Using Parthenogenetic Lineages to Identify Advantages of Sex

The overwhelming predominance of sexual reproduction in nature is surprising given that sex is expected to confer profound costs in terms of production of males and the breakup of beneficial allele combinations. Recognition of these theoretical costs was the inspiration for a large body of empirical research—typically focused on comparing sexual and asexual organisms, lineages, or genomes—dedicated to identifying the advantages and maintenance of sex in natural populations. Despite these efforts, why sex is so common remains unclear. Here, we argue that we can generate general insights into the advantages of sex by taking advantage of parthenogenetic taxa that differ in such characteristics as meiotic versus mitotic offspring production, ploidy level, and single versus multiple and hybrid versus non-hybrid origin. We begin by evaluating benefits that sex can confer via its effects on genetic linkage, diversity, and heterozygosity and outline how the three classes of benefits make different predictions for which type of parthenogenetic lineage would be favored over others. Next, we describe the type of parthenogenetic model system (if any) suitable for testing whether the hypothesized benefit might contribute to the maintenance of sex in natural populations, and suggest groups of organisms that fit the specifications. We conclude by discussing how empirical estimates of characteristics such as time since derivation and number of independent origins of asexual lineages from sexual ancestors, ploidy levels, and patterns of molecular evolution from representatives of these groups can be used to better understand which mechanisms maintain sex in natural populations.     

Host-parasite coevolution and selection on sex through the effects of segregation

The advantage of producing novel variation to keep apace of coevolving species has been invoked as a major explanation for the evolution and maintenance of sex (the Red Queen hypothesis). Recent theoretical investigations of the Red Queen hypothesis have focused on the effects of recombination in haploid species, finding that species interactions rarely favor the evolution of sex unless selection is strong. Yet by focusing on haploids, these studies have ignored a potential advantage of sex in diploids: generating novel combinations of alleles at a particular locus through segregation. Here we investigate models of host-parasite coevolution in diploid species to determine whether the advantages of segregation might rescue the Red Queen hypothesis as a more general explanation for the evolution of sex. We find that the effects of segregation can favor the evolution of sex but only under some models of infection and some parameter combinations, almost always requiring inbreeding. In all other cases, the effects of segregation on selected loci favor reductions in the frequency of sex. In cases where segregation and recombination act in opposite directions, we found that the effects of segregation dominate as an evolutionary force acting on sex in diploids.     

Antagonistic species interaction drives selection for sex in a predator–prey system

The evolutionary maintenance of sexual reproduction has long challenged biologists as the majority of species reproduce sexually despite inherent costs. Providing a general explanation for the evolutionary success of sex has thus proven difficult and resulted in numerous hypotheses. A leading hypothesis suggests that antagonistic species interaction can generate conditions selecting for increased sex due to the production of rare or novel genotypes that are beneficial for rapid adaptation to recurrent environmental change brought on by antagonism. To test this ecology‐based hypothesis, we conducted experimental evolution in a predator (rotifer)–prey (algal) system by using continuous cultures to track predator–prey dynamics and in situ rates of sex in the prey over time and within replicated experimental populations. Overall, we found that predator‐mediated fluctuating selection for competitive versus defended prey resulted in higher rates of genetic mixing in the prey. More specifically, our results showed that fluctuating population sizes of predator and prey, coupled with a trade‐off in the prey, drove the sort of recurrent environmental change that could provide a benefit to sex in the prey, despite inherent costs. We end with a discussion of potential population genetic mechanisms underlying increased selection for sex in this system, based on our application of a general theoretical framework for measuring the effects of sex over time, and interpreting how these effects can lead to inferences about the conditions selecting for or against sexual reproduction in a system with antagonistic species interaction.     

Deleterious effects of recombination and possible nonrecombinatorial advantages of sex in a fungal model

Why sexual reproduction is so prevalent in nature remains a major question in evolutionary biology. Most of the proposed advantages of sex rely on the benefits obtained from recombination. However, it is still unclear whether the conditions under which these recombinatorial benefits would be sufficient to maintain sex in the short term are met in nature. Our study addresses a largely overlooked hypothesis, proposing that sex could be maintained in the short term by advantages due to functions linked with sex, but not related to recombination. These advantages would be so essential that sex could not be lost in the short term. Here, we used the fungus Aspergillus nidulans to experimentally test predictions of this hypothesis. Specifically, we were interested in (i) the short‐term deleterious effects of recombination, (ii) possible nonrecombinatorial advantages of sex particularly through the elimination of mutations and (iii) the outcrossing rate under choice conditions in a haploid fungus able to reproduce by both outcrossing and haploid selfing. Our results were consistent with our hypotheses: we found that (i) recombination can be strongly deleterious in the short term, (ii) sexual reproduction between individuals derived from the same clonal lineage provided nonrecombinatorial advantages, likely through a selection arena mechanism, and (iii) under choice conditions, outcrossing occurs in a homothallic species, although at low rates.     

Sex and speciation: The paradox that non-recombining DNA promotes recombination

The benefits of sexual reproduction that outweigh its costs have long puzzled biologists. Increased genetic diversity generated by new allelic combinations, as enhanced by recombination during meiosis, is considered a primary benefit of sex. Sex-determining systems have evolved independently on numerous occasions. One of the most familiar is the use of sex chromosomes in vertebrates. Other eukaryotic groups also use sex chromosomes or smaller sex-determining regions within their chromosomes, such as the mating type loci in the fungi. In these organisms, sexual reproduction and its associated meiotic recombination are controlled by regions of the genome that are themselves blocked in recombination. Non-recombining DNA that is essential for recombination presents a paradox. One hypothesis is that sex-determination requires or leads to highly diverse alleles, establishing this block in recombination. A second hypothesis to account for the common occurrence of these types of sex-determining systems is that they combine mechanisms for recombination suppression and reproductive isolation, thereby promoting the evolution of new species. The fungal kingdom represents the ideal eukaryotic lineage to elucidate the functions of non-recombining regions in sex-determination and speciation.     

Stress relief may promote the evolution of greater phenotypic plasticity in exotic invasive species: a hypothesis

Invasion ecologists have often found that exotic invaders evolve to be more plastic than conspecific populations from their native range. However, an open question is why some exotic invaders can even evolve to be more plastic given that there may be costs to being plastic. Investigation into the benefits and costs of plasticity suggests that stress may constrain the expression of plasticity (thereby reducing the benefits of plasticity) and exacerbate the costs of plasticity (although this possibility might not be generally applicable). Therefore, evolution of adaptive plasticity is more likely to be constrained in stressful environments. Upon introduction to a new range, exotic species may experience more favorable growth conditions (e.g., because of release from natural enemies). Therefore, we hypothesize that any factors mitigating stress in the introduced range may promote exotic invaders to evolve increased adaptive plasticity by reducing the costs and increasing the benefits of plasticity. Empirical evidence is largely consistent with this hypothesis. This hypothesis contributes to our understanding of why invasive species are often found to be more competitive in a subset of environments. Tests of this hypothesis may not only help us understand what caused increased plasticity in some exotic invaders, but could also tell us if costs (unless very small) are more likely to inhibit the evolution of adaptive plasticity in stressful environments in general.     

The many costs of sex

Explaining the evolution of sex is challenging for biologists. A 'twofold cost' compared with asexual reproduction is often quoted. If a cost of this magnitude exists, the benefits of sex must be large for it to have evolved and be maintained. Focusing on benefits can be misleading, as this sidelines important questions about the cost of sex: what is the source of the twofold cost: males, genome dilution or both? Does the cost deviate from twofold? What other factors make sex costly? How should the costs of sex be empirically measured? The total cost of sex and how it varies in different contexts must be known to determine the benefits needed to account for the origin and maintenance of sex.     

CHROMOSOMAL INVERSIONS AND SPECIES DIFFERENCES: WHEN ARE GENES AFFECTING ADAPTIVE DIVERGENCE AND REPRODUCTIVE ISOLATION EXPECTED TO RESIDE WITHIN INVERSIONS?

Many factors can promote speciation, and one which has received much attention is chromosomal inversions. A number of models propose that the recombination suppressing effects of inversions facilitate the maintenance of differences between interbreeding populations in genes affecting adaptive divergence and reproductive isolation. These models predict that such genes will disproportionately reside within inversions, rather than in collinear regions. This hypothesis has received some support, but exceptions exist. Additionally, the effects of known low levels of recombination within inversions on these models are uninvestigated. Here, simulations are used to compare the maintenance of genetic differences between populations following secondary contact and hybridization in different inversion models. We compare regions with no recombination within them to regions with low recombination and to collinear regions with free recombination. Our most general finding is that the low levels of recombination within an inversion often result in the loss of accentuated divergence in inverted regions compared to collinear ones. We conclude that inversions can facilitate the maintenance of species differences under some conditions, but that large or qualitative differences between inverted and collinear regions need not occur. We also find that strong selection facilitates maintenance of divergence in a manner analogous to inversions.     

The evolution of sex and recombination in response to abiotic or coevolutionary fluctuations in epistasis

Evolutionary biologists have identified several factors that could explain the widespread phenomena of sex and recombination. One hypothesis is that host-parasite interactions favor sex and recombination because they favor the production of rare genotypes. A problem with many of the early models of this so-called Red Queen hypothesis is that several factors are acting together: directional selection, fluctuating epistasis, and drift. It is thus difficult to identify what exactly is selecting for sex in these models. Is one factor more important than the others or is it the synergistic action of these different factors that really matters? Here we focus on the analysis of a simple model with a single mechanism that might select for sex: fluctuating epistasis. We first analyze the evolution of sex and recombination when the temporal fluctuations are driven by the abiotic environment. We then analyze the evolution of sex and recombination in a two-species coevolutionary model, where directional selection is absent (allele frequencies remain fixed) and temporal variation in epistasis is induced by coevolution with the antagonist species. In both cases we contrast situations with weak and strong selection and derive the evolutionarily stable (ES) recombination rate. The ES recombination rate is most sensitive to the period of the cycles, which in turn depends on the strength of epistasis. In particular, more virulent parasites cause more rapid cycles and consequently increase the ES recombination rate of the host. Although the ES strategy is maximized at an intermediate period, some recombination is favored even when fluctuations are very slow. By contrast, the amplitude of the cycles has no effect on the ES level of sex and recombination, unless sex and recombination are costly, in which case higher-amplitude cycles allow the evolution of higher rates of sex and recombination. In the coevolutionary model, the amount of recombination in the interacting species also has a large effect on the ES, with evolution favoring higher rates of sex and recombination than in the interacting species. In general, the ES recombination rate is less than or equal to the recombination rate that would maximize mean fitness. We also discuss the effect of migration when sex and recombination evolve in a metapopulation. We find that intermediate parasite migration rates maximize the degree of local adaptation of the parasite and lead to a higher ES recombination rate in the host.     

Abnormal and variable sex ratios in population samples of ladybirds

While most ladybird species are believed to show a conventional 1:1 sex ratio, population samples from five different species of ladybird have been found to show significant excesses of females. The species involved are Anatis ocellata, Exochomus quadripustulatus, Chilocorus renipustulatus, C. bipustulatus and C. nigritus. All possess neo-XY sex chromosome systems. It is possible that the excesses of females reflect the recombination of segments present at the ends of the neo-XY sex bivalent. If the products of recombination are more lethal in males than females, differences in sex ratio will result. An alternative hypothesis involves an interaction between Y-linked factors and maternally inherited factors, possibly of a transposable element type. The maintenance of such excesses of females in several species, in different taxonomic groups within the Coccinellidae, and the presence of differences in different populations of one of the species, must reflect a selective advantage for these excesses in natural populations of these species.     

Sex ratio variation in mammals

Parents will increase their fitness by varying the sex ratio of their progeny in response to differences in the costs and benefits of producing sons and daughters. Sex differences in energy requirements or viability during early growth, differences in the relative fitness of male and female offspring, and competition or cooperation between siblings or between siblings and parents might all be expected to affect the sex ratio. Although few trends have yet been shown to be consistent, growing numbers of studies have demonstrated significant variation in birth sex ratios in non-human mammals. These are commonly cited as evidence of adaptive manipulation of the sex ratio. However, several different mechanisms may affect the birth sex ratio, and not all of them are likely to be adaptive. Valid evidence that sex ratio trends are adaptive must be based either on the overall distribution of those trends or on cases in which the sex ratio can be shown to vary with the relative fitness of producing sons and daughters. The distribution of observed sex ratio trends does not conform closely to the predictions of any single adaptive theory. Some recent studies, however, indicate that, within species, the sex ratio varies with the costs or benefits of producing male or female offspring.     

Sex differences in recombination

One of the stronger empirical generalizations to emerge from the study of genetic systems is that achiasmate meiosis, which has evolved 25–30 times, is always restricted to the heterogametic sex in dioecious species, usually the male. Here we collate data on quantitative sex differences in chiasma frequency from 54 species (4 hermaphroditic flatworms, 18 dioecious insects and vertebrates and 32 hermaphroditic plants) to test whether similar trends hold. Though significant sex differences have been observed within many species, only the Liliaceae show a significant sexual dimorphism in chiasma frequency across species, with more crossing over in embryo mother cells than in pollen mother cells; chiasma frequencies are unrelated to sex and gamety in all other higher taxa studied. Further, the magnitude of sexual dimorphism, independent of sign, does not differ among the three main ecological groups (dioecious animals, plants, and hermaphroditic animals), contrary to what would be expected if it reflected sex-specific selection on recombination. These results indicate that the strong trends for achiasmate meiosis do not apply to quantitative sex differences in recombination, and contradict theories of sex-specific costs and benefits. An alternative hypothesis suggests that sex differences may be more-or-less neutral, selection determining only the mean rate of recombination. While male and female chiasma frequencies are more similar than would be expected under complete neutrality, a less absolute form of the hypothesis is more difficult to falsify. In female mice the sex bivalent has more chiasmata for its length than the autosomes, perhaps compensating for the absence of recombination in males. Finally, we observe that chiasma frequencies in males and females are positively correlated across species, validating the use of only one sex in comparative studies of recombination.     

Can resource costs of polyploidy provide an advantage to sex?

The predominance of sexual reproduction despite its costs indicates that sex provides substantial benefits, which are usually thought to derive from the direct genetic consequences of recombination and syngamy. While genetic benefits of sex are certainly important, sexual and asexual individuals, lineages, or populations may also differ in physiological and life history traits that could influence outcomes of competition between sexuals and asexuals across environmental gradients. Here, we address possible phenotypic costs of a very common correlate of asexuality, polyploidy. We suggest that polyploidy could confer resource costs related to the dietary phosphorus demands of nucleic acid production; such costs could facilitate the persistence of sex in situations where asexual taxa are of higher ploidy level and phosphorus availability limits important traits like growth and reproduction. We outline predictions regarding the distribution of diploid sexual and polyploid asexual taxa across biogeochemical gradients and provide suggestions for study systems and empirical approaches for testing elements of our hypothesis.     

Using individual-based modeling to investigate whether fluctuating resources help to explain the prevalence of sexual reproduction in animal species

The prevalence of sexual reproduction of animal species is a paradox for evolutionary theory since it remains unclear whether the evolutionary benefits of sexual reproduction outweigh the costs. One attempt at explaining the maintenance of sex is the Tangled Bank hypothesis: Sexual reproduction shuffles around alleles through crossing over and recombination, resulting in a wide range of individuals, some of whom will be able to survive in the harshest of environments with low and dwindling food resources. Whereas, with respect to clonally reproduced individuals there is arguably less genetic variation so that if food resources start to fluctuate, these individuals may not be able to survive under the new conditions. In our study, we conducted individual based modeling computer simulations using the program EcoSim to investigate two hypotheses related to fluctuating resources: First, in the context of fluctuating resources, populations of sexual species will outpace the populations of asexual species who are unable to adapt to changing conditions. The second hypothesis that we investigated is that with respect to facultative species there will be an increase in sexual reproduction and a decrease in asexual reproduction as a response to fluctuating resources. The control runs involved relatively stable food resources for obligate sexual, obligate asexual and facultatively reproducing prey species, whereas the experimental runs involved unstable fluctuating resources. Although we found that population levels were higher for obligate sexual prey vs. obligate asexual prey, this was not due to the manipulation of the independent variable, food resources, since these results were consistent across experimental, and control runs. However, in terms of the runs for facultative species, we found that in experimental runs, there was a discernably lower level of asexual reproduction and a slight increase in sexual reproduction in the later stages of the runs, which is likely a response to fluctuating resources. These results tend to confirm the hypothesis that in terms of facultative species, there will be a decrease in asexual reproduction and an increase in sexual reproduction in response to fluctuating resources. Moreover, we found that these features may be evolutionary in nature rather than simply a matter of phenotypic plasticity, which to the best of our knowledge is not a result in any other simulation or empirical study on Tangled Bank with respect to facultative species. Our study therefore contributes to the ongoing debate of whether the switch to sex in facultative species is the result of phenotypic plasticity or evolutionary in character.     

Competence increases survival during stress in Streptococcus pneumoniae

Horizontal gene transfer mediated by transformation is of central importance in bacterial evolution. However, numerous questions remain about the maintenance of processes that underlie transformation. Most hypotheses for the benefits of transformation focus on what bacteria might do with DNA, but ignore the important fact that transformation is subsumed within the broader process of competence. Accordingly, the apparent benefits of transformation might rely less on recombination than on other potential benefits associated with the broader suite of traits regulated by competence. We examined the importance of this distinction in the naturally competent species Streptococcus pneumoniae, focusing specifically on predictions of the DNA-for-repair hypothesis. We confirm earlier results in other naturally competent species that transformation protects against DNA-damaging stress. In addition, we show that the stress-protection extends to non-DNA-damaging stress. More important, we find that for some forms of stress transformation is not required for cells to benefit from the induction of competence. This rejects the narrowly defined DNA-for-repair hypotheses and provides the first support for Claverys' hypothesis that competence, but not necessarily transformation, may act as a general process to relieve stress. Our results highlight the need to distinguish benefits of transformation from broader benefits of competence that do not rely on DNA uptake and recombination.     

Constraints on the evolution of asexual reproduction

Sexual reproduction is almost ubiquitous among multicellular organisms even though it entails severe fitness costs. To resolve this apparent paradox, an extensive body of research has been devoted to identifying the selective advantages of recombination that counteract these costs. Yet, how easy is it to make the transition to asexual reproduction once sexual reproduction has been established for a long time? The present review approaches this question by considering factors that impede the evolution of parthenogenesis in animals. Most importantly, eggs need a diploid chromosome set in most species in order to develop normally. Next, eggs may need to be activated by sperm, and sperm may also contribute centrioles and other paternal factors to the zygote. Depending on how diploidy is achieved mechanistically, further problems may arise in offspring that stem from 'inbreeding depression' or inappropriate sex determination systems. Finally, genomic imprinting is another well-known barrier to the evolution of asexuality in mammals. Studies on species with occasional, deficient parthenogenesis indicate that the relative importance of these constraints may vary widely. The intimate evolutionary relations between haplodiploidy and parthenogenesis as well as implications for the clade selection hypothesis of the maintenance of sexual reproduction are also discussed.     

MUTUAL MATE CHOICE AND SEX DIFFERENCES IN CHOOSINESS

Sexual competition is associated closely with parental care because the sex providing less care has a higher potential rate of reproduction, and hence more to gain from competing for multiple mates. Sex differences in choosiness are not easily explained, however. The lower-caring sex (often males) has both higher costs of choice, because it is more difficult to find replacement mates, and higher direct benefits, because the sex providing more care (usually females) is likely to exhibit more variation in the quality of contributions to the young. Because both the costs and direct benefits of mate choice increase with increasing parental care by the opposite sex, general predictions about sex difference in choosiness are difficult. Furthermore, the level of choosiness of one sex will be influenced by the choosiness of the other. Here, we present an ESS model of mutual mate choice, which explicitly incorporates differences between males and females in life history traits that determine the costs and benefits of choice, and we illustrate our results with data from species with contrasting forms of parental care. The model demonstrates that sex differences in costs of choice are likely to have a much stronger effect on choosiness than are differences in quality variation, so that the less competitive sex will commonly be more choosy. However, when levels of male and female care are similar, differences in quality variation may lead to higher levels of both choice and competition in the same sex.     

Mate limitation causes sexes to coevolve towards more similar dispersal kernels

Sex‐specific dispersal behavior has been documented in a wide range of different species. Avoidance of inbreeding and kin competition as well as different benefits of philopatry have been invoked as explanations for these patterns. All of these factors have, however, focused on explaining why dispersal behavior differs between the sexes. In this paper, we make the case that dispersal causes an increase in spatial variability in the sex ratio which can reduce the local availability of mates, and thus feed back to influence the evolution of sex‐specific dispersal and lead to more, rather than less, similar dispersal behavior in the sexes. We investigate this mechanism in two different models, first in a conceptually simple case showing why the coevolutionary effect arises, second in an individual‐based model where we model a population in explicit space with dispersal implemented as dispersal kernels. While our mechanism is not expected to completely remove sex‐bias in dispersal, it can act alongside other selection pressures to reduce such biases. Our model thus shows that dispersal of one sex can have an effect on the selective pressures on the opposite sex, without implementing inbreeding avoidance or differential benefits or costs of dispersal.     

The evolutionary success of sex. Science & Society Series on Sex and Science

Sexual reproduction remains a major puzzle for biologists. How did it evolve and why have so many species maintained it, despite its extensive costs? Recent research is shedding light on the answers to some of these questions.Modern human society is obsessed with sex, but even a cursory glance at a natural history documentary should convince anyone that this obsession is not limited to humans. Sex is everywhere in the living world, and its consequences for almost every aspect of life, from morphology to behaviour, are profound. Given the ubiquity of sex, it is easy to forget that it is not necessary for reproduction. Indeed, there are some organisms that reproduce perfectly well without bothering with sex at all. However, the vast majority of eukaryotic species do have sex [1].Sometimes sex is occasional, such as in the malaria parasite Plasmodium falciparum, which reproduces asexually for many generations within a host, only resorting to sex when picked up by its mosquito vector. In other species, including our own, sex and reproduction are intimately linked: the latter cannot occur without the former. However, uncovering the evolutionary forces that produced and maintain this widespread characteristic of life has proven difficult, leading one evolutionary biologist to refer to understanding sex as “the Queen of problems in evolutionary biology” [1]. In this essay, I outline why the widespread existence of sex presents a problem for evolutionary biologists and examine where the solutions to this problem might be found.Given the ubiquity of sex, it is easy to forget that it is not necessary for reproductionSex means different things to different people, and so it is important to be clear about what we are trying to explain. In broad terms, sex can be viewed as any process that brings together and mixes the genetic material from different individuals into a new, single individual. By this definition, sex includes the processes of genetic exchange observed in bacteria and viruses—so-called ‘parasexual'' events—as well as the more familiar, and more elaborate, sexual cycle observed in eukaryotes [2]. However, for the purpose of this essay, when I refer to sex, I mean the eukaryotic sexual cycle (Fig 1). The reason for this is simple: whilst the outcomes of these genetic processes might be similar—and similar selective forces might even explain their early origins—the selective forces maintaining eukaryotic sex are probably fundamentally different to those that maintain the varieties of parasex in prokaryotes [3].Open in a separate windowFigure 1The core aspects of sex in eukaryotes. For simplicity, the figure shows a hypothetical organism in which the whole genome is carried in a single chromosome. The sexual cycle starts with a diploid cell that contains two different copies of the genome on a pair of homologous chromosomes. Each chromosome is first replicated to produce two genetically identical chromatids. The chromosomes then line up and exchange genetic material through recombination, producing chromatids that contain a mix of genetic material from both chromosomes. A two-stage meiotic division then leads the production of haploid gametes, each containing a single chromatid—half of the genetic material of the original diploid cell. Completion of the sexual cycle requires that diploidy is restored through the fusion of two gametes, usually from two different individuals.The key elements of the eukaryotic sexual cycle are outlined in Fig 1. Eukaryotic sex involves an alternation between haploidy and diploidy, coupled with a shuffling of genetic material. There are many variations on this general theme. Many microbial species, termed ‘isogamous'', produce gametes that are morphologically equivalent. Despite the lack of morphological distinction, the gametes usually exist in two or more mating types and fusion can only occur between gametes of different mating types. Beyond the microbial world, sexual organisms are typically anisogamous: they produce two types of morphologically distinct gamete. One type—by convention the male—is generally small and motile, whereas the other is large and stuffed with nutrients. Variation can also be seen in the ‘standard'' ploidy of certain species: some spend most of their life cycle in the diploid stage, whereas others are generally haploid, only briefly becoming diploid immediately after gamete fusion. Despite these variations on a theme, however, the core elements of the sexual cycle are remarkably conserved across eukaryotes from algae to elephants.The ubiquity of sex, coupled with the conservation of its central elements across a diversity of organisms, suggests that the selective forces responsible must be both strong and pervasive. It is therefore surprising that finding a convincing explanation for the evolutionary success of sex has proven to be one of the most difficult challenges for modern evolutionary biologists. The question is: why?Success in evolutionary terms is ultimately judged by an individual''s success in passing on genes to future generations. The simple problem with sex, from an evolutionary perspective, is that it is an extremely inefficient way of achieving this end [4]; there are several costs associated with the sexual cycle. First, there are obvious direct costs. Unless you are a self-fertile hermaphrodite, for example, it is necessary to find a mate with whom to exchange genes. This might consume considerable energy, which could otherwise be diverted to reproducing directly; for species in which sex is an obligate part of the reproductive process, failure to find a mate leads to failure to reproduce. Similarly, for species in which one sex competes for access to the other sex, considerable efforts and energies are diverted to such competition: an asexual peacock would need no elaborate tail. Even at the cellular level, the sexual cycle requires additional time and energy, as meiotic cell division takes considerably longer than simple mitosis. This time could be devoted to other purposes if sex were avoided.It is […] surprising that finding a convincing explanation for the evolutionary success of sex has proven to be one of the most difficult challenges for modern evolutionary biologistsA less obvious cost to sex that occurs in anisogamous organisms has been termed ‘the cost of males'', or as evolutionary biologist John Maynard Smith put it, the two-fold cost of sex [4]. To understand this concept, consider a hypothetical species of obligate sexual fish (Fig 2). In this species, a female produces exactly two offspring in her lifetime. All things being equal, we expect her to invest equally in male and female offspring, so one of the offspring will be male and the other female. Let us assume that the brother and sister pair up to produce the next generation—the logic applies equally well if we do not assume this, but it is easier to follow if we do. Similarly to her mother, the daughter will produce two offspring during her lifetime, and so our original female has produced two grandchildren. Imagine a mutant female that is identical to the first, except that she produces offspring asexually, which are her clones. This asexual female will also produce two offspring, but they will both be female and, unlike the offspring of her sexual cousin, they will both be able to reproduce directly, providing the original asexual female with four granddaughters (Fig 2). It is easy to see how such a demographic advantage can quickly lead to the asexual lineage replacing its sexual ancestor. Put simply, a sexual female wastes up to half of her reproductive resources producing males, which do not reproduce directly themselves.Open in a separate windowFigure 2The cost of males. The number of offspring of a hypothetical sexual species of fish and an asexual clone derived from it are shown. By not investing in male offspring, the asexual clone can double in frequency when rare.There is a further potential genetic cost of recombination in that it potentially breaks up successful combinations of genes, leading to what has been termed ‘recombination load'' [4]. Genes do not generally act independently, and an individual that has survived to reproductive age has demonstrated not only that it has good genes, but that its good genes work well in combination. An asexual organism can pass on their successful genotype intact, whereas a sexual individual risks producing less successful gene combinations by mixing their genes with those of another. Unlike the cost of males, recombination load is a problem for any sexual organism.Thus, we have a conundrum: sex is actually a costly process that ought to be lost quickly from populations. Yet, most eukaryotes are sexual. In that case, what selective benefits does sex provide that outweigh these significant costs?The basis of the sexual cycle was present in the common ancestor of all extant eukaryotic lineages. Indeed the appearance of sex pre-dates the diversification of the eukaryotes themselves, leading to suggestions that the initial spread of sex might be an incidental consequence of the success of eukaryotes, for reasons other than their sexuality [5]. So what benefits could sex have provided to their ancient sexual ancestor?The benefits of syngamy—the fusion of gametes to form a zygote—might be relatively easy to understand. Combining the two genomes of different parents allows for genetic complementation [4]. Essentially, syngamy compensates for the effects of deleterious genes in one genome by providing a functioning copy of the gene from the other genome. However, coming up with plausible explanations for the selective forces that led from here to the full sexual cycle complete with meiosis and recombination is less straightforward. One proposal is that meiosis provides a general way for a cell to repair DNA damage; another is that the benefits of meiosis derive from the genetic diversity that it creates among offspring. Both of these hypotheses have also been invoked to explain the maintenance of sex in extant species. It is worth remembering that the original sexual species would have been isogamous, and so without a two-fold cost of sex. Thus, in principle, the selective benefits required for the origin of sex might be far smaller than those required to explain its maintenance in species with distinct sexes.An intriguing alternative hypothesis is that sex might have evolved as a parasitic adaptation among selfish genetic elements to allow them to spread to other genetic lineages [6]. An analogous process can be observed in bacteria such as Escherichia coli, in which genetic exchange between cells is induced and controlled by an extrachromosomal plasmid, and seems to have evolved as a mechanism for the plasmid to move through a bacterial population.Unfortunately, the unique origin of sex, coupled with the fact that it occurred in the distant past under selective conditions about which we can only guess, and which might have changed dramatically since, makes testing theories for the evolutionary origins of sex extremely problematic. Ultimately, we might be limited to plausible stories and might never have a conclusive answer to why sex evolved in the first place.Regardless of whether we need a selective explanation for the initial spread of sex across the tree of life, we do require one for its continued maintenance against significant evolutionary costs. Furthermore, the selective forces maintaining sex must still be operating, and operating in a diversity of species. This gives evolutionary biologists some hope of observing these forces in action, as well as independent systems in which to test directly different hypotheses. The past 50 years has seen considerable amounts of research dedicated to elucidating these selective forces.One possibility is that sex is simply a mechanism for repairing DNA damage, in particular double-stranded DNA damage. This view has been championed by Harris Bernstein from the University of Arizona, USA, and others [7], and is in some ways a compelling idea. DNA damage is a problem for all organisms, and so selection based on repair would have the kind of universality required to explain the widespread nature of sex. Moreover, many of the enzymes involved in recombination do have roles in DNA repair and probably did evolve initially for that function, only later being co-opted for sex [4]. However, the argument is problematic on several levels [2]. Most obviously, there are organisms that never have sex, but do not apparently suffer from catastrophic DNA damage. Thus, my view—and I think it is also the view of most evolutionary biologists—is that the answer to the prevalence of sex is not repair, even if this was in part involved in its origin.Ultimately, we might be limited to plausible stories and might never have a conclusive answer to why sex evolved in the first placeThe main consequence of sex is that genetic material from two individuals is mixed together into a single individual, leading to the production of offspring that are genetically distinct from either parent. It is to this production of new genetic combinations that many evolutionary biologists have turned in search of an evolutionary advantage to sex. This has led to the conventional wisdom, even present in high-school textbook dogma, that the main function of sex is to increase genetic variability and consequently increase the rate at which a sexual species or population can evolve. This greater variability of sexual species would allow them to persist in the face of environmental change and competition with other species, and ultimately to diversify. By contrast, populations that give up sex are doomed to a short evolutionary lifespan and an early extinction. This logic gained further support from the fact that asexual groups seem to be generally found only at the tips of the tree of life, suggesting that they have a relatively short evolutionary lifespan [4].This simple argument is faced with at least two substantial problems. The first is that, despite appearances, the genetic mixing that results from sex is not guaranteed to increase the heritable genetic variation for fitness, which is the ultimate determinant of the rate of adaptation [8]. Indeed, initial attempts to model the process showed that whilst sex could increase the efficiency of selection, the conditions required for it to do so were by no means universal, often requiring strong selection or high mutation rates and specific types of interaction between genes affecting fitness. Even under conditions where sex was beneficial, the benefits were rarely substantial enough to outweigh the two-fold costs of producing males. Perhaps most importantly, empirical work did not provide much evidence that the stringent conditions required by these models for sex to be beneficial were generally met in real organisms.The second problem is that the process, as described above, is one of group selection; sex, it is argued, is beneficial because sexual groups are more evolutionarily successful—they have a longer evolutionary lifespan—than asexual groups [4]. Evolutionary biologists have developed a deep distrust of arguments based on group advantage, on the grounds that, despite being possible in theory, the conditions for it to operate are incredibly restrictive [9]. To understand why, consider the two forces acting on sexual reproduction. The group-selected advantage operates over a geological timescale, because changes in the frequency of sex depend on differential rates of extinction and speciation. By contrast, the benefits to an asexual mutant within a population operate much faster, as it is based on the differential birth and death rates of individuals. All things being equal, the replacement of a sexual species by a derived asexual population would be essentially instantaneous compared with the rate of group selection. Ultimately, if sex is to be maintained by this process, for every sexual population that gives up sex, a corresponding asexual population must become extinct. Unless mutations producing viable asexual mutants in sexual populations are incredibly rare—of the order of the rate of extinction of asexual populations—group selection cannot maintain sex [4]. Although I argue later that evolving asexuality might actually be difficult for some organisms, species in which sexual and asexual individuals coexist within the same populations, or in which individuals are facultatively sexual, pose extreme problems for explanations based on such long-term benefits of sex.Essentially, sex produces higher quality genotypes, and the genes for sex hitchhike to high frequency on the back of the high-fitness genotypes that they createFaced with these problems, evolutionary biologists were left in the awkward position of lacking a solid theoretical basis to explain one of the most widespread phenomena in nature [1, 4, 9]. Some looked for other selective explanations; for example, whether cyclical fluctuations in the environment, perhaps caused by co-evolving parasites [10], could lead to situations in which it would be selectively beneficial for offspring to be genetically different from their parents. However, these models also showed that sex is only substantially beneficial under limited and extreme conditions, which do not generally appear in nature [8].Yet, work has shown that these problems might be more hypothetical than real. The original models made simplifying and often unrealistic assumptions about natural populations [8]. For example, most assumed that populations were infinite and well mixed, whereas most actual populations are relatively small and structured. Incorporating additional realism into the models has broadened considerably the range of conditions under which sex is predicted to be beneficial. Moreover, the original models typically examined a single evolutionary process at a time, for example the purging of deleterious mutations, or the bringing together of beneficial mutations. This was done in part for practical reasons, but also because there was a feeling that the ubiquity of sex would require a single explanation. However, new models that incorporate multiple selective processes operating simultaneously predict far more substantial benefits of sex than do those that model the effects independently [11]. These new models also show clearly that the benefits of sex can apply at the level of the gene and do not require the invocation of group or species selection [2, 8]. Essentially, sex produces higher quality genotypes, and the genes for sex hitchhike to high frequency on the back of the high-fitness genotypes that they create.In addition to these new theoretical insights, work in experimental microbial systems has begun to examine directly the evolutionary consequences of sex. The overwhelming conclusion of this work is that sex can provide benefits in real organisms as well as in theory. For example, work from my own lab shows that populations of Chlamydomonas, a facultatively sexual single-celled alga, adapt more rapidly to new environments when they are allowed to go through occasional sexual cycles [12]. Similar patterns have been observed in other microbes.Finally, people have begun to look again at the costs of sex, and there has been an increasing acceptance that the importance of some costs might have been overstated. The two-fold cost associated with the production of males, for example, assumes that mutations can produce ‘perfect asexuals''—organisms that produce only asexual female offspring but are otherwise identical to their sexual ancestor. In fact, once a species has been sexual for a period of time, subsequent evolutionary changes might actually make rapid reversion to cost-free asexuality extremely difficult [13]. Asexual mutants are often difficult to produce in the lab, and when they can be produced, they are often extremely sick. A process of chromosomal imprinting in mammals means that unless an individual receives chromosomes from two parents, development fails. This represents an obvious constraint to the loss of sex in this group, and similar situations might well exist in other taxa.In a complex world in which environments are constantly changing […] the differences produced by the sexual cycle provide an important evolutionary advantageIn taxa where sex has been lost, for example, some of the vestiges of sex remain. Some whiptail lizard populations consist entirely of asexual females, but these females still have to mate, despite having lost the need for sex, as the physical act of copulation is required to stimulate egg production. Such populations achieve this end by stealing mates from the males of neighbouring sexual whiptail populations, and it means that not all of the costs associated with sex in this species have been lost [4]. Other costs might be reduced by the careful timing of sex. In many microbes, sex occurs in situations in which conditions for population growth are limited and population density is high, such as the end of the growing season. This timing might considerably reduce the opportunity costs of the time-consuming sexual cycle, as well as the costs of finding a mate [14]. Thus, smaller benefits might often be required to maintain sex in many species than has generally been assumed.Thus, it seems that the original intuition of evolutionary biologists was correct after all: the evolutionary success of sex is down to the diversity that it creates [8, 14]. In a complex world in which environments are constantly changing, competitors, parasites and prey are constantly evolving and mutation is continually eroding adaptation, the differences produced by the sexual cycle provide an important evolutionary advantage. This advantage favours genes for sex and recombination within populations, and can also have profound implications for the evolutionary lifespan of populations and species. Still, some problems remain to be solved. In general, it seems that even occasional sex is sufficient for providing most of the associated evolutionary benefits discussed above, so the important question of why animals such as us have adopted sex as an obligate part of reproduction remains to be answered. Similarly, our understanding of how different selective forces that act on differences in species biology and ecology lead to patterns in the phylogenetic and geographical distribution of sex is still at its early stages. Finally, the favoured theories suppose that the loss of sex leads to a short evolutionary lifespan for a lineage. Thus, explaining the persistence of ‘ancient asexuals'', such as the bdelloid rotifers that apparently gave up sex more than 80 million years ago, presents a challenge [15]. Despite these outstanding issues, it seems that the ‘Queen of problems'' might be close to abdication.? Open in a separate windowNick Colegrave

Science & Society Series on Sex and Science

Sex is the greatest invention of all time: not only has sexual reproduction facilitated the evolution of higher life forms, it has had a profound influence on human history, culture and society. This series explores our attempts to understand the influence of sex in the natural world, and the biological, medical and cultural aspects of sexual reproduction, gender and sexual pleasure.     

Identification of a novel sex determining chromosome in cichlid fishes that acts as XY or ZW in different lineages

Sex determination systems are highly conserved among most vertebrates with genetic sex determination, but can be variable and evolve rapidly in some. Here, we study sex determination in a clade with exceptionally high sex chromosome turnover rates. We identify the sex determining chromosomes in three interspecific crosses of haplochromine cichlid fishes from Lakes Victoria and Malawi. We find evidence for different sex determiners in each cross. In the Malawi cross and one Victoria cross the same chromosome is sex-linked but while females are the heterogametic sex in the Malawi species, males are the heterogametic sex in the Victoria species. This chromosome has not previously been reported to be sex determining in cichlids, increasing the number of different chromosomes shown to be sex determining in cichlids to 12. All Lake Victoria species of our crosses are less than 15,000 years divergent, and we identified different sex determiners among them. Our study provides further evidence for the diversity and evolutionary flexibility of sex determination in cichlids, factors which might contribute to their rapid adaptive radiations.