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Frequency-Dependent Selection, Beneficial Mutations, and the Evolution of Sex
Proceedings of the Royal Society B
Abstract
This paper presents a mathematical model of a population in which multiple alleles at a particular locus are maintained by frequency-dependent selection. The results suggest that, if the population reproduces sexually, the benefit conferred on the population by beneficial mutations at other loci will typically be much larger than if the population reproduces by asexual means. In part, this is true because, in asexual populations, beneficial mutations can produce suboptimal distributions of the alleles that are subject to frequency-dependent selection. Another factor that produces an advantage for sex is that, in asexual populations, beneficial mutations that have achieved a high copy number may nevertheless be lost from the population. This is highly unlikely in sexual populations.
... This allele spreads through the given subpopulation via clonal expansion of the recipient genome. This expansion, however, is restricted within the subpopulation (the idea is similar to the models described in Maynard Smith [30], Peck [42], Majewski and Cohan [31], and Hodgson and Otto [41]). The smaller the frequency of one subpopulation, the stronger the restriction of clonal expansion. ...
... One of these conditions is that high diversity is maintained at S loci within the population (i.e., l n > > 1). Another condition is that NFDS is sufficiently stronger than directional selection on ecologically beneficial alleles (i.e., s i > > s e ) so that NFDS can oppose clonal expansion driven by directional selection (see 'General framework of the model'; see also [42]). The third condition, which is implicitly assumed in the model, is that prokaryotic populations are sufficiently large (see Additional file 1 under 'Effect of finite populations'), which apparently is a realistic assumption based on the available data [43]. ...
... Mathematical models closely related to those analyzed here have been applied to eukaryotic populations by Peck [42], and Hodgson and Otto [41]. These previous studies investigate the advantage of recombination arising from interplay between NFDS and directional selection. ...
Background
Fixation of beneficial genes in bacteria and archaea (collectively, prokaryotes) is often believed to erase pre-existing genomic diversity through the hitchhiking effect, a phenomenon known as genome-wide selective sweep. Recent studies, however, indicate that beneficial genes spread through a prokaryotic population via recombination without causing genome-wide selective sweeps. These gene-specific selective sweeps seem to be at odds with the existing estimates of recombination rates in prokaryotes, which appear far too low to explain such phenomena.
Results
We use mathematical modeling to investigate potential solutions to this apparent paradox. Most microbes in nature evolve in heterogeneous, dynamic communities, in which ecological interactions can substantially impact evolution. Here, we focus on the effect of negative frequency-dependent selection (NFDS) such as caused by viral predation (kill-the-winner dynamics). The NFDS maintains multiple genotypes within a population, so that a gene beneficial to every individual would have to spread via recombination, hence a gene-specific selective sweep. However, gene loci affected by NFDS often are located in variable regions of microbial genomes that contain genes involved in the mobility of selfish genetic elements, such as integrases or transposases. Thus, the NFDS-affected loci are likely to experience elevated rates of recombination compared with the other loci. Consequently, these loci might be effectively unlinked from the rest of the genome, so that NFDS would be unable to prevent genome-wide selective sweeps. To address this problem, we analyzed population genetic models of selective sweeps in prokaryotes under NFDS. The results indicate that NFDS can cause gene-specific selective sweeps despite the effect of locally elevated recombination rates, provided NFDS affects more than one locus and the basal rate of recombination is sufficiently low. Although these conditions might seem to contradict the intuition that gene-specific selective sweeps require high recombination rates, they actually decrease the effective rate of recombination at loci affected by NFDS relative to the per-locus basal level, so that NFDS can cause gene-specific selective sweeps.
Conclusion
Because many free-living prokaryotes are likely to evolve under NFDS caused by ubiquitous viruses, gene-specific selective sweeps driven by NFDS are expected to be a major, general phenomenon in prokaryotic populations.
Electronic supplementary material
The online version of this article (doi:10.1186/s12915-015-0131-7) contains supplementary material, which is available to authorized users.
... One of the classic examples of the success of a pluralist approach explored host-parasite interactions within a genome subject to deleterious mutations, finding that the accumulation of deleterious mutations in asexual lineages through Muller's ratchet is more severe when host-parasite interactions simultaneously occur (Howard & Lively, 1994). Similarly, combining deleterious and beneficial mutations in finite populations increases the selective interference among loci (the Hill-Robertson effect; Hill & Robertson, 1966), generating stronger selection for sex and recombination than either type of mutation alone (Peck, 1993;Hartfield et al., 2010), although the net effect is generally less than the sum would predict (Hartfield et al., 2010). In this article, we combine directional selection for advantageous alleles with host-parasite interactions to explore whether sex and recombination can be favoured by their interaction. ...
... Second, if the beneficial allele does succeed in fixing, it might drag along with it only a subset of alleles at the host-parasite locus, reducing the ability of the focal species to keep up in the Red Queen race. These possibilities were emphasized by Peck (1993), who used a model of negative frequency-dependent selection within a single species to mimic Red Queen dynamics between species, finding that mean fitness was substantially lower in the absence of sex. Here, we determine whether such selective interference between loci subject to host-parasite selection and directional selection favours the evolution of increased rates of sex and recombination, using an explicit two-species model with genetically variable recombination rates. ...
... As illustrated in Fig. 3, beneficial alleles are much less likely to fix when host-parasite interactions are strong, especially when the average recombination rate is low. In these cases, the beneficial allele can initially establish and yet still be lost from the population if associated with an allele at the interaction locus that allows infection by the current or near future population of parasites (Peck, 1993). Proportionately, however, this interference has less of an effect on the fixation probability of strongly beneficial alleles (righthand side of Fig. 3). ...
Why sexual reproduction has evolved to be such a widespread mode of reproduction remains a major question in evolutionary biology. Although previous studies have shown that increased sex and recombination can evolve in the presence of host-parasite interactions (the 'Red Queen hypothesis' for sex), many of these studies have assumed that multiple loci mediate infection vs. resistance. Data suggest, however, that a major locus is typically involved in antigen presentation and recognition. Here, we explore a model where only one locus mediates host-parasite interactions, but a second locus is subject to directional selection. Even though the effects of these genes on fitness are independent, we show that increased rates of sex and recombination are favoured at a modifier gene that alters the rate of genetic mixing. This result occurs because of selective interference in finite populations (the 'Hill-Robertson effect'), which also favours sex. These results suggest that the Red Queen hypothesis may help to explain the evolution of sex by contributing a form of persistent selection, which interferes with directional selection at other loci and thereby favours sex and recombination.
... Several papers published in the 1990s departed sharply from this 'competing hypotheses' approach by applying a strategy that simultaneously included several hypotheses for sex [14][15][16]. In 1999 an influential paper in the Journal of Evolutionary Biology [17] [hereafter, 'West et al. (1999)'] reviewed this broader strategy, focusing on the general failure of the single hypothesistesting approach to solve the problem of sex. ...
... Conceptual Basis for the Pluralistic Approach to Sex and Support for These Ideas There were a few examples in the 1980s and early 1990s of the idea that different mechanisms for sex might apply differently across taxa [19,20] as well as a paper that modeled the simultaneous action of directional and frequency-dependent selection [14]. However, these early papers did not induce a movement away from competitive hypothesis testing. ...
Why sexual reproduction predominates in nature remains a mystery. The mystery stems in part from the fact that many of the plausible hypotheses for sex have restrictive assumptions. Two decades ago these limitations inspired the formulation of a ‘pluralist’ approach in which standalone hypotheses for sex were considered together. Here we review representative literature to address whether this strategy has deepened our understanding of sex. We found surprisingly few papers adopting such an approach, probably reflecting challenges associated with testing multiple mechanisms. Nevertheless, these studies provided new insights, highlighting in particular the potential importance of interaction between parasites and harmful mutations. We conclude with strategies for moving forward, including broader formulations of pluralism and the application of more qualitative types of testing.
... Considered one by one, these arguments are now convincing enough from a theoretical point of view to explain some specific experimental observations, but their relative importance is not yet fully assessed [27]. Several authors pleaded also for a so-called pluralist approach [5,28,29], arguing that the different explanations are likely to act synergistically. Hypotheses explaining the advantage of sex fall into one of five main groups: (1) the Red Queen hypothesis inducing negative frequency-dependent selection on genotypes, (2) the Tangled Bank hypothesis, relying on local competition among siblings (its effect is coined as density-dependent but is likely to result in a negative frequency-dependent selection), (3) the genetic consequences of recombination, (4) ecological factors reducing the benefit of high fecundity in the framework of K selection and (5) randomly fluctuating selection over time. ...
The advantage of sex, and its fixation in some clades and species all over the eukaryote tree of life, is considered an evolutionary enigma, especially regarding its assumed two-fold cost. Several likely hypotheses have been proposed such as (1) a better response to the negative frequency-dependent selection imposed by the “Red Queen” hypothesis; (2) the competition between siblings induced by the Tangled Bank hypothesis; (3) the existence of genetic and of (4) ecological factors that can diminish the cost of sex to less than the standard assumed two-fold; and (5) a better maintenance of genetic diversity and its resulting phenotypic variation, providing a selective advantage in randomly fluctuating environments. While these hypotheses have mostly been studied separately, they can also act simultaneously. This was advocated by several studies which presented a pluralist point of view. Only three among the five causes cited above were considered yet in such a framework: the Red Queen hypothesis, the Tangled Bank and the genetic factors lowering the cost of sex. We thus simulated the evolution of a finite mutating population undergoing negative frequency-dependent selection on phenotypes and a two-fold (or less) cost of sexuality, experiencing randomly fluctuating selection along generations. The individuals inherited their reproductive modes, either clonal or sexual. We found that exclusive sexuality begins to fix in populations exposed to environmental variation that exceeds the width of one ecological niche (twice the standard deviation of a Gaussian response to environment). This threshold was lowered by increasing negative frequency-dependent selection and when reducing the two-fold cost of sex. It contributes advocating that the different processes involved in a short-term advantage of sex and recombination can act in combination to favor the fixation of sexual reproduction in populations.
... Sex is generally considered to provide an adaptive advantage over asexual reproduction for the long-term survival of species because the reshuffling of genetic material by meiotic recombination allows new beneficial allelic combinations and the removal of deleterious alleles [1,2]. Shorter term, heterozygosity resulting from sexual reproduction may be advantageous by masking recessive deleterious mutations [3]. ...
Asexual reproduction in animals, though rare, is the main or exclusive mode of reproduction in some long-lived lineages. The longevity of asexual clades may be correlated with the maintenance of heterozygosity by mechanisms that rearrange genomes and reduce recombination. Asexual species thus provide an opportunity to gain insight into the relationship between molecular changes, genome architecture, and cellular processes. Here we report the genome sequence of the parthenogenetic nematode Diploscapter pachys with only one chromosome pair. We show that this unichromosomal architecture is shared by a long-lived clade of asexual nematodes closely related to the genetic model organism Caenorhabditis elegans. Analysis of the genome assembly reveals that the unitary chromosome arose through fusion of six ancestral chromosomes, with extensive rearrangement among neighboring regions. Typical nematode telomeres and telomeric protection-encoding genes are lacking. Most regions show significant heterozygosity; homozygosity is largely concentrated to one region and attributed to gene conversion. Cell-biological and molecular evidence is consistent with the absence of key features of meiosis I, including synapsis and recombination. We propose that D. pachys preserves heterozygosity and produces diploid embryos without fertilization through a truncated meiosis. As a prelude to functional studies, we demonstrate that D. pachys is amenable to experimental manipulation by RNA interference.
... Subsequent theoretical studies have shown that sex and recombination reduce selective interference in multiple contexts, including separating beneficial from deleterious alleles ('A Ruby in the Rubbish' [34]), separating beneficial alleles from polymorphisms maintained by selection [35], and separating beneficial alleles from sites involved in cyclic hostparasite dynamics [36,37]. Furthermore, not only can Hill-Robertson effects give sexual populations a fitness advantage, but they can also favour the evolution of increased rates of sex and recombination because genes that promote genetic mixing hitchhike up in frequency along with the good gene combinations that they create [38,39]. ...
Few topics have intrigued biologists as much as the evolution of sex. Understanding why sex persists despite its costs requires not just rigorous theoretical study, but also empirical data on related fundamental issues, including the nature of genetic variance for fitness, patterns of genetic interactions, and the dynamics of adaptation. The increasing feasibility of examining genomes in an experimental context is now shedding new light on these problems. Using this approach, McDonald et al. recently demonstrated that sex uncouples beneficial and deleterious mutations, allowing selection to proceed more effectively with sex than without. Here we discuss the insights provided by this study, along with other recent empirical work, in the context of the major theoretical models for the evolution of sex.
... When the fitness costs induced by a novel environment are severe, the ability to rapidly adapt may more than overcome the fitness deficits associated with sex. Therefore novel environmental conditions necessitating rapid adaptation are thought to select for the evolution of greater levels of genetic mixing (Weissmann, 1889, Crow, 1992, Peck, 1993, Peck, 1994. ...
Note: open access, full paper at http://onlinelibrary.wiley.com/doi/10.1111/jeb.12354/abstract
Sexual reproduction is widely regarded as one of the major unexplained phenomena in biology. Nonetheless, while a general answer may remain elusive, considerable progress has been made in the last few decades. Here, we first review the genesis of, and support for, the major ecological hypotheses for biparental sexual reproduction. We then focus on the idea that host-parasite coevolution can favour cross-fertilization over uniparental forms of reproduction, as this hypothesis currently has the most support from natural populations. We also review the results from experimental evolution studies, which tend to show that exposure to novel environments can select for higher levels of sexual reproduction, but that sex decreases in frequency after populations become adapted to the previously novel conditions. In contrast, experimental coevolution studies suggest that host-parasite interactions can lead to the long-term persistence of sex. Taken together, the evidence from natural populations and from laboratory experiments point to antagonistic coevolution as a potent and possibly ubiquitous force of selection favouring cross-fertilization and recombination.
... Where mixed mating is favored by selection, we found that the breeding system tends to be heavily biased toward self-fertilized offspring, suggesting that a bit of crossfertilization is sufficient to evade parasites. This latter result is consistent with mutational models that similarly suggest that a little sex may go a long way (Pamilo et al. 1987;Charlesworth et al. 1991;Charlesworth et al. 1993;Peck 1993;Green and Noakes 1995;review in Hurst and Peck 1996). ...
— Assuming all else is equal, an allele for selfing should spread when rare in an outcrossing population and rapidly reach fixation. Such an allele will not spread, however, if self-fertilization results in inbreeding depression so severe that the fitness of selfed offspring is less that half that of outcrossed offspring. Here we consider an ecological force that may also counter the spread of a selfing allele: coevolution with parasites. Computer simulations were conducted for four different genetic models governing the details of infection. Within each of these models, we varied both the level of selfing in the parasite and the level of male-gamete discounting in the host (i.e., the reduction in outcrossing fitness through male function due to the selfing allele). We then sought the equilibrium level of host selfing under the different conditions. The results show that, over a wide range of conditions, parasites can select for host reproductive strategies in which both selfed and outcrossed progeny are produced (mixed mating). In addition, mixed mating, where it exits, tends to be biased toward selfing.
... Alleles at this sexuality determining locus will be affected by selective pressures that arise from a number of different sources. For example, sex can have a variety of bene®ts such as the amelioration of the effects of deleterious mutations, and the facilitation of the incorporation of bene®cial mutations (Bell, 1982;Crow, 1988;Kondrashov, 1988;Michod & Levin, 1988;Kondrashov, 1993;Peck, 1993Peck, , 1994Peck, , 1996Hurst & Peck, 1996;Peck et al., 1997). Sex can also help in the`arms race' against coevolving parasites (Hamilton, 1980). ...
In many species, most (or all) offspring are produced by sexual means. However, theory suggests that selection should often favour the evolution of species in which a small fraction of offspring are produced sexually, and the rest are produced asexually. Here, we present the analysis of a model that may help to resolve this paradox. We show that, when heterozygote advantage is in force, members of species in which sex is rare will tend to produce poorly adapted offspring when they mate. This problem should be less severe in species where most offspring are produced by sexual means. As a consequence, once the rate of sexual reproduction becomes sufficiently rare, the benefits of sex may vanish, leading to the evolution of obligate asexuality. Substantial benefits of sexual reproduction may tend to accrue only if a large proportion of offspring are produced sexually. We suggest that similar findings are likely in the case of epistatic interactions between loci.
... Further research has investigated various types of selection interference that can be described as a Hill-Robertson effect. Such processes generally lie in 1 of 4 main categories, as summarized by Charlesworth et al. (2009) (Peck 1993). Sweeps can also interfere with fixation of new advantageous alleles if they arise at linked sites, as described in the Fisher-Muller hypothesis (Barton 1995b). ...
The evolution of sex is one of the most important and controversial problems in evolutionary biology. Although sex is almost universal in higher animals and plants, its inherent costs have made its maintenance difficult to explain. The most famous of these is the twofold cost of males, which can greatly reduce the fecundity of a sexual population, compared to a population of asexual females. Over the past century, multiple hypotheses, along with experimental evidence to support these, have been put forward to explain widespread costly sex. In this review, we outline some of the most prominent theories, along with the experimental and observational evidence supporting these. Historically, there have been 4 classes of theories: the ability of sex to fix multiple novel advantageous mutants (Fisher-Muller hypothesis); sex as a mechanism to stop the build-up of deleterious mutations in finite populations (Muller's ratchet); recombination creating novel genotypes that can resist infection by parasites (Red Queen hypothesis); and the ability of sex to purge bad genomes if deleterious mutations act synergistically (mutational deterministic hypothesis). Current theoretical and experimental evidence seems to favor the hypothesis that sex breaks down selection interference between new mutants, or it acts as a mechanism to shuffle genotypes in order to repel parasitic invasion. However, there is still a need to collect more data from natural populations and experimental studies, which can be used to test different hypotheses.
... The frequency of beneficial mutations is largely increased if asexual populations show low segregation rates (Hedrick and Whittam 1989;Green and Noakes 1995) or low recombination rates (Pamilo et al. 1987;Green and Noakes 1995). In addition to the classical Fisher-Muller models, rare sex may also accelerate the incorporation of extremely rare, beneficial mutations arising in populations that are prone to frequency-dependent selection (Peck 1993). Moreover, if a favorable mutation arises in a genome with deleterious mutations, sex rates of 5-10% largely increase the probability of its fixation (Peck 1994). ...
Theory predicts that occasional sexual reproduction in predominantly parthenogenetic organisms offers all the advantages of obligate sexuality without paying its full costs. However, empirical examples identifying and evaluating the costs and benefits of rare sex are scarce. After reviewing the theoretical perspective on rare sex, we present our findings of potential costs and benefits of occasional sex in polyploid, sperm-dependent parthenogens of the planarian flatworm Schmidtea polychroa. Despite costs associated with the production of less fertile tetraploids as sexual intermediates, the benefits of rare sex prevail in S. polychroa and may be sufficiently strong to prevent extinction of parthenogenetic populations. This offers an explanation for the dominance of parthenogenesis in S. polychroa. We discuss the enigmatic question why not all organisms show a mixed reproduction mode.
... Red Queen dynamics can also work, although simulations suggest that drift matters more when multiple parasites interact with different host genes (Hamilton et al. 1990) than when a host interacts with a single parasite via a pair of genes (Kouyos et al. 2007b). Of course, in the real world, organisms experience all forms of selection (Rice 1999), and combinations of these selective forces have also been shown to benefit sex in finite populations, involving beneficial and deleterious mutations (Peck's [1994] "Ruby in the Rubbish"), beneficial mutations and the Red Queen (Peck 1993), or deleterious mutations and the Red Queen (Howard and Lively 1994). ...
Sexual reproduction entails a number of costs, and yet the majority of eukaryotes engage in sex, at least occasionally. In this article, I review early models to explain the evolution of sex and why they failed to do so. More recent efforts have attempted to account for the complexities of evolution in the real world, with selection that varies over time and space, with differences among individuals in the tendency to reproduce sexually, and with populations that are limited in size. These recent efforts have clarified the conditions that are most likely to explain why sex is so common, as exemplified by the articles in this symposium issue of the American Naturalist.
... Where mixed mating is favored by selection, we found that the breeding system tends to be heavily biased toward self-fertilized offspring, suggesting that a bit of crossfertilization is sufficient to evade parasites. This latter result is consistent with mutational models that similarly suggest that a little sex may go a long way (Pamilo et al. 1987;Charlesworth et al. 1991;Charlesworth et al. 1993;Peck 1993;Green and Noakes 1995;review in Hurst and Peck 1996). ...
Assuming all else is equal, an allele for selfing should spread when rare in an outcrossing population and rapidly reach fixation. Such an allele will not spread, however, if self-fertilization results in inbreeding depression so severe that the fitness of selfed offspring is less that half that of outcrossed offspring. Here we consider an ecological force that may also counter the spread of a selfing allele: coevolution with parasites. Computer simulations were conducted for four different genetic models governing the details of infection. Within each of these models, we varied both the level of selfing in the parasite and the level of male-gamete discounting in the host (i.e., the reduction in outcrossing fitness through male function due to the selfing allele). We then sought the equilibrium level of host selfing under the different conditions. The results show that, over a wide range of conditions, parasites can select for host reproductive strategies in which both selfed and outcrossed progeny are produced (mixed mating). In addition, mixed mating, where it exits, tends to be biased toward selfing.
... For example, in a variety of models, small amounts of recombination have been shown to impart nearly as much advantage to sex as does free recombination (Charlesworth et al., 1991Green & Noakes, 1995;review in Pamilo et al., 1987;Peck, 1993;Hurst & Peck, 1996). In addition, it has been shown that environmental fluctuations select for intermediate rates of recombination when the fluctuations are imposed externally (i.e. ...
We explored the evolution of recombination under antagonistic coevolution, concentrating on the equilibrium frequencies of modifier alleles causing recombination in initially nonrecombining populations. We found that the equilibrium level of recombination in the host depended not only on parasite virulence, but also on the strength of the modifier allele, and on whether or not the modifier was physically linked to the parasite interaction loci. Nonetheless, the maximum level of recombination for linked loci at equilibrium was about 0.3 (60% of free recombination) for interactions with highly virulent parasites; the level decreased for unlinked modifiers, and for lower levels of parasite virulence. We conclude that recombination spreads because it provides a combination of an immediate (next-generation) fitness benefit and a delayed (two or more generations) increase in the rate of response to directional selection. The relative impact of these two mechanisms depends on the virulence of parasites early in the spread of the modifier, but a trade-off between the two dictates the equilibrium modifier frequency for all nonzero virulences that we examined. In addition, population mean fitness was higher in populations at intermediate equilibria than populations fixed for free recombination or no recombination. The difference, however, was not enough on its own to overcome the two-fold cost of producing males.
In this chapter, we deal with the change from the exception to the rule in biological systems, both by the action of nature and by the changes that occur due to human action. We talk about the origin of life on planet Earth, the first organisms that colonized primitive environments and changed the atmosphere, giving rise to new forms of life, the appearance of eukaryotic, multicellular organisms, and the different forms of reproduction. We focus on events and changes that were initially considered teratological and that are familiar to our current vision. We also mention adaptations, plasticity, and different phenotypes that became advantages and allowed organisms to continue living in different environments. On the other hand, we point to global processes that affect humans and that in many cases are caused by humans. We discuss examples of diseases that turn into pandemics, the processes of environmental pollution, and accelerated climate change. Finally, we will discuss the changes in scientific ideas, which are closely linked to the social context at each moment in human history, the changes in the different fields of study and within society itself.
Attempts to resolve the paradox of sexual reproduction in animal species have typically involved single factor
explanations, including but not limited to sexual species being better able to cope with fluctuating resources,
being better able to evade pathogens and predators and sex facilitating the elimination of deleterious alleles.
Our study is the first three-factor study to examine the potential interaction between purifying selection, the ability to avoid predators and the ability to cope with fluctuating resources. Therefore, we addressed a number of open eco-evolutionary questions in our study: First, what is the effect of these three factors on the prevalence of sexual reproduction in animals? Second, do these factors act integratively, antagonistically or independently in determining the prevalence of sexual reproduction. What we found is that purifying selection purging deleterious alleles in sexual species was integratively enhanced by the two additional factors of increased predation and fluctuating resources. On the other hand, the effect of purifying selection and increased predation had an antagonistic effect on the levels of sexual reproduction and asexual reproduction in facultative species where there were fluctuating resources. Finally, the presence of an intermediate intensity deleterious allele and fluctuating resources had no discernable effect on the extinction levels of sexual and asexual species where there is increased predation. These results are not surprising, as there is no a priori reason to assume that multiple factors will have a greater impact on mode of reproduction than any of these factors acting independently. Our results suggest that multiple factors can act intergratively, antagonistically and non-reductively all at the same time, which is a significant contribution to the open question in the biological literature regarding the effect of multiple factors on the prevalence of sexual reproduction.
Just as intraorganismal selection can produce “selfish” elements that lower individual fitness, selection at the organismal level can favour traits that reduce the fitness of conspecifics and potentially impact population survival. Because dispersal can affect how these traits are distributed within species, it may determine whether their negative consequences are restricted locally or spread throughout the species’ range. We present an individual‐based simulation model that explores the interaction between dispersal rate and traits that increase individual fecundity at the expense of conspecific fitness. We first modelled dispersal as a trait that varied within species and then fixed the within‐species dispersal rates and modelled competition between species that differed only in dispersal rate. Reproductive isolation allowed species differences in dispersal rates to become associated with traits moulded by intraspecific competition, but this association did not occur when dispersal variation was distributed within species due to recombination between the dispersal and competition loci. Alleles that reduced the fitness of conspecifics were maintained at lower frequencies in low‐dispersal species, resulting in a competitive advantage over high‐dispersing species. While high‐dispersal species initially outcompeted low‐dispersal species owing to enhanced colonization opportunities, low‐dispersal species ultimately showed greater representation across a range of ecological and genetic scenarios. This process may shift the makeup of communities over time toward a greater representation of low‐dispersal species.
Apomixis or asexual formation of seeds involves three major features, absence of meiotic reduction, recombination and fertilisation, and thereby leads to formation of genetically uniform progeny. Though Winkler coined the term ‘apomixis’ in 1908 to describe ‘asexual reproductive process in place of sexual reproduction without nuclear or cell fusion’, the definition of apomixis is now restricted to the formation of seeds via an asexual process. Today apomictic forms are reported in several flowering plant taxa in species of both monocotyledonous and dicotyledonous genera. Although apomixis seems to be a simple phenomenon, several pathways are speculated to achieve it. Also this phenomenon has many subcomponents which should be achieved consistently and simultaneously to ensure formation of seeds (or next generation). There has been much focus on several facets of apomixis including cyto-embryological, molecular and biotechnological aspects. However, the origin of apomixis (independently in several plant taxa) and its ecological and evolutionary significance is still not completely deciphered. Nonetheless, we do understand that polyploidisation and/or hybridisation-associated shifts as well as environmental gradients play a role in establishing apomixis in most of the studied taxa. Further diversification occurs through several processes including mutation, chromosome rearrangements and aneuploidy, residual sexuality and backcrossing. While environmental changes bring about range shifts and secondary contact hybridisation of different ecotypes results in origin of apomictic lineages, apomixis is also an important factor in changing the ecological scenarios. Previously apomictic lineages were considered to be a dead end, but the current understanding treats them as a means of diversification of polyploid complexes and evolution in angiosperms.
Premise of the study:
Ecological differentiation (ED) between sexual and asexual organisms may permit the maintenance of reproductive polymorphism. Several studies of sexual/asexual ED in plants have shown that the geographic ranges of asexuals extend beyond those of sexuals, often in areas of higher latitude or elevation. But very little is known about ED at fine scales, wherein coexistence of sexuals and asexuals may be permitted by differential niche occupation.
Methods:
We used 149 populations of sexual and apomictic lineages in the genus Boechera (rock cress) collected across a portion of this mustard's vast range. We characterized reproductive mode, ploidy, and species identity or hybrid parentage of each individual, and then used a multipronged statistical approach to (1) identify ED between sexuals and asexuals; (2) investigate the impacts of two confounding factors, polyploidy and hybridization, on ED; and (3) determine the environmental variables underlying ED.
Key results:
We found that sexuals and asexuals are significantly ecologically differentiated across the landscape, despite fine-scale interdigitation of these two reproductive forms. Asexual reproduction was strongly associated with greater disturbance, reduced slope, and greater environmental variability. Although ploidy had little effect on the patterns observed, hybridization has a unique impact on the relationships between asexual reproduction and specific environmental variables.
Conclusions:
Ecological differentiation along the axes of disturbance, slope, and climatic variability, as well as the effects of heterozygosity, may contribute to the maintenance of sexuality and asexuality across the landscape, ultimately impacting the establishment and spread of asexual lineages.
Overdominance, or a fitness advantage of a heterozygote over both homozygotes, can occur commonly with adaptation to a new optimum phenotype. We model how such overdominant polymorphisms can reduce the evolvability of diploid populations, uncovering a novel form of epistatic constraint on adaptation. The fitness load caused by overdominant polymorphisms can most readily be ameliorated by evolution at tightly linked loci; therefore traits controlled by multiple loosely linked loci are predicted to be strongly constrained. The degree of constraint is also sensitive to the shape of the relationship between phenotype and fitness, and the constraint caused by overdominance can be strong enough to overcome the effects of clonal interference on the rate of adaptation for a trait. These results point to novel influences on evolvability that are specific to diploids and interact with genetic architecture, and they predict a source of stochastic variability in eukaryotic evolution experiments or cases of rapid evolution in nature. This article is protected by copyright. All rights reserved.
The evolution of meiosis introduced an alternation between haploid and diploid phases into the life cycle of living organisms. With meiosis came the need to reestablish the diploid condition through fusion of two genetically distinct gametes (syngamy) each containing half of the parental genome scrambled during the recombinational processes leading up to meiotic division. The fusion of nuclei (karyogamy), following syngamy, can generate a basis for variation which natural selection can act upon only if the gametes involved originate from different individuals (Maynard Smith 1978). It is not surprising, therefore, that the majority of organisms show adaptations which favor fusion of gametes from different genetic backgrounds and, consequently, outbreeding (Jain 1976; Charlesworth and Charlesworth 1987; Jarne and Charlesworth 1993).
— The idea that sex functions to provide variation for natural selection to act upon was first advocated by August Weismann and it has dominated much discussion on the evolution of sex and recombination since then. The goal of this paper is to further extend this hypothesis and to assess its place in a larger body of theory on the evolution of sex and recombination. A simple generic model is developed to show how fitness variation and covariation interact with selection for recombination and illustrate some important implications of the hypothesis: (1) the advantage of sex and recombination can accrue both to reproductively isolated populations and to modifiers segregating within populations, but the former will be much larger than the latter; (2) forces of degradation that are correlated across loci within an individual can reduce or reverse selection for increased recombination; and (3) crossing-over (which can occur at different places in different meioses) will create more variability than having multiple chromosomes and so will have more influence on the efficacy of selection. Several long-term selection experiments support Weismann's hypothesis, including those showing a greater response to selection in populations with higher rates of recombination and higher rates of recombination evolving as a correlated response to selection for some other character. Weismann's hypothesis is also consistent with the sporadic distribution of obligate asexuality, which indicates that clones have a higher rate of extinction than sexuals. Weismann's hypothesis is then discussed in light of other patterns in the distribution of sexuality versus asexuality. To account for variation in the frequency of obligate asexuality in different taxa, a simple model is developed in which this frequency is a function of three parameters: the rate of clonal origin, the initial fitness of clones when they arise, and the rate at which that fitness declines over time. Variation in all three parameters is likely to be important in explaining the distribution of obligate asexuality. Facultative asexuality also exists, and for this to be stable it seems there must be ecological differences between the sexual and asexual propagules as well as genetic differences. Finally, the timing of sex in cyclical parthenogens is most likely set to minimize the opportunity costs of sex. None of these patterns contradict Weismann's hypothesis, but they do show that many additional principles unrelated to the function of sex are required to fully explain its distribution. Weismann's hypothesis is also consistent with what we know about the mechanics and molecular genetics of recombination, in particular the tendency for chromatids to recombine with a homolog rather than a sister chromatid at meiosis, which is opposite to what they do during mitosis. However, molecular genetic studies have shown that cis-acting sites at which recombination is initiated are lost by gene conversion as a result, a factor that can be expected to affect many fine details in the evolution of recombination. In summary, although Weismann's hypothesis must be considered the leading candidate for the function of sex and recombination, nevertheless, many additional principles are needed to fully account for their evolution.
The evolution of sex has been the focus of considerable attention during recent years. There is some consensus that the solution to the mystery is that sex either enables the creation and spread of advantageous traits (possibly parasite resistance) or helps to purge the genome of deleterious mutations. Recent experimental work has allowed testing of some of the assumptions underlying the theoretical models, most particularly whether interactions between genes are synergistic and whether the mutation rate is adequately high. However, although a variety of theories point out advantages to sex, most of them predict that a little sex and recombination can go a long way towards improving the fitness of a population, and it remains unclear why obligate sex is so common.
Although the evolution of recombination is still a major problem in evolutionary genetics, recent theoretical studies have shown that recombination can evolve by breaking down interference ("Hill-Robertson effects") among multiple loci. This leads to selection on a recombination modifier in a population subject to recurrent deleterious mutation. Here, we use computer simulations to investigate the evolution of a recombination modifier under three different scenarios of recurrent mutation in a finite population: (1) mutations are deleterious only, (2) mutations are advantageous only, and (3) there is a mixture of deleterious and advantageous mutations. We also investigate how linkage disequilibrium, the strength of selection acting on a modifier, and effective population size change under the different scenarios. We observe that adding even a small number of advantageous mutations increases the fixation rate of modifiers that increase recombination, especially if the effects of deleterious mutations are weak. However, the strength of selection on a modifier is less than the summed strengths had there been deleterious mutations only and advantageous mutations only.
Examination of the geographic distributions of sexual organisms and
their asexual, or parthenogenetic, competitors reveals certain
consistent patterns. These patterns are called geographic parthenogenes
is. For example, if we compare sexual organisms with closely related
asexuals, we find that, in the Northern Hemisphere, there is a strong
tendency for the asexuals to occur further to the north. One researcher
to document this pattern is Bierzychudek, who examined 43 cases (drawn
from 10 genera) where the geographic distributions of a sexual plant and
a closely related asexual are known. In 76% of these cases, the asexual
plant's range was more northerly than the range of the sexual. Some of
the remaining cases probably fit with this pattern, but more data must
be obtained before this suggestion can be confirmed. Asexuals also tend
to occur at high altitudes, and in marginal, resource-poor environments.
We have constructed a mathematical model of a habitat that stretches
from south to north in the Northern Hemisphere. Our computer simulations
based on this model support the idea that a single basic process may
account for much of what is known about geographic parthenogenesis. This
process involves the movement of individuals from areas in which they
are well adapted to areas where they are poorly adapted.
We present the results of a computer simulation model in which a sexual population produces an asexual mutant. We estimate the probability that the new asexual lineage will go extinct. We find that whenever the asexual lineage does not go extinct the sexual population is out-competed, and only asexual individuals remain after a sufficiently long period of time has elapsed. We call this type of outcome an asexual takeover. Our results suggest that, given repeated mutations to asexuality, asexual takeover is likely in an unstructured environment. However, if the environment is subdivided into demes that are connected by migration, then asexual takeover becomes less likely. The probability of asexual takeover declines towards zero as the number of demes increases and as the rate of migration decreases. The reason for this is that asexuality leads to a greater loss of fitness due to mutation and genetic drift, in comparison to what occurs under sexual reproduction. Population subdivision slows the spread of asexual lineages, which allows more time for the genetic degeneration caused by asexuality to take place.
Information is stored in neural circuits through long-lasting changes in synaptic strengths. Most studies of information storage have focused on mechanisms such as long-term potentiation and depression (LTP and LTD), in which synaptic strengths change in a synapse-specific manner. In contrast, little attention has been paid to mechanisms that regulate the total synaptic strength of a neuron. Here we describe a new form of synaptic plasticity that increases or decreases the strength of all of a neuron's synaptic inputs as a function of activity. Chronic blockade of cortical culture activity increased the amplitude of miniature excitatory postsynaptic currents (mEPSCs) without changing their kinetics. Conversely, blocking GABA (gamma-aminobutyric acid)-mediated inhibition initially raised firing rates, but over a 48-hour period mESPC amplitudes decreased and firing rates returned to close to control values. These changes were at least partly due to postsynaptic alterations in the response to glutamate, and apparently affected each synapse in proportion to its initial strength. Such 'synaptic scaling' may help to ensure that firing rates do not become saturated during developmental changes in the number and strength of synaptic inputs, as well as stabilizing synaptic strengths during Hebbian modification and facilitating competition between synapses.
Plant taxa that reproduce asexually display some distinct geographical and ecological patterns. A literature review reveals that such taxa 1) tend to have larger ranges, 2) tend to range into higher latitudes, and 3) tend to range to higher elevations than do their sexual relatives. Asexual taxa have a greater tendency than sexual taxa do to colonize once-glaciated areas. These trends have previously been identified as characteristic of parthenogenetic animals as well. While many authors have interpreted these trends as providing support for the 'biotic uncertainty' hypothesis for the maintenance of sex, these trends are consistent with several other interpretations as well. Furthermore, all of these interpretations have ignored the positive correlation that exists between ploidy level and breeding system: asexual plant and animal taxa are generally polyploid, while their sexual relatives are generally diploid. Evidence is presented for plants, and by extension for animals as well, that high ploidy levels alone-independent of breeding system-could endow individuals with the ability to tolerate these 'extreme' environments. For this reason, it appears premature to interpret observed distribution patterns as evidence to support hypotheses about what forces maintain sexual reproduction. Only experimental tests, using sexuals and asexuals of comparable ploidy levels, can permit us to discriminate among the alternatives.
When an advantageous mutation is fixed in a population by selection, a closely linked selectively neutral or mildly detrimental mutation may "hitchhike" to fixation along with it. It has been suggested that hitchhiking might increase the rate of molecular evolution. Computer simulations and a mathematical argument show that complete linkage to either advantageous or deleterious mutations does not affect the substitution of selectively neutral mutations. However, the simulations show that linkage to selected background mutations decreases the rate of fixation of advantageous mutations and increases the rate of fixation of detrimental mutations. This is true whether the linked background mutations are advantageous or detrimental, and it verifies and extends previous observations that linkage tends to reduce the effects of selection on evolution. These results can be interpreted in terms of the Hill-Robertson effect: a locus linked to another locus under selection experiences a reduction in effective population size. The interpretation of differences in evolutionary rates between different genomes or different regions of a genome may be confounded by the effects of strong linkage and selection. Recombination is expected to reduce the overall rate of molecular evolution while enhancing the rate of adaptive evolution.
The accumulation of beneficial and harmful mutations in a genome is studied by using analytical methods as well as computer simulation for different modes of reproduction. The modes of reproduction examined are biparental (bisexual, hermaphroditic), uniparental (selfing, automictic, asexual) and mixed (partial selfing, mixture of hermaphroditism and parthenogenesis). It is shown that the rates of accumulation of both beneficial and harmful mutations with weak selection depend on the within-population variance of the number of mutant genes per genome. Analytical formulae for this variance are derived for neutral mutant genes for hermaphroditic, selfing and asexual populations; the neutral variance is largest in a selfing population and smallest in an asexual population. Directional selection reduces the population variance in most cases, whereas recombination partially restores the reduced variance. Therefore, biparental organisms accumulate beneficial mutations at the highest rate and harmful mutations at the lowest rate. Selfing organisms are intermediate between biparental and asexual organisms. Even a limited amount of outcrossing in largely selfing and parthenogenetic organisms markedly affects the accumulation rates. The accumulation of mutations is likely to affect the mean population fitness only in long-term evolution.
The controversy over the evolutionary advantage of recombination initially discovered by Fisher and by Muller is reviewed. Those authors whose models had finite-population effects found an advantage of recombination, and those whose models had infinite populations found none. The advantage of recombination is that it breaks down random linkage disequilibrium generated by genetic drift. Hill and Robertson found that the average effect of this randomly-generated linkage disequilibrium was to cause linked loci to interfere with each other's response to selection, even where there was no gene interaction between the loci. This effect is shown to be identical to the original argument of Fisher and Muller. It also predicts the "ratchet mechanism" discovered by Muller, who pointed out that deleterious mutants would more readily increase in a population without recombination. Computer simulations of substitution of favorable mutants and of the long-term increase of deleterious mutants verified the essential correctness of the original Fisher-Muller argument and the reality of the Muller ratchet mechanism. It is argued that these constitute an intrinsic advantage of recombination capable of accounting for its persistence in the face of selection for tighter linkage between interacting polymorphisms, and possibly capable of accounting for its origin.
It has recently been argued that because the genetic load borne by an asexual species resulting from segregation, relative to a comparable sexual population, is greater than two, sex can overcome its twofold disadvantage and succeed. We evaluate some of the assumptions underlying this argument and discuss alternative assumptions. Further, we simulate the dynamics of competition between sexual and asexual types. We find that for populations of size 100 and 500 the advantages of segregation do not outweigh the cost of producing males. We conclude that, at least for small populations, drift and the cost of sex govern the evolution of sexuality, not selection or segregation. We believe, however, that if sexual and asexual populations were isolated for a sufficiently long period, segregation might impart a fitness advantage upon sexuals that could compensate for the cost of sex and allow sexuals to outcompete asexuals upon their reunion.
This study tests the hypothesis that one evolutionary advantage of sexual repro- duction is that it produces genetically variable progeny with a density-dependent advantage mediated by resource partitioning or pest pressure. Our experimental approach involved planting separate plots of sexually-derived and asexually-derived tillers of the grass An- thoxanthum odoratum in density gradients at the two natural sites from which the source material was taken. The sexual progeny displayed a significant fitness advantage compared to the asexual progeny. But, in contrast to the expectations of the density-dependent selection hypothesis, the advantage of the sexually produced progeny is most marked at lower den- sities. Thus, the results of this experiment and our previous report (Antonovics and Ellstrand, 1984) seem to best support the frequency-dependent selection hypothesis for the advantage of sexual reproduction.
Previous studies (Gibson et al., 1970; Nestmann and Hill, 1973, Cox and Gibson, 1974) have shown that strains of E. coli with high mutation rates have a marked advantage in competition with wild-type strains. Those studies, however, failed to discriminate between the hypotheses that the mutator bacteria acquired an advantage by evolving faster, on the one hand, or that they had an intrinsic competitive advantage, on the other Our present investigation supports the first hypothesis. We also present estimates for the mutational load in E. coli mutT strains and the mutation rate to higher fitness mutants in these experiments.
This study tests the hypothesis that one evolutionary advantage of sexual reproduction is that it produces rare or unique genotypes with a frequency-dependent advantage. Our experimental approach involved planting clonal tillers of the grass Anthoxanthum odoratum into natural sites. In two different experiments, clones in situations as a minority genotype had approximately a twofold increase of fitness compared to those in majority genotype situations. Although fitness data were strongly skewed and highly variable, overall these differences were significant. The data reported here are in concordance with the theoretical expectations of the frequency-dependent hypothesis for the evolutionary significance of sex and represent the first experimental demonstration of frequency-dependent selection under natural field conditions.
Pollen-ovule ratios (P/O's) of flowering plants, including grasses, reflect their breeding system and these can be divided into five classes: xenogamy, facultative xenogamy, facultative autogamy, obligate autogamy and cleistogamy. The evolutionary shift from class to class is accompanied by a significant decrease in the mean P/O. This pattern is found in anemophilous plants and their relatives as well as zoophilous plants and their relatives. Plants in Asclepiadaceae and Mimosaceae are exceptions in the xenogamous group. These plants invest minimal energy in pollen production and their fecundity is low, but when pollination is successful the reproductive return is relatively high. A comparison of P/O's with successional stage shows that P/O's increase significantly from disturbed habitats to late successional seres. In addition to suggesting that autogamy is adaptive in disturbed habitats and xenogamy in advanced successional stages, the data show that in intermediate habitats P/O's, hence breeding systems, also are intermediate, and display a balance between autogamy and xenogamy. P/O's may be minimal and if P/O's fall below a certain minimum, fecundity decreases. This is probably a consequence of insufficient pollen grains reaching the stigmas. Several examples are discussed showing that P/O's are a better indicator of a plant's breeding system than floral size and morphology.
INTRODUcnON Over a decade ago, I wrote two papers (Felsenstein, 1974; Felsenstein and Yokoyama, 1976) on models for the evolution of recombination. The central concern of those papers was to demonstrate the relationship between various models that had previously been proposed for the evolution of recombination and to present some simulation and theoretical results. The problem has con-tinued to be of interest to evolutionary biologists, although they seem particularly entranced by it when it is called "the evolution of sex" rather than, more accurately, "the evolution of recombination." When books are written on the subject, the noun in their title is inevitably "sex" rather than "recombination." One wonders how man)' fewer people would buy a book on this subject if the word "sex" were not in the title. . Recently, interest in the subject seems to be increasing. In his monograph, Williams (1975, p. v) has declared that ") hope at least to convince [readers) that there is a kind of crisis at hand in evolutionary biology, and that my suggestions 3rc plausible enough to warrant serious consideration." Crises in evolutionary biology have been declared quite frequently recently, although it has been noticeable that the biologist declaring one usually just happens to have completed a piece of work that is thought to solve it. These crises seem com-parable in importance to the "constitutional crises" that used to be declared daily by the press during the Watergate hearings of 1973. After a time, it became clear that a constitutional crisis was somewhat less serious than a flat tire on your car.
The controversy over the evolutionary advantage of recombination initially discovered by Fisher and by Muller is reviewed. Those authors whose models had finite-population effects found an advantage of recombination, and those whose models had infinite populations found none. The advantage of recombination is that it breaks down random linkage disequilibrium generated by genetic drift. Hill and Robertson found that the average effect of this randomly-generated linkage disequilibrium was to cause linked loci to interfere with each other's response to selection, even where there was no gene interaction between the loci. This effect is shown to be identical to the original argument of Fisher and Muller. It also predicts the ''ratchet mechanism'' discovered by Muller, who pointed out that deleterious mutants would more readily increase in a population without recombination. Computer simulations of substitution of favorable mutants and of the long-term increase of deleterious mutants verified the essential correctness of the original Fisher-Muller argument and the reality of the Muller ratchet mechanism. It is argued that these constitute an intrinsic advantage of recombination capable of accounting for its persistence in the face of selection for tighter linkage between interacting polymorphisms, and possibly capable of accounting for its origin.
A simple genetic model based on Haldane's arguments about the evolution of host-parasite interaction is described and its applicability and limitations with respect to plant-fungus interactions is discussed. The basic form of frequency-dependent selection envisaged by Haldane can be demonstrated in agricultural systems, but no data are available from natural systems.
New factors arise in a species by the process of mutation. The frequency of mutation is generally small, but it seems probable that it can sometimes be increased by changes in the environment (1,2). On the whole mutants recessive to the normal type occur more commonly than dominants. The frequency of a given type of mutation varies, but for some factors in Drosophila it must be less than 10−6, and is much less in some human cases. We shall first consider initial conditions, when only a few of the new type exist as the result of a single mutation; and then the course of events in a population where the new factor is present in such numbers as to be in no danger of extinction by mere bad luck. In the first section the treatment of Fisher (3) is followed.(Received May 21 1927)(Revised July 25 1927)
It has recently been argued that because the genetic load borne by an asexual species resulting from segregation, relative to a comparable sexual population, is greater than two, sex can overcome its twofold disadvantage and succeed. We evaluate some of the assumptions underlying this argument and discuss alternative assumptions. Further, we simulate the dynamics of competition between sexual and asexual types. We find that for populations of size 100 and 500 the advantages of segregation do not outweigh the cost of producing males. We conclude that, at least for small populations, drift and the cost of sex govern the evolution of sexuality, not selection or segregation. We believe, however, that if sexual and asexual populations were isolated for a sufficiently long period, segregation might impart a fitness advantage upon sexuals that could compensate for the cost of sex and allow sexuals to outcompete asexuals upon their reunion.
The consequences of favourable and deleterious mutations in an asexual population with two alleles A and a are considered. The frequency of A = p and that of a = q, p ≠ q is likely so that p > q is assumed. The polymorphism is maintained by frequency dependent selection. In such a species there will be a tendency for advantageous mutations to accumulate most rapidly in clone A and deleterious mutations to accumulate most rapidly in clone a. Eventually the species will become monomorphic for A. During the process clone A will become larger but will lose fitness. Sex prevents clonal loss and permits the existence of intense variation.
This paper proposes that alleles increasing recombination rates may be selected for as a result of the perturbing effects of the spread of selectively favored alleles on neighboring loci maintained polymorphic by sleection. The recombination genes are favored since their presence increases the production of selectively advantageous types of gametes with which they tend to remain associated. Numerical examples are presented, and some consequences of this model discussed. One such consequence is the wicespread existence of polymorphism for genes affecting recombination values.
Darwinian theory has yet to explain adequately the fact of sex. If males provide little or no aid to offspring, a high (up to 2-fold) extra average fitness has to emerge as a property of a sexual parentage if sex is to be stable. The advantage must presumably come from recombination but has been hard to identify. It may well lie in the necessity to recombine defenses to defeat numerous parasites. A model demonstrating this works best for contesting hosts whose defense polymorphisms are constrained to low mutation rates. A review of the literature shows that the predictions of parasite coevolution fit well with the known ecology of sex. Moreover, parasite coevolution is superior to previous models of the evolution of sex by supporting the stability of sex under the following challenging conditions: very low fecundity, realistic patterns of genotype fitness and changing environment, and frequent mutation to parthenogenesis, even while sex pays the full 2-fold cost.
Sexual reproduction confronts evolutionary biology with a paradox: other things being equal, an asexual (all-female) population will have twice the reproductive potential of a competing sexual population and therefore should rapidly drive the sexual population to extinction. Thus, the persistence of sexual reproduction in most life forms implies a compensatory advantage to sexual reproduction. Work on this problem has emphasized the evolutionary advantages produced by the genetic recombination that accompanies sexual reproduction. Here we show that genetic segregation produces an advantage to sexual reproduction even in the absence of an advantage from recombination. Segregation in a diploid sexual population allows selection to carry a single advantageous mutation to a homozygous state, whereas two separate mutations are required in a parthenogenetic population. The complete fixation of advantageous mutations is thus delayed in a heterozygous state in asexual populations. Calculation of the selective load incurred suggests that it may offset the intrinsic twofold reproductive advantage of asexual reproduction and maintain sexual reproduction in diploid populations.
When Darwin and Wallace first formulated the theory of evolution by natural selection, they were greatly influenced by the idea that populations tend to increase geometrically and rapidly outgrow the resources available to them. They argued that the ensuing competition among individuals would be a major agent of natural selection. Since their day, competition has become almost synonymous with the idea of natural selection or survival of the fittest. In this paper we examine the relation between competition and selection by using simple competition models, consider the interaction of density and frequency in determining competitive outcome, and review the literature on frequency-dependent competitive interactions among genotypes within populations.
A two-species genetic model of host-parasite interaction is used to study the dynamical consequences of varying the number of genotypes in each species, and the recombination rate in the host. With two genotypes in each species, the model's behaviour is very simple; there is either a stable interior equilibrium, a stable cycle or a smooth outward spiral toward the boundaries. But with three or more genotypes, complex cycles and apparently chaotic behaviour may arise over wide ranges of parameter values. Increasing the number of genotypes also tends to slow the rate of gene-frequency change. Recombination in the host does not affect the stability of the interior fixed point, but intermediate rates of recombination may give dynamic stability to an otherwise dynamically unstable pattern of cycling. Intermediate rates of recombination also tend to decrease the amplitudes of gene-frequency cycles in the host, which implies that they could promote the accumulation of genetic variation involved in complementary, antagonistic interactions with parasites.
Sometimes predators tend to concentrate on common varieties of prey and overlook rare ones. Within prey species, this could result in the fitness of each variety being inversely related to its frequency in the population. Such frequency-dependent or 'apostatic' selection by predators hunting by sight could maintain polymorphism for colour pattern, and much of the supporting evidence for this idea has come from work on birds and artificial prey. These and other studies have shown that the strength of the observed selection is affected by prey density, palatability, coloration and conspicuousness. When the prey density is very high, selection becomes 'anti-apostatic': predators preferentially remove rare prey. There is still much to be learned about frequency-dependent selection by predators on artificial prey: work on natural polymorphic prey has hardly begun.
There are many situations in which the direction and intensity of natural selection in bacterial populations will depend on the relative frequencies of genotypes. In some cases, this selection will favour rare genotypes and result in the maintenance of genetic variability; this is termed stabilizing frequency-dependent selection. In other cases, selection will only favour genotypes when they are common. Rare types cannot invade and genetic variability will not be maintained; this is known as disruptive frequency-dependent selection. Phage-mediated selection for bacteria with novel restriction-modification systems is frequency-dependent and stabilizing. In mass culture, selection for the production of toxins and allelopathic agents is likely to be frequency-dependent but disruptive. This also occurs in selection favouring genes and transposable elements that cause mutations. Here I review the results of theoretical and experimental studies of stabilizing and disruptive frequency-dependent selection in bacterial populations, and speculate on the importance of this kind of selection in the adaptation and evolution of these organisms and their accessory elements (plasmid, phage and transposons).
(i) A computer simulation study has been made of selection on two linked loci in small populations, where both loci were assumed to have additive effects on the character under selection with no interaction between loci. If N is the effective population size, i the intensity of selection in standard units, α and β measure the effects of the two loci on the character under selection as a proportion of the pheno-typic standard deviation and c is the crossover distance between them, it was shown that the selection process can be completely specified by Ni α, Ni βand Nc and the initial gene frequencies and linkage disequilibrium coefficient. It is then easily possible to generalize from computer runs at only one population size. All computer runs assumed an initial population at linkage equilibrium between the two loci. Analysis of the results was greatly simplified by considering the influence of segregation at the second locus on the chance of fixation at the first (defined as the proportion of replicate lines in which the favoured allele was eventually fixed).
(ii) The effects of linkage are sufficiently described by Nc. The relationship between chance of fixation at the limit and linkage distance (expressed as 2Nc /( 2Nc + 1)) was linear in the majority of computer runs.
(iii) When gene frequency changes under independent segregation were small, linkage had no effect on the advance under selection. In general, segregation at the second locus had no detectable influence on the chance of fixation at the first if the gene effects at the second were less than one-half those at the first. With larger gene effects at the second locus, the chance of fixation passed through a minimum and then rose again. For two loci to have a mutual influence on one another, their effects on the character under selection should not differ by a factor of more than two.
(iv) Under conditions of suitable relative gene effects, the influence of segregation at the second locus was very dependent on the initial frequency of the desirable allele. The chance of fixation at the first, plotted against initial frequency of the desirable allele at the second, passed through a minimum when the chance of fixation at the second locus was about 0·8.
(v) A transformation was found which made the influence of segregation at the second locus on the chance of fixation at the first almost independent of initial gene frequency at the first and of gene effects at the first locus when these are small.
(vi) In the population of gametes at final fixation, linkage was not at equilibrium and there was an excess of repulsion gametes.
(vii) The results were extended to a consideration of the effect of linkage on the limits under artificial selection. Linkage proved only to be of importance when the two loci had roughly equal effects on the character under selection. The maximum effect on the advance under selection occurred when the chance of fixation at both of the loci was between 0·7 and 0·8. When the advance under selection is most sensitive to changes in recombination value, a doubling of the latter in no case increased the advance under selection by more than about 6%. The proportion selected to give maximum advance under individual selection (0·5 under independent segregation) was increased, but only very slightly, when linkage is important.
(viii) These phenomena could be satisfactorily accounted for in terms of the time scale of the selection process and the effective size of the population within which changes of gene frequency at the locus with smaller effect must take place.
Sexual populations will accumulate favourable mutations more rapidly than asexual populations. This is true if it is often the case that two different favourable mutations can be found to be spreading simultaneously through populations. It is argued here that sexual species will incorporate single favourable mutations more quickly than asexual “species”, if the latter are multi-clonal. Thus one mutation can spread to fixation within a sexual species but in an asexual “species” with Nc clones at least Nc mutations must occur if the mutation is to be subsequently found in every member of the “species”. Asexual “species” may minimise this disadvantage by evolving polyploidy or occasional episodes of hybridisation. Both are in fact common in asexual “species”.
Parthenogenesis is a very common phenomenon in the animal kingdom, forms with parthenogenetic reproduction being found in most animal groups. This chapter discusses the modes of reproduction in animals, the occurrence of parthenogenesis in animals, and the systems of parthenogenesis. Parthenogenesis can be considered from the following points of view: mode of reproduction, sex determination, and cytology. The chromosonal conditions in parthenogenetic animal include generative or haploid parthenogenesis, automictic parthenogenesis, and apomictic parthenogenesis. In many parthenogenetic animals, in all those with obligatory parthenogenesis, reproduction is exclusively parthenogenetic. In such forms, males are usually completely unknown. In other parthenogenetic animals, both parthenogenetic and sygogenetic reproduction are present. Such is the case in cyclical parthenogenesis, in which parthenogenetic generations alternate with a bisexual generation. Other species again occur as two races; bisexual and parthenogenetic.
The evolution of sex
- Maynard Smith