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Opinion TRENDS in Ecology and Evolution Vol.20 No.7 July 2005 ‘Haldane’s Sieve’ in a metapopulation: sifting through plant reproductive polymorphisms John R. Pannell1, Marcel E. Dorken1 and Sarah M. Eppley1,2 1 2 Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, UK, OX1 3RB Current address: Department of Biological Sciences, Victoria University of Wellington, PO Box 600, Wellington, New Zealand An important result of population genetics is that advantageous mutations will be fixed by selection in a population with a greater probability if they are dominant rather than recessive. This selective filter on new variants entering a population, termed ‘Haldane’s Sieve’, has hitherto been invoked to account for the greater role of dominant than completely recessive mutations in adaptive evolution. Here, we suggest that a process similar to Haldane’s Sieve will act on migrants into subpopulations of a metapopulation, and that the repeated action of Haldane’s Sieve on alleles maintained by frequency-dependent selection, such as those responsible for many plant reproductive polymorphisms, is expected to bias their frequency distribution in favour of dominant alleles. The genetic and phenotypic signatures left by these processes might provide additional indirect support for the contentious idea that metapopulation dynamics have had an important role in shaping the ecology and evolution of some plant species. Evolutionary models of a wide range of life-history, mating-system and behavioural phenomena in plants and animals are often expressed solely in terms of the phenotypes involved without regard to the underlying genetic mechanisms. Although such models ignore all genetic details, they often agree with their genetically explicit counterparts about the expected trait composition of populations at equilibrium ([1], but see [2]). Unlike genetic models, however, phenotypic models are generally unable to predict the details of evolutionary trajectories. For instance, it is well known that the trajectory describing the expected increase in frequency of an advantageous mutation depends on whether the new allele is recessive or dominant. In particular, because variants occur almost exclusively in heterozygotes when they are rare, recessive advantageous alleles will be effectively neutral and thus easily lost by drift until they become common, whereas dominant or co-dominant alleles will be immediately selected. This idea is the basis of an old but still remarkable result of population genetics, attributable to J.B.S. Haldane [3], that Corresponding author: Pannell, J.R. ([email protected]). Available online 17 May 2005 advantageous mutations will be swept to fixation when they first arise in an outcrossing species with a probability equal to twice the selective advantage they confer multiplied by their dominance coefficient. The expected fixation bias in favour of dominant over recessive advantageous mutations has been called ‘Haldane’s Sieve’ [4]. It exemplifies the kind of prediction that cannot be made by evolutionary models coined solely in phenotypic terms. Haldane’s Sieve has been invoked to account for a range of observations from the prominence of derived dominant alleles for the melanic forms of several insect species [5], through dominant expression of alleles coding for derived wing patterns in Müllerian mimics [4], to the dominance of alleles for pesticide resistance [6]. In these and other examples, Haldane’s Sieve provides a possible explanation for the observed genetic basis of adaptation in terms of the fixation of dominant versus recessive mutations. Here, we propose that a process similar to Haldane’s Sieve should act repeatedly on dominant versus recessive alleles following migration into populations of geographically subdivided species. In particular, when the allelic variation is maintained in a metapopulation by negative frequency-dependent selection, Haldane’s Sieve will be an on-going process that should alter the frequency distribution of alleles at the selected locus, and thus the corresponding phenotypes, in a predictable way. A great many species have genetically subdivided populations that can be influenced by metapopulation dynamics, and several processes such as mimicry and disassortative mating are known to give rise to negative frequencydependent selection (Box 1). We first describe the process of Haldane’s Sieve in a metapopulation in terms of overlapping evolutionary trajectories within local populations that are prevented from reaching equilibrium by recurrent population turnover. We then highlight the potential for studying this phenomenon in subdivided plant populations that display reproductive or mating polymorphisms maintained by negative frequency-dependent selection as a result of disassortative mating; such systems continue to offer outstanding material for addressing a broad range of evolutionary questions. Finally, we note that the effect of Haldane’s Sieve in a metapopulation should depend on the size and dynamics of the populations concerned, and that www.sciencedirect.com 0169-5347/$ - see front matter Q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2005.05.004 Opinion TRENDS in Ecology and Evolution Vol.20 No.7 July 2005 375 Box 1. Negative frequency-dependent selection and plant reproductive polymorphisms Under negative frequency-dependent selection (FDS), rare phenotypes have higher fitness than do more common ones, with the implication that polymorphism is protected from loss through drift and that underlying genetic variation can be maintained for long periods of evolutionary time [39]. A particularly well understood mechanism of negative FDS is disassortative mating, where mating unions are more common between different mating phenotypes and rare phenotypes enjoy high fitness through their access to a greater number of compatible mating partners (e.g. [40,41]). We list here a diverse range of polymorphisms maintained by negative FDS through disassortative mating in plants. These are typically a result of the expression of major genes with dominant-recessive relations. † Androdioecy: the co-occurrence of hermaphrodites and males. Although rare, androdioecy has evolved several times independently in plants and animals [25]. Maleness is governed by a dominant allele in several plant species (e.g. [42]) and by a recessive allele in several interrelated species of crustaceans (e.g. [43]). † Dioecy: the co-occurrence of males and females. Dioecy has multiple evolutionary origins and occurs in 157 (43%) angiosperm families [44]. Its genetic basis varies, but males commonly carry a dominant allele conferring maleness [45]. † Distyly: the co-occurrence of two classes of hermaphrodite, ‘pins’ and ‘thrums’, that differ in their stigma and anther positions. Pins have long styles and anthers held low in the floral tube, whereas thrums have short styles and high-placed anthers. Distyly has multiple evolutionary origins and is known in 22 families. Short-styled plants usually result from expression of a dominant allele [46]. † Enantiostyly: the co-occurrence of hermaphrodites with either ‘right-handed’ or ‘left-handed’ flowers, in which the style and anthers are held to one or other side of the flower, with reciprocal placement of floral parts in the two different morphs. Dimorphic enantiostyly is reported in three plant families [47]. In one species, right-styled plants are heterozygous for the dominant allele [48]. † Flexistyly: the co-occurrence of two classes of hermaphrodites that differ in the direction of movement that styles undergo during flowering. In one morph, styles begin in an upward position and move downward, whereas the movement is in the opposite direction in the other morph. Anthers are held in the same position throughout, but shed pollen only when styles are in the ‘up’ position, promoting disassortative mating between floral morphs. Flexistyly was discovered only recently and is known in only a single family [49]. † Flower colour polymorphism: the co-occurrence of plants with different coloured flowers in a population. In at least one case [50], the polymorphism appears to be maintained by negative FDS. a distinct process of drift will oppose it when local populations are small. This balance between the forces of drift, migration and selection can account for observed phenotype frequencies that deviate from those expected in a single large population at equilibrium. We also suggest that the effect of processes such as Haldane’s Sieve and the interaction among drift, migration and selection might help to establish the extent to which metapopulation dynamic processes have been important in the evolution and ecology of plants. Haldane’s Sieve in a subdivided population Analyses predicting the action of Haldane’s Sieve usually consider the fate of new recessive versus non-recessive variants as they arise in a population through mutation (although see [7]). However, a similar process should occur when advantageous alleles invade a population via immigration. If the population is large and mating is random, all the early descendants of immigrants that carry an advantageous allele will be heterozygous. Those alleles that are recessive will remain unexpressed while in www.sciencedirect.com † Gametophytic self-incompatibility (GSI): a genetic polymorphism in which hermaphrodites are prevented both from self-fertilising their own ovules and from crossing with hermaphrodites that share the same diploid genotype at the self-incompatibility (SI) locus. Mating thus occurs only between plants that do not share both incompatibility alleles [51]. GSI is widespread among flowering plants and is common in several large families [52]. † Gynodioecy: the co-occurrence of hermaphrodites and females. Gynodioecy is taxonomically widespread in flowering plants, occurring in at least 35 plant families [53]. It commonly results from the expression of genes in the mitochondrion, but simple dominantrecessive relations are typical when governed by nuclear loci. † Heterodichogamy: the co-occurrence of two classes of hermaphrodite, a protandrous class that flowers first as male and a protogynous class that flowers first as female. Heterodichogamy has a widespread taxonomic distribution, occurring in 11 families of flowering plants [54]. In two species, a dominant allele gives rise to protogynous individuals (reviewed in [54]). † Sporophytic self-incompatibility (SSI): SSI is similar to GSI in that it prevents self-fertilization and outcrossing with individuals with the same diploid genotype at the SI locus. However, it differs in that it can also prevent mating between individuals that share just one of the two alleles at the SI locus. If the SI alleles contained by a mating pair of individuals have co-dominant expression, mating is possible only if all four alleles are unique [51]. However, unlike GSI, gene expression of SI alleles can be dominant or recessive. SSI has evolved on several occasions in flowering plants and is common in several large families [52]. † Stigma-height dimorphism: the co-occurrence of two classes of hermaphrodites, one with long styles and one with short styles. The dimorphism is analogous to distyly, except that all individuals share a similar anther position. Stigma-height dimorphism has evolved independently in several angiosperm families [47]. The inheritance of style length is analogous to that found in distyly, with a dominant allele for short styles, and long-styled plants modified into plants with mid-styles by a dominant allele at a second locus [55]. † Tristyly: the co-occurrence of short-styled, mid-styled and longstyled hermaphrodites, with the reciprocal placement of two levels of anthers at the position not occupied by the stigma (cf. distyly, which has only two morphs). Tristyly is reported from six families. The inheritance of short styles under tristyly is typically the same as that under distyly, with a dominant allele at a second locus modifying longstyled plants to those with mid-length styles [46]. the heterozygous state, rendering them prone to early loss as a result of drift. By contrast, dominant alleles will be expressed in all progeny and will thus be better protected against random loss by positive selection. As a consequence, dominant alleles should diffuse more readily through a subdivided metapopulation than should recessive alleles. This effect of Haldane’s Sieve was termed ‘dominance drive’ by Mallet [8], who modelled the maintenance of dominant versus recessive wing-colour variants in a hybrid zone between Müllerian butterfly mimics. Mallet [8] found that ‘[e]ven if the two phenotypes are equally fit ‘dominance drive’ tends to increase the area in which the dominant allele is present.’ We expect a particularly interesting scenario to arise when a polymorphism is maintained by negative frequency-dependent selection in a subdivided population or metapopulation. In this case, Haldane’s Sieve will be an ongoing process that acts indefinitely on standing genetic variation during its repeated introduction into subpopulations through migrations (Figure 1). The outcome of this process is likely to be complicated because the advantage Opinion 376 TRENDS in Ecology and Evolution 0.8 Recessive allele Allele frequency 0.6 1 2 3 0.4 Dominant allele 0.2 0.0 Time TRENDS in Ecology & Evolution Figure 1. The action of Haldane’s Sieve on migrant alleles in a large population. The curves show expected frequency trajectories of dominant versus recessive alleles under negative frequency-dependent selection following their migration into a population. Alleles migrate into the population at time point 1. The rate of increase in frequency is slower for a recessive allele than for a dominant one. Therefore, it takes longer for a recessive allele to get close to its equilibrium frequency (time point 3) than it does for a dominant one (time point 2). Shading corresponds to an elevated risk of allele loss because of drift in small populations: while the frequency of the migrant allele remains low, it runs a high risk of stochastic loss through drift (dark shading). Although Haldane’s Sieve favours dominant migrant alleles because they more quickly rise to higher frequency in the population, they are maintained at a lower frequency and are more likely to be lost through drift in small populations than are recessive alleles (light shading). This is because frequencydependent selection acts on phenotypes rather than on the alleles themselves. There will therefore be more recessive alleles segregating in a population at equilibrium than dominant ones because all recessive alleles in heterozygotes are not expressed as well as because individuals with phenotypes with recessive expression carry two recessive alleles whereas those with phenotypes with dominant expression might carry only one. In small populations, Haldane’s Sieve will also be less effective because inbreeding increases the frequency of homozygotes. conferred upon dominant alleles by Haldane’s Sieve will be opposed by the tendency of recessive alleles to be maintained at higher frequencies in a population at equilibrium and thus to be better protected from loss by drift than dominant alleles. We suggest that this interaction between selection, drift, migration and gene expression can be illuminated by its potential effect on the maintenance of plant reproductive polymorphisms in a metapopulation. Although the prevalence of metapopulation dynamics in plants is still hotly debated (Box 2), variation in the frequency of mating-system phenotypes of several plant species suggests that metapopulation processes might have been important in their past. Haldane’s Sieve and plant reproductive polymorphisms Plants are famously diverse in their reproductive strategies [9]. Not only do they display a broad range of floral forms across species, but they also present numerous examples of floral or reproductive polymorphisms maintained within single populations by negative frequencydependent selection (Box 1). The functional significance of these polymorphisms has attracted the attention of many evolutionary biologists, including Darwin [10], Haldane [11], Wright [12] and Fisher [13]. One of the attractive features of plant reproductive polymorphisms for evolutionary study is the relative ease with which models www.sciencedirect.com Vol.20 No.7 July 2005 predicting the proportions of the different mating types in a population can be tested. This is because the models are simple, in that they deal with the predictable tendency of phenotypes to mate disassortatively (i.e. like phenotypes avoid mating), and because the frequencies of the different mating types can usually be estimated easily in natural populations by counting phenotypes. Plant reproductive polymorphisms continue to be widely adopted as models for the study of various aspects of evolutionary biology, including the evolution of sexual systems [14], plant-pollinator interactions [15], plantherbivore interactions [16], sex allocation [17], speciation [18], sexual dimorphism and sexual selection [19], the maintenance of genetic diversity [20], vestigialization [21], and the evolution of sex and recombination [22]. They can also provide fertile material in which to look for signatures of population structure and possible metapopulation dynamics. This is perhaps best exemplified by the interaction between maternally inherited male-sterility genes and nuclear genes that restore male fertility in gynodioecious species, where females co-exist with hermaphrodites (reviewed in [23]). Here, the high variation in sex ratio between populations is most probably a result of colonization by genotypes with mismatched sterility and restorer genes, giving rise to high female frequencies, and the subsequent migration and local spread of complementary fertility restorer alleles that allow hermaphrodite frequencies to increase (e.g. [24]). Metapopulation processes should also affect the distribution of mating phenotypes determined by alleles at nuclear loci with simple dominant-recessive expression patterns, and this can be understood in terms of the recurrent action of Haldane’s Sieve. In androdioecious species, for example, where males co-occur with hermaphrodites [25], males are maintained at frequencies lower than 0.5 by frequency-dependent selection if hermaphrodites sire any progeny through their male function [26]. In a metapopulation, the repeated episodes of colonization will tend to select against males and favour hermaphrodites that are capable of founding new populations by self-fertilization, thereby reducing the frequency of males still further [27,28]. If alleles determining unisexuality are rare in the metapopulation, colonization of a new habitat by one or more hermaphrodites will usually give rise to a purely hermaphroditic population. In the absence of males, these populations will be relatively female-biased in their sex allocation, and rare males would enjoy a fitness advantage through the large numbers of their potential mating partners. Dominant male-determining (female-sterility) alleles, therefore, should easily invade hermaphroditic populations because they will immediately experience the positive effects of negative frequency-dependent selection on the sex allocation. By contrast, hermaphroditic populations will be relatively protected against the local spread of recessive male-determining alleles as a result of Haldane’s Sieve. Thus, dominant sterility alleles should be more likely to persist in a metapopulation when they are at low frequency than would those that are recessive [28]. Opinion TRENDS in Ecology and Evolution Vol.20 No.7 July 2005 377 Box 2. Do plant metapopulations exist? A metapopulation is a regional group of populations that is maintained in a balance between local population extinctions and re-colonizations [56]. The concept has been extremely influential in the study of animal populations, but its utility for understanding the abundance and distribution of plants has been disputed and is still unresolved [57–61]. From a practical point of view, several peculiarities of plant life history and growth form make it difficult to estimate extinction and colonization rates, or even to identify habitat patches. From a conceptual perspective, the issue of plant metapopulations concerns whether the regional patterns of occupancy and abundance of a plant species can be adequately explained by extrapolating up from the local processes of birth and death, or whether distinctly regional processes such as migration, colonization and local extinction need to be invoked to account for what we observe [58,62]. respond to gradients in environmental variables such that habitat quality is better characterized as a multidimensional vector on a continuum rather than as a binary ‘good’–‘bad’ variable [61]. This also means that the distinction between new colonizations and recolonizations is blurred. These practical difficulties will be difficult to resolve until models that deal with the peculiarities of plants more explicitly can be applied to data. Thus, Bullock et al. [57] recently concluded that it was still ‘too early to determine whether true plant metapopulations exist.’ Nonetheless, a few species, such as aquatic herbs, that do not present major difficulties associated with seed banks and habitat identification provide relatively uncontroversial examples of plant metapopulations (reviewed in [58]). Conceptual issues Practical issues Many plants have a dormant seed bank The utility of metapopulation theory depends largely on the extent to which rates of extinction and colonization can be estimated. In species with a seed bank, estimating these values can be difficult because habitat occupancy becomes difficult to assess. For example, it is not useful to consider the disappearance of the cohort of adult plants from a site as an extinction event if the species persists in a seed bank. Neither is it useful from a metapopulation perspective to consider the re-establishment of adults from a dormant seed bank as a form of temporal rather than spatial colonization because ‘colonization’ from a seed bank involves local processes only and does not require consideration of the regional process of dispersal [62]. The incorporation of seed-bank dynamics into metapopulation theory is not straightforward and will require the consideration of time lags in the extinction process [63]; more work is needed in this arena. Habitat identification, and the distinction between colonization and re-colonization The application of classical metapopulation theory to empirical data also presupposes an ability to distinguish categorically between suitable and unsuitable habitats [56]. In a great many plant species, habitat characterization is difficult because plants tend to Reproductive polymorphisms and the effect of drift in small populations We expect that Haldane’s Sieve will discriminate between dominant and recessive alleles in the way we have described as long as local populations grow rapidly to a large size following colonization, but not when population sizes remain small. There are essentially two reasons for this. First, homozygosity will be increased by inbreeding in small populations, so that advantageous recessive alleles are immediately selected and Haldane’s Sieve is therefore compromised [29]. Second, alleles maintained by frequency-dependent selection (see Box 1) are always vulnerable to stochastic loss from small populations (Figure 1), but dominant alleles will be lost more often in this case than recessive ones because their equilibrium frequencies will be lower [30,31]. The effect of Haldane’s Sieve will therefore not only be relaxed in metapopulations with small subpopulations, but it might also be reversed (Figure 1). The biased loss of dominant alleles through the process of drift has been invoked to explain the observed variation in the frequency of floral morphs in the tristylous annual plant Eichhornia paniculata, in which mating occurs between three morphs with different style lengths and anther positions [32]. In large tristylous populations of E. paniculata, disassortative mating between the three stylar morphs gives rise to negative frequency-dependent www.sciencedirect.com The conceptual issue of how often metapopulation dynamics need to be invoked to explain observations made at a regional level is unclear. Ultimately, the answer will depend on the nature of the data. From the point of view of genetic data, there is an increasing body of evidence from plant populations for the importance of the regional process of colonization (reviewed in [60]). Here, the practical problems of identifying habitat patches are less of an issue; what matters are the populations themselves as well as the interactions among genetic processes, such as drift during colonization bottlenecks, directional or frequency-dependent selection, and the homogenizing force of migration among populations [60]. Such interactions can yield different patterns in genetic data from those acting solely at a local level. Indeed, regional surveys of a range of plant genetic markers and discretely inherited phenotypic traits (e.g. the plant reproductive systems reviewed here) indicate that the colonizations and extinctions expected in metapopulations are likely to be occurring in plants (reviewed in [60]). That such processes can leave a genetic signature even in species for which ecological or demographic observations are readily explained by predominantly local processes suggests that a distinction between ‘genetic metapopulations’ and ‘ecological metapopulations’ might be useful [64]. selection that maintains each at equal frequencies of 1/3 [33]. However, the genetic mode of inheritance for tristyly implies that the dominant allele, which causes expression of a short-styled phenotype, is maintained at a frequency of 1/6 compared with the higher frequency of 5/6 at which its recessive homologue is maintained [32]. In a metapopulation made up of small subpopulations, the frequency of the short-styled morph should thus be lower than its equilibrium expectation because of its stochastic loss from some populations [32]. This hypothesis could explain the lower frequency of the short-styled morph of E. paniculata in areas where populations are small [32] as well as the more frequent loss of the short-styled morph from small populations of tristylous Lythrum salicaria [34]. As in tristylous species, disassortative mating is also responsible for the maintenance of the striking levels of polymorphism commonly found in plant species at loci governing molecular self-incompatibility systems (e.g. [35]). Under sporophytic self-incompatibility (SSI), S alleles are expected to be equally frequent in a population when they are expressed co-dominantly [36]. However, self-incompatibility reactions in many species are complicated by the fact that some S alleles show dominant expression over others, in either the pollen and/ or the carpel [35,37]. Again, dominant alleles are more likely to be lost from small populations by drift than those with recessive expression [31,38]. This prediction that Opinion 378 TRENDS in Ecology and Evolution dominant alleles should be less frequent across the metapopulation has found some empirical support in a study of the frequencies of sporophytic self-incompatibility alleles in Arabidopsis lyrata [37]. Conclusion: a balance between Haldane’s Sieve and drift in small populations The interaction between frequency-dependent selection, genetic drift and gene expression is complex. However, we suggest that some of the complexity arising from genetic interactions in subdivided populations can be characterized by considering it in the context of two opposing forces. On the one hand, Haldane’s Sieve should favour dominant over recessive alleles when they migrate into large populations. On the other hand, genetic drift within small populations should cause the local loss of dominant alleles more often than recessive ones. The latter effect has often been invoked to account for the biased loss of dominant alleles maintained by frequency-dependent selection, with or without the added complexities of population subdivision. However, it has been less widely appreciated that this effect can be reversed by the repeated action of Haldane’s Sieve acting on alleles migrating into large subpopulations of a metapopulation. The balance between these two opposing forces is evident in the results of computer simulations of allelic diversity maintained at an SSI locus in subdivided populations [30]. These simulations show that dominant alleles can be either more or less frequent than recessive alleles depending on the level of migration between subpopulations ([30] and Figure 2). SSI and the other plant reproductive polymorphisms are idiosyncratic in both the details of disassortative mating and the precise mode of inheritance of alleles under frequency-dependent 0.30 Frequency of allele 0.25 0.20 0.15 0.10 0.05 0.00 Panmixis co-dominance Panmixis dominance Subdivision dominance TRENDS in Ecology & Evolution Figure 2. The expected frequency spectrum for six S alleles maintained in a population with sporophytic self-incompatibility under contrasting scenarios of population subdivision and gene expression. The first distribution assumes panmixis and co-dominant gene expression in both pollen and carpel. The second distribution assumes panmixis and dominant gene expression in carpel but not pollen. The third distribution assumes the same pattern of gene expression as the middle distribution, but also that the population is strongly subdivided with low gene flow (NmZ0.01). In the middle and right-hand distributions, bars are ranked for S alleles in increasing order of dominance. Under panmixis, recessive alleles are maintained at a higher frequency than dominant or co-dominant ones (second distribution), whereas this frequency hierarchy is altered substantially in a subdivided population (third distribution). Data from [30]. www.sciencedirect.com Vol.20 No.7 July 2005 selection. However, they illustrate a potentially widespread phenomenon that deserves further modelling, particularly for the situation where population sizes fluctuate in time or are prone to local extinctions and re-colonizations. Plant reproductive polymorphisms also present a diverse range of independent systems within which to consider the old idea of Haldane’s Sieve in a new context. Finally, although it is widely accepted that metapopulation dynamics can be important in regulating the abundance and distribution of animals, the extent to which such processes occur in plants is still unclear. It might therefore be profitable to explore the principle of using reproductive-trait distributions as genetic signatures of such processes, as has been done with patterns of neutral genetic diversity. In this context, further modelling will be needed to predict the outcome of specific genetic and phenotypic interactions under different metapopulation scenarios in terms of observable patterns of variation among subpopulations. Equally important is the need for more data describing these patterns. Acknowledgements We thank S.C.H. Barrett, M. Whitlock and an anonymous reviewer for useful input, and we acknowledge grants from the NSF (USA) to S.M.E. (grant INT 0202645), the NSERC (Canada) to M.E.D., and the NERC (UK) to J.R.P. and M.E.D. References 1 Bulmer, M. (1994) Theoretical Evolutionary Ecology, Sinauer Associates 2 Day, T. and Taylor, P.D. (1998) Unifying genetic and game theoretic models of kin selection for continuous traits. J. Theor. Biol. 194, 391–407 3 Haldane, J.B.S. (1924) A mathematical theory of natural and artificial selection, part I. Proc. Camb. Philos. Soc. 23, 19–41 4 Turner, J.R.G. (1977) Butterfly mimicry: the genetical evolution of an adaptation. Evol. Biol. 11, 163–206 5 James, J.W. (1965) Simultaneous selection for dominant and recessive mutants. Heredity 20, 142–144 6 Charlesworth, B. (1998) Adaptive evolution: the struggle for dominance. Curr. Biol. 8, R502–R504 7 Orr, H.A. and Betancourt, A.J. (2001) Haldane’s sieve and adaptation from the standing genetic variation. Genetics 157, 875–884 8 Mallet, J. (1986) Hybrid zones of Heliconius butterflies in Panama and the stability and movement of warning color clines. Heredity 56, 191–202 9 Barrett, S.C.H. (2002) The evolution of plant sexual diversity. Nat. Rev. Genet. 3, 274–284 10 Darwin, C. (1877) The Different Forms of Flowers on Plants of the Same Species, Appleton 11 Haldane, J.B.S. (1933) Two new allelomorphs for heterostyly in Primula. Am. Nat. 67, 559–560 12 Wright, S. (1939) The distribution of self-sterility alleles in populations. Genetics 24, 538–552 13 Fisher, R.A. and Mather, K. (1943) The inheritance of style length in Lythrum salicaria. Ann. Eugen. 12, 1–23 14 Weiblen, G.D. et al. (2000) Phylogenetic analysis of dioecy in monocotyledons. Am. Nat. 155, 46–58 15 Bradshaw, H.D. and Schemske, D.W. (2003) Allele substitution at a flower colour locus produces a shift in monkey flowers. Nature 426, 176–178 16 Ashman, T.L. et al. (2004) Sex-differential resistance and tolerance to herbivory in a gynodioecious wild strawberry. Ecology 85, 2550–2559 17 Ashman, T.L. (2003) Constraints on the evolution of males and sexual dimorphism: field estimates of genetic architecture of reproductive traits in three populations of gynodioecious Fragaria virginiana. Evolution 57, 2012–2025 Opinion TRENDS in Ecology and Evolution 18 Vamosi, J.C. and Vamosi, S.M. (2004) The role of diversification in causing the correlates of dioecy. Evolution 58, 723–731 19 Delph, L.F. et al. (2004) Genetic constraints on floral evolution in a sexually dimorphic plant revealed by artificial selection. Evolution 58, 1936–1946 20 Stadler, T. and Delph, L.F. (2002) Ancient mitochondrial haplotypes and evidence for intragenic recombination in a gynodioecious plant. Proc. Natl. Acad. Sci. U. S. A. 99, 11730–11735 21 Dorken, M.E. et al. (2001) Evolutionary vestigilization of sex in a clonal plant: selection versus neutral mutation in geographically peripheral populations. Proc. R. Soc. Lond. B Biol. Sci. 271, 2375–2380 22 Filatov, D. et al. (2000) Low variability in a Y-linked plant gene and its implications for Y-chromosome evolution. Nature 404, 388–390 23 Frank, S.A. and Barr, C.M. (2001) Spatial dynamics of cytoplasmic male sterility. In Integrating Ecological and Evolutionary Processes in a Spatial Context (Silvertown, J. and Antonovics, J., eds), pp. 219–243, Blackwell 24 Taylor, D.R. et al. (2001) A quantitative genetic analysis of nuclearcytoplasmic male sterility in structured populations of Silene vulgaris. Genetics 158, 833–841 25 Pannell, J.R. (2002) The evolution and maintenance of androdioecy. Annu. Rev. Ecol. Syst. 33, 397–425 26 Charlesworth, D. and Charlesworth, B. (1978) A model for the evolution of dioecy and gynodioecy. Am. Nat. 112, 975–997 27 Baker, H.G. (1955) Self-compatibility and establishment after “longdistance” dispersal. Evolution 9, 347–348 28 Pannell, J. (1997) The maintenance of gynodioecy and androdioecy in a metapopulation. Evolution 51, 10–20 29 Whitlock, M.C. (2003) Fixation probability and time in subdivided populations. Genetics 164, 767–779 30 Schierup, M.H. et al. (2000) The effect of subdivision on variation at multi-allelic loci under balancing selection. Genet. Res. 76, 51–62 31 Bateman, A.J. (1952) Self-incompatibility systems in angiosperms. I. Theory. Heredity 6, 285–310 32 Barrett, S.C.H. et al. (1989) The dissolution of a complex genetic polymorphism: the evolution of self-fertilization in tristylous Eichhornia paniculata (Pontederiaceae). Evolution 43, 1398–1416 33 Heuch, I. (1979) Equilibrium populations of heterostylous plants. Theor. Popul. Biol. 15, 43–57 34 Eckert, C.G. et al. (1996) Genetic drift and founder effect in native versus introduced populations of an invading plant, Lythrum salicaria (Lythraceae). Evolution 50, 1512–1519 35 Mable, B.K. et al. (2003) Estimating the number, frequency, and dominance of S-alleles in a natural population of Arabidopsis lyrata (Brassicaceae) with sporophytic control of self-incompatibility. Heredity 90, 422–431 36 Charlesworth, D. et al. (2000) Population-level studies of multiallelic self-incompatibility loci, with particular reference to Brassicaceae. Ann. Bot. (London) 85, 227–239 37 Bechsgaard, J. et al. (2004) Uneven segregation of sporophytic selfincompatibility alleles in Arabidopsis lyrata. J. Evol. Biol. 17, 554–561 38 Schierup, M.H. et al. (1997) Evolutionary dynamics of sporophytic self-incompatibility alleles in plants. Genetics 147, 835–846 39 Nordborg, M. and Innan, H. (2003) The genealogy of sequences containing multiple sites subject to strong selection in a subdivided population. Genetics 163, 1201–1213 40 Schierup, M.H. et al. (2001) Recombination, balancing selection and phylogenies in MHC and self-incompatibility genes. Genetics 159, 1833–1844 www.sciencedirect.com Vol.20 No.7 July 2005 379 41 Richman, A.D. and Kohn, J.R. (1999) Self-incompatibility alleles from Physalis: implications for historical inference from balanced genetic polymorphisms. Proc. Natl. Acad. Sci. U. S. A. 96, 168–172 42 Wolf, D.E. et al. (2001) Sex determination in the androdioecious plant Datisca glomerata and its dioecious sister species D. cannabina. Genetics 159, 1243–1257 43 Sassaman, C. (1995) Sex determination and the evolution of unisexuality in the Conchostraca. Hydrobiologia 298, 45–65 44 Renner, S.S. and Ricklefs, R.E. (1995) Dioecy and its correlates in the flowering plants. Am. J. Bot. 82, 596–606 45 Charlesworth, D. (2002) Plant sex determination and sex chromosomes. Heredity 88, 94–101 46 Lewis, D. and Jones, D.A. (1992) The genetics of heterostyly. In Evolution and Function of Heterostyly (Barrett, S.C.H., ed.), pp. 129–150, Springer-Verlag 47 Barrett, S.C.H. et al. (2000) The evolution and function of stylar polymorphisms in flowering plants. Ann. Bot. 85, 253–265 48 Jesson, L.K. and Barrett, S.C.H. (2002) Enantiostyly: Solving the puzzle of mirror-image flowers. Nature 417, 707–707 49 Li, Q.J. et al. (2001) Flexible style that encourages outcrossing. Nature 410, 432 50 Gigord, L.D.B. et al. (2001) Negative frequency-dependent selection maintains a dramatic flower color polymorphism in the rewardless orchid Dactylorhiza sambucina (L.) Soo. Proc. Natl. Acad. Sci. U. S. A. 98, 6253–6255 51 Hiscock, S.J. and McInnis, S.M. (2003) The diversity of selfincompatibility systems in flowering plants. Plant Biol. 5, 23–32 52 Hiscock, S. and Kües, U. (1999) Cellular and molecular mechanisms of sexual incompatibility in plants and fungi. Int. Rev. Cytol. 193, 165–295 53 Maurice, S. et al. (1993) The evolution of gender in hermaphrodites of gynodioecious populations with nucleo-cytoplasmic male-sterility. Proc. R. Soc. London B. Biol. Sci. 251, 253–261 54 Renner, S.S. (2001) How common is heterodichogamy? Trends Ecol. Evol. 16, 595–597 55 Dulberger, R. (1964) Flower dimorphism and self-incompatibility in Narcissus tazetta L. Evolution 18, 361–363 56 Levins, R. (1970) Extinction. In Some Mathematical Questions in Biology (Gerstenhaber, M., ed.), pp. 77–107, American Mathematical Society 57 Bullock, J.M. et al. (2002) Plant dispersal and colonisation processes at local and landscape scales. In Dispersal Ecology (Bullock, J.M. et al., eds), pp. 279–302, Blackwell Science 58 Freckleton, R.P. and Watkinson, A.R. (2002) Large-scale spatial dynamics of plants: metapopulations, regional ensembles and patchy populations. J. Ecol. 90, 419–434 59 Ehrlén, J. and Eriksson, O. (2003) Large-scale spatial dynamics of plants: a response to Freckleton & Watkinson. J. Ecol. 91, 316–320 60 Pannell, J.R. and Obbard, D.J. (2003) Probing the primacy of the patch: what makes a metapopulation? J. Ecol. 91, 485–488 61 Murphy, H.T. and Lovett-Doust, J. (2004) Context and connectivity in plant metapopulations and landscape mosaics: does the matrix matter? Oikos 105, 3–14 62 Stokes, K.E. et al. (2004) Population dynamics across a parapatric range boundary: Ulex gallii and Ulex minor. J. Ecol. 92, 142–155 63 Ouborg, N.J. and Eriksson, O. (2004) Toward a metapopulation concept for plants. In Ecology, Genetics and Evolution of Metapopulations (Hanski, I.A. and Gaggiotti, O.E., eds), pp. 447–469, Elsevier 64 Ives, A.R. and Whitlock, M.C. (2002) Inbreeding and metapopulations. Science 295, 454–455