Cost Of Sex Research Articles

The origination events of gametic sexual reproduction and anisogamy

The evolution of gametic sex (meiosis and fertilization) and subsequent transition from isogamy (fusion between two equal-sized gametes) to anisogamy (dimorphism into eggs and sperm, namely, females and males) is one of the largest enigmas of evolutionary biology. Meiosis entails genome-dilution cost and anisogamy entails male-production cost. Despite much progress has been made for the maintenance mechanisms of sex, its origination events under such “twofold cost of sex” are still unsolved. Here, we posit two hypothetical scenarios as follows: the “Seesaw Effect” hypothesizes that automictic selfing between isogametes effectively purged deleterious mutations from an organism’s lineage and simultaneously fixed the sex-controlling allele and all other loci (no genome-dilution cost raised). The high relatedness among homoeologous cell colonies led to multicellularization. The “inflated isogamy” hypothesizes that multicellularity increased the reproductive investment of both mates, resulting in excessively large isogametes. This redundancy induced cheating of one sex (evolving to male) to reduce gamete size. However, the other sex (evolving to female) allowed this cheat because her cost did not change. Therefore, anisogamy originated as a kind of commensalism but turned into beneficial for females because it solved the gamete limitation problem inherent to isogamy. Thus, smooth transition to anisogamy had been attained.

Increased adaptability to sudden environmental change can more than make up for the two-fold cost of males(a)(a)Contribution to the Focus Issue Evolutionary Modeling and Experimental Evolution edited by José Cuesta, Joachim Krug and Susanna Manrubia.

The famous “two-fold cost of sex” is really the cost of anisogamy – why should females mate with males who do not contribute resources to offspring, rather than isogamous partners who contribute equally? In typical anisogamous populations, a single very fit male can have an enormous number of offspring, far larger than is possible for any female or isogamous individual. If the sexual selection on males aligns with the natural selection on females, anisogamy thus allows much more rapid adaptation via super-successful males. We show via simulations that this effect can be sufficient to overcome the two-fold cost and favor anisogamy over isogamy in populations adapting to environmental change. The key quantity is the variance in male fitness – if this exceeds what is possible in an isogamous population, anisogamous populations can win out in direct competition by adapting faster. This advantage in adaptability is particularly effective at maintaining anisogamy against invasion by isogamy. We discuss the extensions to our simple model needed to determine how important this mechanism is to overcoming the two-fold cost in natural populations.

The two-fold cost of sex: experimental evidence from a natural system.

Over four decades ago, John Maynard Smith showed that a mutation causing asexual reproduction should rapidly spread in a dioecious sexual population. His reasoning was that the per‐capita birth rate of an asexual population would exceed that of a sexual population, because asexual females do not invest in sons. Hence, there is a cost of sexual reproduction that Maynard Smith called the “cost of males.” Assuming all else is otherwise equal among sexual and asexual females, the cost is expected to be two‐fold in outcrossing populations with separate sexes and equal sex ratios. Maynard Smith's model led to one of the most interesting questions in evolutionary biology: why is there sex? There are, however, no direct estimates of the proposed cost of sex. Here, we measured the increase in frequency of asexual snails in natural, mixed population of sexual and asexual snails in large outdoor mesocosms. We then extended Maynard Smith's model to predict the change in frequency of asexuals for any cost of sex and for any initial frequency of asexuals. Consistent with the “all‐else equal” assumption, we found that the increase in frequency of asexual snails closely matched that predicted under a two‐fold cost.

What do isogamous organisms teach us about sex and the two sexes?

Isogamy is a reproductive system where all gametes are morphologically similar, especially in terms of size. Its importance goes beyond specific cases: to this day non-anisogamous systems are common outside of multicellular animals and plants, they can be found in all eukaryotic super-groups, and anisogamous organisms appear to have isogamous ancestors. Furthermore, because maleness is synonymous with the production of small gametes, an explanation for the initial origin of males and females is synonymous with understanding the transition from isogamy to anisogamy. As we show here, this transition may also be crucial for understanding why sex itself remains common even in taxa with high costs of male production (the twofold cost of sex). The transition to anisogamy implies the origin of male and female sexes, kickstarts the subsequent evolution of sex roles, and has a major impact on the costliness of sexual reproduction. Finally, we combine some of the consequences of isogamy and anisogamy in a thought experiment on the maintenance of sexual reproduction. We ask what happens if there is a less than twofold benefit to sex (not an unlikely scenario as large short-term benefits have proved difficult to find), and argue that this could lead to a situation where lineages that evolve anisogamy-and thus the highest costs of sex-end up being associated with constraints that make invasion by asexual reproduction unlikely (the 'anisogamy gateway' hypothesis).This article is part of the themed issue 'Weird sex: the underappreciated diversity of sexual reproduction'.

Relative effects of segregation and recombination on the evolution of sex in finite diploid populations

The mechanism of reproducing more viable offspring in response to selection is a major factor influencing the advantages of sex. In diploids, sexual reproduction combines genotype by recombination and segregation. Theoretical studies of sexual reproduction have investigated the advantage of recombination in haploids. However, the potential advantage of segregation in diploids is less studied. This study aimed to quantify the relative contribution of recombination and segregation to the evolution of sex in finite diploids by using multilocus simulations. The mean fitness of a sexually or asexually reproduced population was calculated to describe the long-term effects of sex. The evolutionary fate of a sex or recombination modifier was also monitored to investigate the short-term effects of sex. Two different scenarios of mutations were considered: (1) only deleterious mutations were present and (2) a combination of deleterious and beneficial mutations. Results showed that the combined effects of segregation and recombination strongly contributed to the evolution of sex in diploids. If deleterious mutations were only present, segregation efficiently slowed down the speed of Muller's ratchet. As the recombination level was increased, the accumulation of deleterious mutations was totally inhibited and recombination substantially contributed to the evolution of sex. The presence of beneficial mutations evidently increased the fixation rate of a recombination modifier. We also observed that the twofold cost of sex was easily to overcome in diploids if a sex modifier caused a moderate frequency of sex.

The Paradox of Sexual Reproduction and the Levels of Selection: Can Sociobiology Shed a Light?

The rejection of group selection in the 1960s left the evolutionary maintenance of sex bereft of its previous explanations and turned it into an anomaly or paradox. While the levels of selection debate advanced towards multilevel selection theory as a tentative resolution, the paradox of sex became increasingly decoupled from it. Only differential extinction or speciation of sexual and asexual taxa have been considered in relation to the maintenance of sex. This agrees with multilevel selection scenario 2 (MLS2) in which the groups have their own component of fitness. In multilevel selection scenario 1 (MLS1), however, groups can structure selection without having their own component of fitness. Moreover, MLS1 defines trait-groups via social interactions. Here I suggest that MLS1 can be applied to the maintenance of sexual reproduction against the twofold cost of sex. This neither denies the existence of other costs of sex nor the legitimacy of other hypotheses concerning these costs.

DIFFERENTIAL SELECTION BETWEEN THE SEXES AND SELECTION FOR SEX

Anisogamy is known to generate an important cost for sexual reproduction (the famous "twofold cost of sex"). However, male-female differences may have other consequences on the evolution of sex, due to the fact that selective pressures may differ among the sexes. On the one hand, intralocus sexual conflict should favor asexual females, which can fix female-beneficial, male-detrimental alleles. On the other hand, it has been suggested repeatedly that sexual selection among males may help to purge the mutation load, providing an advantage to sexual females. However, no analytical model has computed the strength of selection acting on a modifier gene affecting the frequency of sexual reproduction when selection differs between the sexes. In this article, we analyze a two-locus model using two approaches: a quasi-linkage-equilibrium (QLE) analysis and a local stability analysis, whose predictions are verified using a multilocus simulation. We find that costly sex can be maintained when selection is stronger in males than in females, but acts in the same direction in both. Complete asexuality, however, evolves under any other form of selection. Finally, we discuss how experimental measurements of fitness variances and covariances between sexes could be used to determine the overall direction and strength on selection for sex arising from differences in selection between males and females.

Individual optimization efforts and population dynamics: a mathematical model for the evolution of resource allocation strategies, with applications to reproductive and mating systems

We develop a formal framework for the optimal allocation of limited resources that includes and clarifies the interplay between individual optimization and the resulting effects at the population level. As an example, in regard to the evolution of sexual recombination, the paradox of the twofold cost of sex is avoided by distinguishing between the evolution of recombination and the subsequent emergence and stability of different mating types as a result of individual optimization within a population that benefits from recombination.

The potential role of chromosome telomere resetting consequent upon sex in the population dynamics of aphids: an hypothesis

Models of population structure have emphasized the importance of sex in maintaining lineages. This is because, despite the well known ‘two-fold cost of sex’ compared with asex, it is considered that recombination rids the genome of accumulated mutations and increases its potential for adaptive variation. However, asexual lineages of eukaryotic organisms can also rapidly gain genetic variance directly by various mutational processes, thereby proving that so-called ‘clones’ do not have strict genetic fidelity (Lushai & Loxdale, 2002; Loxdale & Lushai, 2003a), whereas the variation so produced may well have adaptive advantage during the evolutionary process. This being so, obligated asexuals or cyclical parthenogens that occasionally indulge in sexual recombination (‘rare sex’) cannot be deemed as ‘evolutionary dead-ends’(Lushai, Loxdale & Allen, 2003a). In addition, the persistence of asexual lineages (i.e. lineage longevity) may also involve the integrity of the telomere region, the physical end of the chromosomes (Loxdale & Lushai, 2003b). In this earlier study on this topic, we argued that the persistence and ultimate senescence of eukaryotic cell lineages (based upon the frequency of ‘capped’ and ‘uncapped’ chromosomes related to telomere functionality; Blackburn, 2000) may directly relate to the survival and persistence of lineages of whole asexual organisms. Aphids are a good model system to test this hypothesis because they show a variety of sexual/asexual reproductive strategies, whereas their mode of asexual reproduction is of the mitotic (= apomictic) type. We also suggested that many aphid lineages require occasional or even rare sexual recombination to re-set telomere length to allow lineages to persist. Ample empirical evidence from diverse taxa, lineages, and different developmental stages now reveals that the telomere states are indeed re-set by recombination (homologous or meiotic), thereby rejuvenating the lineage in question. The generational clock element of telomeric functionality has also been successfully described in artificially-induced mammalian clonal systems. It thus appears that telomere function is a central molecular mechanism instigating and promoting lineage continuity per se. By contrast, we hypothesized that other long-lived asexuals, or the rare category of ancient asexuals such as bdelloid rotifers, have compensatory mechanisms for maintaining chromosome functional integrity, which are somewhat different from conventional telomeric repeats. In the present study, we carry the analogy between eukaryotic cell functionality and aphid lineages a stage further. Here, we hypothesize that the changing frequency of capped and uncapped telomeres, progressing to senescence in a stochastic manner, may be an underlying factor that significantly contributes to population dynamics in asexual lineage evolution.

Sex increases the efficacy of natural selection in experimental yeast populations

Why sex evolved and persists is a problem for evolutionary biology, because sex disrupts favourable gene combinations and requires an expenditure of time and energy. Further, in organisms with unequal-sized gametes, the female transmits her genes at only half the rate of an asexual equivalent (the twofold cost of sex). Many modern theories that provide an explanation for the advantage of sex incorporate an idea originally proposed by Weismann more than 100 years ago: sex allows natural selection to proceed more effectively because it increases genetic variation. Here we test this hypothesis, which still lacks robust empirical support, with the use of experiments on yeast populations. Capitalizing on recent advances in the molecular biology of recombination in yeast, we produced by genetic manipulation strains that differed only in their capacity for sexual reproduction. We show that, as predicted by the theory, sex increases the rate of adaptation to a new harsh environment but has no measurable effect on fitness in a new benign environment where there is little selection.

Coexistence of a sexual and an unisexual form stabilized by parasites

An unisexual species (either parthenogenetic or gynogenetic form) often coexists sympatrically with a closely related anisogamous sexual species, forming a unisexual complex. This is puzzling because, all else being equal, a sexual population with the two-fold cost of sex (or the cost of producing males) cannot coexist with a unisexual population. This suggests that some ecological processes are at work to make possible the coexistence of the unisexual complex. Field and laboratory studies suggest that parasitism in a gynogenetic complex of the Japanese crucian carp ( Carassius auratus) may play an important role in realizing the coexistence by giving frequency-dependent benefit to sexual population. Here, we study the simple dynamics of host–parasite interactions in which non-specific immune reaction of a sexual host is more effective than that of an unisexual host. We simply assume that the infective individuals are sterile. Stable coexistence of a unisexual species with their sexual relative is possible if pathogens are virulent and if the susceptibility of the unisexual form is more than twice as high as that of the sexual form. The coexistence is more difficult, when the fertility of males is relatively low in gynogenetic complexes. This implies that the coexistence of gynogenetic complexes is more difficult than that of parthenogenetic complexes in which parthenogenesis has no constraint on males. We conclude that parasitism is a promising candidate mechanism for the coexistence of unisexual complexes.

Eliminating the cost of sex with sexual selection

Why should males be so common when, in many species, they contribute few resources to the production and rearing of offspring? Indeed, if males do not provision offspring, a sexual species that divides resources evenly between daughters and sons would halve its intrinsic growth rate relative to an ecologically equivalent asexual species that invests only in daughters. What advantage might pay for this twofold cost of sex? Two recent papers 1xSexual selection and the maintenance of sexual reproduction. Agrawal, A.F. Nature. 2001; 411: 692–695Crossref | PubMed | Scopus (153)See all References, 2xSexual selection and the maintenance of sex. Siller, S. Nature. 2001; 411: 689–692Crossref | PubMed | Scopus (133)See all References suggest that sexual reproduction might allow the more efficient purging of deleterious mutations from the genome as a result of sexual selection. If males that succeed in siring offspring carry fewer deleterious mutations than does the average male within a population, deleterious mutations are eliminated without reducing either the fitness of females or the growth rate of a population.The idea that females might choose mates that carry ‘good genes’ is an old one. What is novel in these papers is that the authors determine the extent to which sexual selection reduces the load of deleterious mutations and whether this could offset the cost of sex. With strong enough sexual selection and a high enough mutation rate, they find that the cost of sex can be completely repaid. For example, Siller 2xSexual selection and the maintenance of sex. Siller, S. Nature. 2001; 411: 689–692Crossref | PubMed | Scopus (133)See all References2 found that, with a mutation rate of U = 1 per diploid genome per generation, sexual selection can balance the twofold cost of sex as long as males that reproduce bear, on average, 0.25 standard deviations fewer deleterious mutations than does the average male. This result assumes that each mutation is weakly selected (causing a 1% fitness reduction, hs, in heterozygotes), that the number of mutations (m) is normally distributed, and that females choose among the males that they encounter on the basis of a male trait correlated with m.Agrawal 1xSexual selection and the maintenance of sexual reproduction. Agrawal, A.F. Nature. 2001; 411: 692–695Crossref | PubMed | Scopus (153)See all References1 considered how much stronger the combination of natural and sexual selection against deleterious mutations in males would have to be than selection in females for the twofold cost of sex to be removed. With U = 1 and hs = 0.01, selection that is 5.6 times stronger in males than in females suffices to make sexual populations fitter, on average, than asexual populations. Even in species with a low mutation rate, sexual selection could increase the chance that fathers are better matched to the current environmental conditions (including the biotic environment posed by parasites, competitors, and predators) than the average male, which could also reduce or eliminate the cost of sex.The beauty of these ideas is that they rely on assumptions that can often be met: (a) mate choice or male–male competition occurs; and (b) compared with males that remain unmated, sexually selected males pass on genes that, on average, increase the fitness of their offspring. Although these theoretical models might not explain the maintenance of sex in every species, they do suggest that males, when properly chosen, might not be so bad after all.

Counting the cost of sex

Henry Gee reports on a possible solution of one of the great puzzles of biology: why did sex evolve?