Evolving Inversions
2019; Elsevier BV; Volume: 34; Issue: 3 Linguagem: Inglês
10.1016/j.tree.2018.12.005
ISSN1872-8383
AutoresRui Faria, Kerstin Johannesson, Roger K. Butlin, Anja M. Westram,
Tópico(s)Genomics and Phylogenetic Studies
ResumoEmpirical data suggest that many inversions are maintained polymorphic within populations by balancing selection, which impedes divergence and speciation. Contrary to earlier beliefs, we here argue that balancing and divergent selection may act together shaping the frequencies of inversions, maintaining many of them polymorphic, and having important consequences for adaptation and speciation. Inversions are not static but the derived and ancestral arrangements of an inversion continue to evolve, partly separately from each other and from the collinear genome, until lost or fixed. However, the evolution of inversions after their establishment is often neglected. New modelling approaches and data from additional taxa are needed to understand how inversions evolve over time and space, and what roles they play in adaptation, divergence, and speciation. Empirical data suggest that inversions in many species contain genes important for intraspecific divergence and speciation, yet mechanisms of evolution remain unclear. While genes inside an inversion are tightly linked, inversions are not static but evolve separately from the rest of the genome by new mutations, recombination within arrangements, and gene flux between arrangements. Inversion polymorphisms are maintained by different processes, for example, divergent or balancing selection, or a mix of multiple processes. Moreover, the relative roles of selection, drift, mutation, and recombination will change over the lifetime of an inversion and within its area of distribution. We believe inversions are central to the evolution of many species, but we need many more data and new models to understand the complex mechanisms involved. Empirical data suggest that inversions in many species contain genes important for intraspecific divergence and speciation, yet mechanisms of evolution remain unclear. While genes inside an inversion are tightly linked, inversions are not static but evolve separately from the rest of the genome by new mutations, recombination within arrangements, and gene flux between arrangements. Inversion polymorphisms are maintained by different processes, for example, divergent or balancing selection, or a mix of multiple processes. Moreover, the relative roles of selection, drift, mutation, and recombination will change over the lifetime of an inversion and within its area of distribution. We believe inversions are central to the evolution of many species, but we need many more data and new models to understand the complex mechanisms involved. Early studies of inversions were restricted to species with easily visualised chromosomes (e.g., flies). Today, inferring the presence of inversions is technically possible in many species as reference genomes, genetic maps, and extensive sequencing data become available. Classical work has suggested that inversions are important in local adaptation and speciation [1White M.J.D. Animal Cytology and Evolution. Cambridge University Press, 1973Google Scholar, 2Dobzhansky T.G. Genetics of the Evolutionary Process. Columbia University Press, 1970Google Scholar], and later studies have emphasised that they offer a potential solution to Felsenstein’s dilemma [3Felsenstein J. Skepticism towards Santa Rosalia, or why are there so few kinds of animals?.Evolution. 1981; 35: 124-138Crossref PubMed Google Scholar] (see Glossary). Suppressed recombination among genes inside the inversion, in heterokaryotype individuals, results in largely independent genome evolution of derived and ancestral arrangements and opportunities for divergence and speciation [4Kirkpatrick M. How and why chromosome inversions evolve.PLoS Biol. 2010; 8e1000501Crossref PubMed Scopus (317) Google Scholar, 5Butlin R.K. Recombination and speciation.Mol. Ecol. 2005; 14: 2621-2635Crossref PubMed Scopus (220) Google Scholar, 6Kirkpatrick M. Barton N. Chromosome inversions, local adaptation and speciation.Genetics. 2006; 173: 419-434Crossref PubMed Scopus (691) Google Scholar, 7Hoffmann A.A. Rieseberg L.H. Revisiting the impact of inversions in evolution: from population genetic markers to drivers of adaptive shifts and speciation?.Annu. Rev. Ecol. Syst. 2008; 39: 21-42Crossref Scopus (419) Google Scholar, 8Feder J.L. et al.Assessing when chromosomal rearrangements affect the dynamics of speciation: implications from computer simulations.Front. Genet. 2014; 5: 295Crossref PubMed Scopus (31) Google Scholar, 9Charlesworth B. Barton N.H. The spread of an inversion with migration and selection.Genetics. 2018; 208: 377-382Crossref PubMed Scopus (42) Google Scholar]. Yet, inversions are commonly polymorphic within populations [10Wellenreuther M. Bernatchez L. Eco-evolutionary genomics of chromosomal inversions.Trends Ecol. Evol. 2018; 33: 427-440Abstract Full Text Full Text PDF PubMed Scopus (222) Google Scholar]. This is a paradox that current models cannot resolve, because balancing selection (which maintains polymorphism within populations) typically opposes divergence (needed for speciation). However, the evolution of inversions is multifaceted and variable over space and time. Using a life-history framework that describes the possible fates of new inversions, we highlight the need for a deeper understanding of the evolution of inversions by making connections among existing ideas and identifying gaps in our knowledge. Many authors have considered the conditions for the initial spread of a new inversion [4Kirkpatrick M. How and why chromosome inversions evolve.PLoS Biol. 2010; 8e1000501Crossref PubMed Scopus (317) Google Scholar, 8Feder J.L. et al.Assessing when chromosomal rearrangements affect the dynamics of speciation: implications from computer simulations.Front. Genet. 2014; 5: 295Crossref PubMed Scopus (31) Google Scholar, 11Connallon T. et al.Local adaptation and the evolution of inversions on sex chromosomes and autosomes.Phil. Trans. R. Soc. B. 2018; 37320170423Crossref PubMed Scopus (20) Google Scholar], while the subsequent evolution of the inversion has been studied less, especially the changing allelic contents of the ancestral and derived arrangements. The life history of an inversion embraces evolutionary change from its appearance by mutation of a single, flipped haplotype, to its loss or fixation. Importantly, a new derived arrangement has no genetic variation at the start, while the ancestral arrangement is variable (in common with collinear regions of the genome). Over time, the derived arrangement tends to become increasingly variable (unless selective sweeps are frequent), and recombination among haplotypes increases as homokaryotypic individuals become more common. Thus, the dynamics of inversion polymorphisms change over time, and there are also many possible interactions between the derived and the ancestral arrangement with implications for the fate of the inversion and its role in the evolution of the population (Box 1).Box 1Concepts and MechanismsWhen a chromosomal mutation forms an inversion, the derived arrangement has no variation (Figure I) but accumulates new genetic variation over time by mutation, or by rare gene flux (double crossovers and gene conversion, [44Pegueroles C. et al.Gene flow and gene flux shape evolutionary patterns of variation in Drosophila subobscura.Heredity. 2013; 110: 520-529Crossref PubMed Scopus (25) Google Scholar]) in heterozygotes for the inversion (heterokaryotypes). Within the pool of derived haplotypes, recombination is possible in homozygotes for the inversion (homokaryotypes). If the derived arrangement is favourable and finally fixed, it becomes the new collinear region and is only distinguishable by comparing the sequence order with other populations or species (Figure I).The initial stages in the life history of an inversion are governed by its direct effects (positive or negative breakpoint effects), its allelic content, and/or its effects on neighbouring genes. Meiotic problems, including the loss of unbalanced recombinant gametes, might cause underdominance [1White M.J.D. Animal Cytology and Evolution. Cambridge University Press, 1973Google Scholar] (Figure IIA1,2). Underdominance usually causes loss of the derived arrangement, unless drift or other fitness effects bring it to high frequency.The inversion might capture different types of alleles that increase or decrease the fitness of the derived arrangement and, critically, mutations subsequently introduce new variation at random into the derived and ancestral arrangements. Some of these mutations tend towards fixing one arrangement locally, thus generating divergence among populations and progress towards speciation (Figure IIB). Others tend to promote polymorphism within populations by generating balancing selection (Figure IIC).Multiple and locally advantageous alleles within the inverted region, in the presence of gene flow, can favour establishment of the derived arrangement [6Kirkpatrick M. Barton N. Chromosome inversions, local adaptation and speciation.Genetics. 2006; 173: 419-434Crossref PubMed Scopus (691) Google Scholar], and further locally advantageous alleles can accumulate subsequently (Figure IIB3). Dobzhansky–Müller incompatibilities might accumulate within the inverted region [21Navarro A. Barton N.H. Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation.Evolution. 2003; 57: 447-459Crossref PubMed Scopus (293) Google Scholar], and the inversion helps to maintain them following secondary contact [20Noor M.A.F. et al.Chromosomal inversions and the reproductive isolation of species.Proc. Natl. Acad. Sci. U. S. A. 2001; 98: 12084-12088Crossref PubMed Scopus (611) Google Scholar] (Figure IIB4). High linkage disequilibrium within the inversion favours the spread of alleles causing nonrandom mating in response to low fitness of heterokaryotypes (i.e., reinforcement [27Trickett A.J. Butlin R.K. Recombination suppressors and the evolution of new species.Heredity. 1994; 73: 339-345Crossref PubMed Scopus (64) Google Scholar]) (Figure IIB5).Individual loci within the inversion might show overdominance or be under negative frequency-dependent selection (including frequency dependence due to environmental heterogeneity; e.g., [19Wilson D.S. Turelli M. Stable underdominance and the evolutionary invasion of empty niches.Am. Nat. 1986; 127: 835-850Crossref Scopus (148) Google Scholar]), generating balancing selection within populations (Figure IIC6). Overdominance for the inversion can result from epistatic interactions among alleles at different loci [14Charlesworth B. Charlesworth D. Selection on new inversions in multi-locus genetic systems.Genet. Res. 1973; 21: 167-183Crossref Scopus (58) Google Scholar], and new alleles that contribute to this coadaptation are subsequently favoured [2Dobzhansky T.G. Genetics of the Evolutionary Process. Columbia University Press, 1970Google Scholar] (Figure IIC7). Finally, associations maintained by suppressed recombination between recessive deleterious alleles at different loci, dominant advantageous alleles at different loci, or both, can make the heterokaryotype more fit than either homokaryotype (associative overdominance [15Ohta T. Associative overdominance caused by linked detrimental mutations.Genet. Res. 1971; 18: 277-286Crossref PubMed Scopus (148) Google Scholar]) (Figure IIC8,9).Figure IIEvolutionary Effects of Inversions and the Loci within Them. The genetic mechanisms of direct (A) and indirect (B, C) effects of an inversion are illustrated, including those generating divergence (B) and polymorphism (C). Ancestral alleles are in black, upper case indicates dominance, derived alleles are green if advantageous, red if deleterious, and blue if neutral but generating assortment. An allele that causes overdominance is indicated by an asterisk. Arrows indicate epistatic interactions.View Large Image Figure ViewerDownload Hi-res image Download (PPT) When a chromosomal mutation forms an inversion, the derived arrangement has no variation (Figure I) but accumulates new genetic variation over time by mutation, or by rare gene flux (double crossovers and gene conversion, [44Pegueroles C. et al.Gene flow and gene flux shape evolutionary patterns of variation in Drosophila subobscura.Heredity. 2013; 110: 520-529Crossref PubMed Scopus (25) Google Scholar]) in heterozygotes for the inversion (heterokaryotypes). Within the pool of derived haplotypes, recombination is possible in homozygotes for the inversion (homokaryotypes). If the derived arrangement is favourable and finally fixed, it becomes the new collinear region and is only distinguishable by comparing the sequence order with other populations or species (Figure I). The initial stages in the life history of an inversion are governed by its direct effects (positive or negative breakpoint effects), its allelic content, and/or its effects on neighbouring genes. Meiotic problems, including the loss of unbalanced recombinant gametes, might cause underdominance [1White M.J.D. Animal Cytology and Evolution. Cambridge University Press, 1973Google Scholar] (Figure IIA1,2). Underdominance usually causes loss of the derived arrangement, unless drift or other fitness effects bring it to high frequency. The inversion might capture different types of alleles that increase or decrease the fitness of the derived arrangement and, critically, mutations subsequently introduce new variation at random into the derived and ancestral arrangements. Some of these mutations tend towards fixing one arrangement locally, thus generating divergence among populations and progress towards speciation (Figure IIB). Others tend to promote polymorphism within populations by generating balancing selection (Figure IIC). Multiple and locally advantageous alleles within the inverted region, in the presence of gene flow, can favour establishment of the derived arrangement [6Kirkpatrick M. Barton N. Chromosome inversions, local adaptation and speciation.Genetics. 2006; 173: 419-434Crossref PubMed Scopus (691) Google Scholar], and further locally advantageous alleles can accumulate subsequently (Figure IIB3). Dobzhansky–Müller incompatibilities might accumulate within the inverted region [21Navarro A. Barton N.H. Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation.Evolution. 2003; 57: 447-459Crossref PubMed Scopus (293) Google Scholar], and the inversion helps to maintain them following secondary contact [20Noor M.A.F. et al.Chromosomal inversions and the reproductive isolation of species.Proc. Natl. Acad. Sci. U. S. A. 2001; 98: 12084-12088Crossref PubMed Scopus (611) Google Scholar] (Figure IIB4). High linkage disequilibrium within the inversion favours the spread of alleles causing nonrandom mating in response to low fitness of heterokaryotypes (i.e., reinforcement [27Trickett A.J. Butlin R.K. Recombination suppressors and the evolution of new species.Heredity. 1994; 73: 339-345Crossref PubMed Scopus (64) Google Scholar]) (Figure IIB5). Individual loci within the inversion might show overdominance or be under negative frequency-dependent selection (including frequency dependence due to environmental heterogeneity; e.g., [19Wilson D.S. Turelli M. Stable underdominance and the evolutionary invasion of empty niches.Am. Nat. 1986; 127: 835-850Crossref Scopus (148) Google Scholar]), generating balancing selection within populations (Figure IIC6). Overdominance for the inversion can result from epistatic interactions among alleles at different loci [14Charlesworth B. Charlesworth D. Selection on new inversions in multi-locus genetic systems.Genet. Res. 1973; 21: 167-183Crossref Scopus (58) Google Scholar], and new alleles that contribute to this coadaptation are subsequently favoured [2Dobzhansky T.G. Genetics of the Evolutionary Process. Columbia University Press, 1970Google Scholar] (Figure IIC7). Finally, associations maintained by suppressed recombination between recessive deleterious alleles at different loci, dominant advantageous alleles at different loci, or both, can make the heterokaryotype more fit than either homokaryotype (associative overdominance [15Ohta T. Associative overdominance caused by linked detrimental mutations.Genet. Res. 1971; 18: 277-286Crossref PubMed Scopus (148) Google Scholar]) (Figure IIC8,9). The rates of origin of new inversions or new mutations inside inversions are rarely recorded, but most new, derived arrangements are lost by genetic drift soon after they appear, as the initial frequency is low (∼1/2N). Deleterious effects at breakpoints or fitness reduction in heterokaryotypes due to the elimination of recombinant gametes increase the probability of rapid loss [4Kirkpatrick M. How and why chromosome inversions evolve.PLoS Biol. 2010; 8e1000501Crossref PubMed Scopus (317) Google Scholar]. In contrast, inversions with positive fitness effects in heterokaryotypes occur less frequently but are more likely to become established, that is, to be maintained long enough in the population for other evolutionary processes to influence their fate. Rarely, a new inversion might capture a universally favoured haplotype, for example, one with a low load of deleterious mutations [12Nei M. et al.Frequency changes of new inversions in populations under mutation-selection equilibria.Genetics. 1967; 57: 741-750PubMed Google Scholar] or favoured by meiotic drive [13Coyne J.A. A test of the role of meiotic drive in fixing a pericentric inversion.Genetics. 1989; 123: 241-243PubMed Google Scholar], and spread rapidly to fixation. An inversion polymorphism can establish in one of two ways. The derived arrangement might spread to fixation by drift or selection in some populations while being absent or lost in others, potentially with some local polymorphism maintained by gene flow (we refer to this as Type I inversion polymorphism). Alternatively, a balanced polymorphism can be supported within one or more populations, for example, by overdominance or frequency dependence (Type II inversion polymorphism) (Figure 1). Several different mechanisms influence these alternatives. Genetic drift in small and isolated populations can fix a new arrangement locally, even with some underdominance [1White M.J.D. Animal Cytology and Evolution. Cambridge University Press, 1973Google Scholar], leading to Type I polymorphisms. Selection for local adaptation, even in the presence of gene flow [6Kirkpatrick M. Barton N. Chromosome inversions, local adaptation and speciation.Genetics. 2006; 173: 419-434Crossref PubMed Scopus (691) Google Scholar], can also generate Type I polymorphisms. However, balancing selection is needed to maintain Type II polymorphisms. This can arise from epistatic interactions among alleles at different loci [14Charlesworth B. Charlesworth D. Selection on new inversions in multi-locus genetic systems.Genet. Res. 1973; 21: 167-183Crossref Scopus (58) Google Scholar], from associative overdominance [15Ohta T. Associative overdominance caused by linked detrimental mutations.Genet. Res. 1971; 18: 277-286Crossref PubMed Scopus (148) Google Scholar] or, on rare occasions, when the inversion captures a locus that is, itself, under balancing selection (Box 1). Local adaptation with gene flow is common, and has been suggested as a likely driver for the establishment of new inversions [6Kirkpatrick M. Barton N. Chromosome inversions, local adaptation and speciation.Genetics. 2006; 173: 419-434Crossref PubMed Scopus (691) Google Scholar]. If locally fit alleles at two or more loci on the same chromosome are captured by an inversion, their association is conserved for extensive periods of time and the haplotype within the inversion is favoured over recombining haplotypes. Importantly, the rate of spread of the inversion is proportional to the migration rate between populations [6Kirkpatrick M. Barton N. Chromosome inversions, local adaptation and speciation.Genetics. 2006; 173: 419-434Crossref PubMed Scopus (691) Google Scholar], and larger inversions that capture more locally adapted alleles are more likely to spread. Furthermore, populations that cycle between stages of isolation and migration promote the spread of inversions under even broader sets of conditions [16Feder J.L. et al.Adaptive chromosomal divergence driven by mixed geographic mode of evolution.Evolution. 2011; 65: 2157-2170Crossref PubMed Scopus (60) Google Scholar]. Critically, the types of alleles that drive these processes continue to arise by mutation, on both the ancestral and derived arrangements, with potentially profound consequences for the life history of the inversion. The relative roles of selection, drift, mutation, and recombination change over the lifetime of an inversion. For example, the derived and ancestral arrangements diverge by new mutations, but converge by occasional gene flux (see Figure I in Box 1). As the contents of both the ancestral and derived arrangements change over time, the opportunities for selection also change. Recombination is infrequent in a low-frequency arrangement, because homokaryotypes are rare, and this also shifts the balance between drift and selection towards drift [5Butlin R.K. Recombination and speciation.Mol. Ecol. 2005; 14: 2621-2635Crossref PubMed Scopus (220) Google Scholar]. Further inversion mutations in the same genomic region might reduce gene flux or extend the genomic region of suppressed recombination [17Navarro A. et al.Recombination and gene flux caused by gene conversion and crossing over in inversion heterokaryotypes.Genetics. 1997; 146: 695-709Crossref PubMed Google Scholar]. The result can be a complex and changing pattern of differentiation between arrangements, as seen in the Payne inversion in the vinegar fly Drosophila melanogaster [18Kennington W.J. et al.Patterns of diversity and linkage disequilibrium within the cosmopolitan inversion In(3R)Payne in Drosophila melanogaster are indicative of coadaptation.Genetics. 2006; 172: 1655-1663Crossref PubMed Scopus (64) Google Scholar], analogous to the patterns of differentiation among populations generated by selection–migration balance. To maintain a Type II (balanced) inversion polymorphism requires either heterosis or negative frequency-dependent selection (including selection in temporally or spatially heterogeneous environments), while divergent selection maintains Type I polymorphism. In either case, the alternative arrangements receive different types of mutations (see Figure II in Box 1). At the same time, the fates of these mutations depend on the state of the inversion polymorphism. For example, in the absence of homokaryotypes, recessive deleterious mutations are not exposed to selection and tend to accumulate on the rarer arrangement (initially the derived arrangement). Importantly, recent modelling (Berdan et al. personal communication) shows that the ancestral arrangement also accumulates deleterious recessive alleles slowly, but at a higher rate than the collinear genome. This is because there is also a lower recombination rate in the ancestral arrangement compared to the collinear genome. These processes might result in fitness loss in both homokaryotypes and increased heterokaryotype advantage due to associative overdominance (see Figure II in Box 1). This accumulation of deleterious recessive alleles is more likely under Type II polymorphism than Type I polymorphism where each arrangement has a large local effective population size (Figure 1). In contrast, inversions that differentiate populations are likely to accumulate further locally adapted alleles and can also acquire alleles that promote assortative mating. However, the advantage provided by suppressed recombination is available only in populations that are influenced by gene flow. Divergent selection can also create and maintain among-population variation for underdominant inversions [6Kirkpatrick M. Barton N. Chromosome inversions, local adaptation and speciation.Genetics. 2006; 173: 419-434Crossref PubMed Scopus (691) Google Scholar], which are less likely to persist within populations (although this is possible with some forms of frequency dependence [19Wilson D.S. Turelli M. Stable underdominance and the evolutionary invasion of empty niches.Am. Nat. 1986; 127: 835-850Crossref Scopus (148) Google Scholar]). Dobzhansky–Müller incompatibilities are most likely to become associated with inversions that are fixed different between isolated populations, due to the independent spread of mutations under drift or selection. These incompatibilities might be expressed on secondary contact and be important in maintaining reproductive barriers [20Noor M.A.F. et al.Chromosomal inversions and the reproductive isolation of species.Proc. Natl. Acad. Sci. U. S. A. 2001; 98: 12084-12088Crossref PubMed Scopus (611) Google Scholar]. They can also accumulate within inversions in the presence of gene flow [21Navarro A. Barton N.H. Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation.Evolution. 2003; 57: 447-459Crossref PubMed Scopus (293) Google Scholar]. However, it is unlikely that alleles causing incompatibilities could spread within inversions that are maintained as balanced polymorphisms within populations (Type II inversion polymorphisms), unless the same alleles are advantageous within their own genomic background. Generally, the conditions for inversion polymorphisms seem broader than those for single-locus balanced polymorphisms. This is for the simple reason that an inversion contains many, potentially interacting loci resulting in many possible allele combinations that could drive the balance. For example, a new inversion that captures both locally favoured or epistatic alleles and deleterious recessive alleles will increase in frequency but rarely reach fixation as the homokaryotype for the inversion expresses the deleterious alleles and is selected against. However, a central point here is that the mechanisms maintaining inversion polymorphisms are not static. If an inversion polymorphism is initially established by, for example, one overdominant locus inside the inversion or by frequency-dependent selection, over time, increasing stability might evolve by the accumulation of different recessive deleterious mutations in the derived and ancestral arrangements building up associative overdominance. Alternatively, increasing divergence between populations might occur as locally adapted alleles and, later, Dobzhansky–Müller incompatibilities accumulate within the inversion. Frequency-dependent selection or heterosis could maintain both balanced polymorphism and divergence between populations at the same time. Equilibrium frequencies of arrangements differ between populations either because the same sets of alleles confer different fitness, or because the same arrangements carry different alleles in each local population, as observed in D. melanogaster [22Fryenberg J. et al.DNA sequence variation and latitudinal associations in hsp23, hsp26 and hsp27 from natural populations of Drosophila melanogaster.Mol. Ecol. 2003; 12: 2025-2032Crossref PubMed Scopus (91) Google Scholar, 23Kennington W.J. et al.Mapping regions within cosmopolitan inversion In(3R)Payne associated with natural variation in body size in Drosophila melanogaster.Genetics. 2007; 177: 549-556Crossref PubMed Scopus (36) Google Scholar]. Thus the end point need not be either among-population divergence (Type I) or balanced polymorphism (Type II); it can be a combination of both (Box 2).Box 2What Happens When Balancing Selection and Local Adaptation Both Influence Inversion Frequencies?We constructed a simple simulation model to show how balancing selection interacts with divergent selection when they both impact on the same inversion. We simulated a linear chain of 150 demes, each of width 1, with a habitat transition after deme 75 and with dispersal of 1.5. Random mating was followed by viability selection, dispersal and then drift (deme size 20). The allele frequency was initially equal for all demes in one environment but different between the two environments (randomly chosen from the range 0–1 for each environment independently), treating the inversion as a single locus, and simulations were run for 1000 generations.We considered three forms of selection: divergent only, divergent with heterosis, and frequency-dependent with different equilibria in the two habitats. Fitness is indicated in Table I.As expected, we find that divergent selection alone generates clines that approach fixation in populations distant from the habitat transition (Figure I). When divergent selection is weak, clines are wide and noisy. In contrast, balancing selection can result in different equilibrium frequencies in the two habitats, with steep clines close to the habitat transition.Table IFitness of the Three Karyotypes in Each of Two Habitats (Left and Right) for Three Different Model SimulationsLeft habitatRight habitatDivergent onlyAncestral homokaryotype1–2sleft1Heterokaryotype1–sleft1–srightDerived homokaryotype11–2srightDivergent plus heterosisAncestral homokaryotype1–2sleft1Heterokaryotype1–sleft + h1–sright + hDerived homokaryotype11–2srightFrequency dependentaPhenotype frequency P=pD2+2 pD pA, where pA is the ancestral arrangement frequency and pD is the derived arrangement frequency.Dominant phenotypealeft + bParight + bPRecessive phenotype11a Phenotype frequency P = pD2 + 2 pD pA, where pA is the ancestral arrangement frequency and pD is the derived arrangement frequency. Open table in a new tab We constructed a simple simulation model to show how balancing selection interacts with divergent sele
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