygotic isolation, namely, the within-population effects of genes that cause hybrid inviability or sterility. (In the following sections, for purposes of simplification, we call such genes RI genes.) The examination of how incompatibility genes spread within populations, despite their deleterious effects, has been a major subject of models of postzygotic isolation (Barton and Charlesworth 1984; Orr 1996; Gavrilets 1997). Because the evolutionary dynamics of postzygotic isolation greatly depend on the deleterious (or beneficial) effects of the incompatibility genes within populations, it is important to understand how their within-population effects affect the dynamics of the RI genes. In this review, we first introduce the idea of the Dobzhansky Muller model as a basic model of postzygotic isolation. We then classify the recent extension of the model into three categories according to the within-population effect of genes that cause hybrid inviability or sterility, and discuss factors that affect the applicability of the models. Finally, empirical findings supporting the assumptions of the models are discussed. Basic idea: the Dobzhansky Muller model The evolution of postzygotic isolation seems to be difficult because it includes the evolution of maladaptive traits such as inviability or sterility. The Dobzhansky Muller model explains how populations become reproductively isolated without passing through a stage with such unfit traits, by assuming that epistatic interaction between loci causes the inviability or sterility (Fig. 1). Suppose that an ancestral population had genotype aabb, and that genotype AaBb is inviable or sterile (capital letters denote derived alleles). If Aabb and AAbb genotypes are perfectly fit, a new mutation Fig. 1. The Dobzhansky Muller model. Postzygotic isolation is easily achieved if genetic compatibility is the consequence of epistastic interaction. The genotype of the ancestral population is aabb. The hybrid whose genotype is AaBb is assumed to be inviable or sterile. Here, a and b represent original alleles, and A and B represent derived alleles. Suppose the alleles A and B are fixed in different isolated populations. When these two descendant populations (AAbb and aabb) come into contact, the resulting hybrid (AaBb) is inviable or sterile. In this scenario, reproductive isolation evolves, but not through a maladaptive individual whose genotype is AaBb at one locus (allele A) could become fixed by selection or drift within an isolated population. Similarly, a new mutation at another locus (allele B) could become fixed within another population. If these two populations (AAbb and aabb) come into contact, the resulting hybrids are inviable or sterile (AaBb). In this scenario, reproductive isolation evolves without selection against the maladaptive individuals whose genotype is AaBb. The most important feature of this model is that the deleterious effects which appear in genetic interactions between populations (i.e., hybrid sterility or inviability) do not affect the processes of fixation (and substitutions) of the genes within populations. This model postulates that gene interaction within populations can be independent of those between populations. In the following section, we briefly review previous models of postzygotic isolation with regard to the within-population effects of RI genes. Three types of models There are three types of models of postzygotic isolation with regard to the within-population effects of genes that contribute to hybrid inviability or sterility. 1. Beneficial effect model. This type of model assumes that RI genes spread within populations by a positive selective force via natural or sexual selection (see Table 1). The effect of RI genes within a population is assumed to be approximately independent of that between populations. The evolutionary dynamics of RI genes essentially depends on assumed selective forces within populations. If RI genes are responsible for local adaptation or sexual conflict, their fixation would be enhanced in an advantageous habitat (Gavrilets 2000) or by multiple

3 159 mating of females (Kondoh and Higashi 2000), respectively. 2. Neutral effect model. This type of model assumes that RI genes do not affect the fitness of individuals in their fixation process and are spread by genetic drift (see Table 1). The effect of deleterious genetic interactions between populations, which create inviable or sterile genotypes, is assumed to be ignorable within a population. The conditions under which the effect can be ignored are discussed later. 3. Deleterious effect model. RI genes are assumed to exhibit some (slightly) deleterious effects, which are caused either by the additive effects of RI genes or by their epsitatic gene interaction in their fixation process. RI genes are assumed to be spread by genetic drift. Recently, this type of model usually assumes that the within-population deleterious effect is caused by their epistatic gene interaction that creates inviable or sterile genotypes (see Table 1). The inviability or sterility of hybrids (i.e., offspring from mating between populations) is often assumed to be determined by the difference between two trait values in the individuals (Nei et al. 1983; Johnson and Porter 2000; Hayashi and Kawata 2001). Inviable or sterile genotypes can also arise in a population by the same genetic interactions as those which arise in hybridization. Because the deleterious effect of RI genes appears through such unfit genotypes, selection pressure against RI genes within populations depends on the frequency of such unfit genotypes within populations (i.e., the genetic load due to the RI genes). RI genes behave like slightly deleterious (or underdominant) mutations and spread by genetic drift within populations when the frequency of such unfit genotypes within populations is low (i.e., the genetic load due to the RI gene is small) (e.g., Gavrilets 1999; Hayashi and Kawata 2001). These three types of model essentially lead to different evolutionary dynamics of postzygotic isolation. In the deleterious effect model, a large population size greatly retards the evolution of postzygotic isolation (e.g., Nei et al. 1983; Gavrilets 1999; Hayashi and Kawata 2001). Conversely, the neutral effect model predicts that population size does not affect the evolutionary rates of postzygotic isolation (e.g., Orr and Orr 1996) because neutral fixation does not depend on population size (Kimura 1983). In the beneficial effect model, the prediction of evolutionary rates essentially depends on parameters that affect the intensity of positive selection rather than on population size itself (e.g., Gavrilets 2000; Hayashi and Kawata 2001). Factors affecting the effects of RI genes within populations If selective forces such as sexual conflict or natural selection enhance the fixation of RI genes, the beneficial effect model should be applied. Otherwise, either the neutral effect model or the deleterious effect model should be applied. When the possibility that RI genes will produce inviable or sterile genotypes within a population is rare, the RI genes are less likely to be subjected to negative selection. In such a case, the neutral effect model should be applied. Conversely, if this possibility is rather high, the deleterious effect model should be applied. The frequency of inviable or sterile genotypes within populations decreases as mutation rates of RI genes decrease (Gavrilets 1999). The frequency also decreases with the increasing specificity of epistatic interaction for postzyogtic isolation (i.e., a case where special combinations of alleles of multiple loci are required for unfit genotypes). Thus, if mutation rates are low and the specificity of epistatic interaction is high, the neutral effect model should be applied. If the situation is the converse, the deleterious effect model should be applied. The specificity of epistatic interaction may increase with an increasing number of loci required for postzygotic isolation, because a more complex epistatic combination is required to cause inviability or sterility when the number of loci is large (cf., Orr 1995; Gavrilets 1997). If interactions between a derived allele and an ancestral allele at the same locus cause hybrid inviability or sterility, genotypes with deleterious effects may frequently arise in the fixation process of the derived allele, where the deleterious effect model is applicable. The effect of RI genes within populations retards their spread in the populations. If we postulate allelic incompatibility between a and A (a capital letter denotes a derived allele), genotype aa and AA are reproductively isolated. However, genotype Aa will inhibit the spread of A within populations. Postzygotic isolation due to allelic interaction within loci is frequently assumed in the models of speciation by a founder effect or peak shift (e.g., Wagner et al. 1994; Gavrilets and Hastings 1996). However, few studies on a genetic analysis of postzygotic isolation have shown that allelic interaction within a locus contributes to hybrid inviability or sterility (see Wu and Palopoli 1994 for a review). Empirical findings on the effect of RI genes within populations Selective forces Recent studies have suggested that positive selection for RI genes is responsible for the evolution of hybrid male sterility, e.g., a candidate gene for hybrid male sterility of Drosophila, called Odysseus (Ting et al. 1998). Many studies have also suggested that sexual selection or sexual conflict enhances the evolution of genes affecting male reproductive characters, and may result in the evolution of hybrid male sterility (Nurminsky et al. 1998; Tsaur et al. 1998). Nevertheless, few empirical studies have attempted to demonstrate the selective forces in the evolution of hybrid inviability and female sterility. Some studies have suggested that genetic divergence driven by natural selection pro-

4 160 Table 1. List of theoretical models for postzygotic (postmating) isolation References Type of model Evolutionary Form of gene Gene Main concern Main results of the effect of force for interaction between interaction RI genes within population populations within/ populations a divergence b (fitness function) between populations c Nei (1976) d Beneficial, Natural Epistatic interaction Same Mathematical The Dobzhansky Muller model is first shown as a possible deleterious selection, between two loci formulation of the model of postzygotic isolation genetic drift Dobzahnsky Muller model Nei et al. Deleterious Genetic drift Truncation selection Same Temporal pattern of Postzygotic isolation can be achieved only by mutation and (1983) d that depends on the speciation drift. Reproductive isolation evolves faster in small difference between populations than in large populations two trait values Wagner et al. Deleterious Genetic drift Epistatic interaction Same Effect of epistatic With epistatic characters, there is no consistent relationship (1994) d between two loci, interaction in between the probability of peak shift and the degree of allelic interaction speciation by peak the resulting reproductive isolation shift Orr (1995) Not specified Not specified Epistatic interactions Different Temporal pattern of The number of incompatibilities contributing to postzygotic among loci speciation isolation increases at a rate faster than the square of time ( the snowball effect ) Gavrilets and Deleterious Genetic drift Epistatic interaction Same Effect of epistatic If appropriate parameter values are postulated, reproductive Hasting among mutliloci, interaction in isolation can evolve with a high probability within dozens (1996) d allelic interaction speciation by or hundreds of generations founder effect Orr and Orr Beneficial, Natural selection, Epistatic interactions Different Temporal pattern of The degree of subdivision of ancestral populations does not (1996) neutral genetic drift among loci speciation, population affect the waiting time for speciation by genetic drift, but structure affects that by natural selection Gavrilets and Deleterious Genetic drift Truncation selection Same Structure and property Reproductive isolation between populations easily evolves Gravner that depends on each of holey adaptive as a side-effect of accumulating different mutations (1997) d genotype landscape under a holey adaptive landscape Gavrilets et al. Deleterious Genetic drift Truncation selection Same Temporal and spatial Genetic drift facilitates rapid speciation without extreme (1998) d that depends on the pattern of speciation founder effects or complete loss of gene flow genetic distance e Gavrilets Deleterious, Natural selection, Truncation selection Same Mathematical Rapid speciation is a plausible outcome of the evolutionary (1999) d beneficial genetic drift that depends on the formulation of holey dynamics of subdivided populations. Rapid speciation genetic distance e adaptive landscape is most likely to occur in populations that are subdivided model into a large number of small populations Lynch and Not specified Not specified Epistatic interaction Same Effect of gene Gene duplication, or more generally any kind of genomic Force between loci duplication as the redundancies, provides a powerful substrate for the (2000) d origin of genetic origin of genomic incompatibility in isolated populations incompatibility Gavrilets Deleterious, Natural selection, Truncation selectin Different Temporal pattern of Even relatively weak selection for local adaptation can (2000) d beneficial genetic drift that depends on the parapatric speciation, dramatically decrease the waiting time to speciation genetic distance e local adaptation

5 161 Gavrilets et al. Deleterious Genetic drift Truncation selection Same Temporal and spatial The spatial pattern across which populations become (2000a) d that depends on the pattern of speciation, isolated depends on mutation rates, local densities of genetic distance e population structure populations, and the degree of genetic changes required for reproductive isolation Gavrilets et al. Deleterious, Natural selection, Truncation or linear Different Temporal and spatial The dynamics of species border and the distribution of (2000b) d beneficial genetic drift selection that dynamics of species range size are shown depends on the speciation, genetic distance e metapopulation dynamics Johnson and Deleterious, Natural Exponential function Same Condition for speciation Parallel and directional selection can result in speciation, Porter beneficial selection, that depends on the due to the divergence but genetic drift alone cannot. Hybrid fitness reduction (2000) drift difference between on gene regulatory occurs more often as the number of loci in the pathway two traits system increase, but and as the binding site interactions become more complex Kondoh and Beneficial Sexual conflict Function that depends Gene Mathematical The difference in population-specific balance among factors Higashi on evolutionary interaction formulation for that are involved in the optimal offspring size (such as (2000) conflict between between speciation due to production costs of growth factors and paternity) results two traits populations is intragenomic sexual in postzygotic isolation not specified conflict Hayashi and Deleterious, Genetic drift, Truncation selection Same Temporal pattern of The dynamics of speciation due to three possible genetic Kawata beneficial sexual selection that depends on the speciation, difference mechanisms are shown. Sexual selection facilitates (2001) difference between of genetic interactions speciation two trait values. Epistatic interaction due to the combination of alleles Orr and Beneficial type, Natural selection, Epistatic interactions Different Temporal pattern of The distribution of the number of incompatibilities as a Turelli neutral genetic drift among loci speciation, function of divergence time and that of waiting time for (2001) stochastic factors speciation are derived Hayashi and Deleterious Genetic drift Truncation selection Same Population structure, The mutation selection drift equilibrium of ancestral Kawata that depends on the temporal pattern of populations largely affects the dynamics of postzygotic (submitted) number of mutations speciation isolation among its descendant populations a Beneficial (neutral/deleterious) means the type of model that assumes that RI genes (that contribute to hybrid inviability or sterility) spread by positive selective forces (are neutral/show some deleterious effects) within populations (see text for details) b Mutation as an evolutionary force is not specified in the list because it is assumed by all models as a premise of evolution c Same/different means the case in which the form of genetic interaction (i.e., fitness function) within a population is the same as/different from that between populations d Models are not specific to postzygotic (postmating) isolation e Genetic distance is defined as the number of loci at which two parental individuals are different

6 162 motes extrinsic postzygotic isolation (i.e., a decrease of hybrid fitness due to poor adaptation to the environment) (Schluter 1998, 2001), but whether natural selection promotes the evolution of intrinsic postzygotic isolation (i.e., hybrid inviability or sterility) is still unclear (e.g., Rundle 2002). Specificity of epistatic interaction Introgression analysis using the Drosophila melanogaster subgroup showed that hybrid male sterility is often caused by polygenic (e.g., 5 loci) epistatic interaction (Cabot et al. 1994; Naveira and Maside 1998; Wu and Hollocher 1998). On the other hand, hybrid female sterility may be caused by a single gene with major effect (Sawamura et al. 2002). Thus, the specificity of epistatic interactions may be higher in male reproduction than in female reproduction. The effect of inviable or sterile genotypes within populations It is difficult to measure directly the mutation rates and the specificity of epistatic interaction (i.e., the ratio of the number of inviable or sterile genotypes to the total number of possible genotypes in the loci that contribute to the unfit genotypes) leading to inviability or sterility. However, it may be possible to estimate the frequency of inviable or sterile genotypes formed by RI genes in natural populations. If we can detect any within-population deleterious effect of genes that actually cause hybrid inviability or sterility in natural populations, the frequency of the unfit genotypes within populations (i.e., genetic load due to RI genes) may not be small. Wade and Johnson (1994) and Wade et al. (1997) examined traits observed in hybrids (hybrid numbers, hybrid sex ratios, and hybrid male deformities) between two species of flour beetles, Triborioum castaneum and T. freeman. They found within-species genetic variation for these hybrid traits. When sires from T. castaneum are mated to conspecific and heterospecific females, they observed no significant correlation at the level of the family mean between the intraspecific and interspecific phenotypes (productivity, sex ratio, male deformities, and adult dry weights) (Wade et al. 1997). This suggested that the effects of RI genes between species (populations) do not appear within species (populations). However, there is one important caveat: it may be difficult to detect the effects of RI genes within populations because the frequency of inviable or sterile genotypes must be low when the populations are at equilibrium due to mutation and selection. In fact, Gavrilets (1999) showed analytically that the equilibrium frequency of the unfit genotypes within populations is very low (the genetic load is about ). Although these values of genetic load are sufficiently large to affect the fixation of RI genes, a considerable sample size is required to detect any small effect. Conclusion We have discussed the models of postzytogtic isolation, especially with regard to the within-population effects of reproductive isolation genes (RI genes) that cause hybrid inviability or sterility. There are several factors affecting assumptions as to the effect of RI genes within populations. (1) If a selective force such as sexual conflict or natural selection facilitates the evolution of RI genes, the beneficial effect model should be applied. This type of model assumes that RI genes spread within populations by a positive selective force. Many empirical studies have suggested that positive selection plays an important role in the evolution of hybrid male sterility. (2) If the mutation rates of the genes for hybrid inviability or sterility are low and the specificity of epistatic interaction for that is high, the neutral effect model should be applied. This type of model assumes that RI genes do not affect the fitness of individuals in their fixation process and are spread by genetic drift. Conversely, if the condition is the reverse, the deleterious effect model should be applied. This type of model assumes that selection against inviable or sterile genotypes within a population affects the fixation process of RI genes. Although there is little empirical evidence, there is a possibility that the frequency of these genotypes is sufficiently high to affect the fixation process of RI genes, but too low to permit the detection of such an effect in natural populations. Further experimental studies should be conducted. 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