Sexual selection for rare beneficial mutations promotes the evolution of sexual reproduction and adaptation

The evolution and widespread maintenance of sexual reproduction remains a conundrum in biology because asexual reproduction should allow twice the reproductive rate. One hypothesis is that sexual selection lessens the negative impact on fitness of accumulating deleterious mutations. However, for adaptation to occur, there must also be selection for beneficial mutations. Here we show that sexual selection can help explain the evolution and maintenance of sexual reproduction. In our model, females chose males with more beneficial mutations (as opposed to just fewer harmful ones) even when these occurred much more rarely. Sexual selection thereby increased fixation of beneficial mutations which increased the absolute genetic quality of sexual offspring. This increase in fitness relative to asexual offspring adds to the previously postulated effect of reduced mutation load in offsetting the cost of sex. Analysing our simulations reveals that female choice among males raised the fitness of reproducing males above that of females. We found that this effect could overcome the decline in average fitness that occurs when mutation rate increases, allowing an increase in the fixation of beneficial mutations. Sexual selection thereby not only facilitates the evolution of sexual reproduction but maintains sex by leveraging its benefits and driving adaptation.

Identifying the fitness consequences of sex in complex natural environments

In the natural world, sex prevails, despite its costs. While much effort has been dedicated to identifying the intrinsic costs of sex (e.g. the cost of males), few studies have identified the ecological fitness consequences of sex. Furthermore, correlated biological traits that differ between sexuals and asexuals may alter these costs, or even render the typical costs of sex irrelevant. Here we use a large-scale transplant experiment of a North American wildflower to show that sex is associated with reduced lifetime fitness, despite lower herbivory. We separate the effects of sex from hybridity, finding that over-winter survival is elevated in asexuals regardless of hybridity, but herbivores target hybrid asexuals. Survival is lowest in homozygous sexual lineages, implicating inbreeding depression as a cost of sex. Our results show that the consequences of sex are shaped by complex natural environments, correlated traits, and the identity of mates, rather than sex itself.

Increased adaptability to rapid environmental change can more than make up for the two-fold cost of males

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 maintain anisogamy against 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.

Daphnia invest in sexual reproduction when its relative costs are reduced

The timing of sex in facultatively sexual organisms is critical to fitness, due to the differing demographic consequences of sexual versus asexual reproduction. In addition to the costs of sex itself, an association of sex with the production of dormant life stages also influences the optimal use of sex, especially in environments where resting eggs are essential to survive unfavourable conditions. Here we document population dynamics and the occurrence of sexual reproduction in natural populations of Daphnia magna across their growing season. The frequency of sexually reproducing females and males increased with population density and with decreasing asexual clutch sizes. The frequency of sexually reproducing females additionally increased as population growth rates decreased. Consistent with population dynamic models showing that the opportunity cost of sexual reproduction (foregoing contribution to current population growth) diminishes as populations approach carrying capacity, we found that investment in sexual reproduction was highest when asexual population growth was low or negative. Our results support the idea that the timing of sex is linked with periods when the relative cost of sex is reduced due to low potential asexual growth at high population densities. Thus, a combination of ecological and demographic factors affect the optimal timing of sexual reproduction, allowing D. magna to balance the necessity of sex against its costs.

Signatures of the evolution of parthenogenesis and cryptobiosis in panagrolaimid nematodes

Most animal species reproduce sexually, but parthenogenesis, asexual reproduction of various forms, has arisen repeatedly. Parthenogenetic lineages are usually short lived in evolution; though in some environments parthenogenesis may be advantageous, avoiding the cost of sex.Panagrolaimusnematodes have colonised environments ranging from arid deserts to arctic and antarctic biomes. Many are parthenogenetic, and most have cryptobiotic abilities, being able to survive repeated complete desiccation and freezing. It is not clear which genomic and molecular mechanisms led to the successful establishment of parthenogenesis and the evolution of cryptobiosis in animals in general. At the same time, model systems to study these traits in the laboratory are missing.We compared the genomes and transcriptomes of parthenogenetic and sexualPanagrolaimusable to survive crybtobiosis, as well as a non-cryptobioticPropanogrolaimusspecies, to identify systems that contribute to these striking abilities. The parthenogens are most probably tripoids originating from hybridisation (allopolyploids). We identified genomic singularities like expansion of gene families, and selection on genes that could be linked to the adaptation to cryptobiosis. AllPanagrolaimushave acquired genes through horizontal transfer, some of which are likely to contribute to cryptobiosis. Many genes acting inC. elegansreproduction and development were absent in distant nematode species (including the Panagrolaimids), suggesting molecular pathways cannot directly be transferred from the model system.The easily culturedPanagrolaimusnematodes offer a system to study developmental diversity in Nematoda, the molecular evolution of parthenogens, the effects of triploidy on genomes stability, and the origin and biology of cryptobiosis.

Diapause and maintenance of facultative sexual reproductive strategies

Facultative sex combines sexual and asexual reproduction in the same individual (or clone) and allows for a large diversity of life-history patterns regarding the timing, frequency and intensity of sexual episodes. In addition, other life-history traits such as a diapause stage may become linked to sex. Here, we develop a matrix modelling framework for addressing the cost of sex in facultative sexuals, in constant, periodic and stochastically fluctuating environments. The model is parametrized using life-history data from Brachionus calyciflorus , a facultative sexual rotifer in which sex and diapause are linked. Sexual propensity was an important driver of costs in constant environments, in which high costs (always > onefold, and sometimes > twofold) indicated that asexuals should outcompete facultative sexuals. By contrast, stochastic environments with high temporal autocorrelation favoured facultative sex over obligate asex, in particular, if the penalty to fecundity in ‘bad’ environments was large. In such environments, obligate asexuals were constrained by their life cycle length (i.e. time from birth to last reproductive adult age class), which determined an upper limit to the number of consecutive bad periods they could tolerate. Nevertheless, when facultative asexuals with different sexual propensities competed simultaneously against each other and asex, the lowest sex propensity was the most successful in stochastic environments with positive autocorrelation. Our results suggest that a highly specific mechanism (i.e. diapause linked to sex) can alone stabilize facultative sex in these animals, and protect it from invasion of both asexual and pure sexual strategies. This article is part of the themed issue ‘Weird sex: the underappreciated diversity of sexual reproduction’.

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’.