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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2016 Oct 19;371(1706):20150539. doi: 10.1098/rstb.2015.0539

Condition-dependent sex: who does it, when and why?

Yoav Ram 1, Lilach Hadany 1,✉
PMCID: PMC5031623  PMID: 27619702

Abstract

We review the phenomenon of condition-dependent sex—where individuals' condition affects the likelihood that they will reproduce sexually rather than asexually. In recent years, condition-dependent sex has been studied both theoretically and empirically. Empirical results in microbes, fungi and plants support the theoretical prediction that negative condition-dependent sex, in which individuals in poor condition are more likely to reproduce sexually, can be evolutionarily advantageous under a wide range of settings. Here, we review the evidence for condition-dependent sex and its potential implications for the long-term survival and adaptability of populations. We conclude by asking why condition-dependent sex is not more commonly observed, and by considering generalizations of condition-dependent sex that might apply even for obligate sexuals.

This article is part of the themed issue ‘Weird sex: the underappreciated diversity of sexual reproduction’.

Keywords: sexual reproduction, evolution of sex, stress-induced variation, fitness-associated recombination, abandon-ship

1. Introduction

Sex can be classified as obligate or facultative. Obligate sexual organisms only reproduce sexually, never asexually, while facultative organisms can switch between sexual and asexual reproduction. Facultative sex is common [1–3]: many higher plants reproduce by both cross-pollination and self-pollination or vegetative reproduction [4]; various forms of parthenogenesis are found in insects, such as thelytoky, in which females hatch from unfertilized eggs [5]; several vertebrates reproduce mostly sexually but occasionally via parthenogenesis [6]; and numerous unicellular eukaryotes reproduce mostly asexually but occasionally via sex and meiosis [2,7]. Many facultative organisms exhibit condition-dependent sex, switching between sexual and asexual reproduction depending on the condition of the individual in the current environment.

This review is focused on negative dependence: where sexual reproduction is more common among individuals in poor condition. Such negative dependence can occur due to either environmental or individual phenotypic variation. It has long been known that in certain species the level of sexual reproduction is regulated according to environmental cues [1,8] (environment-dependent sex, figure 1c). When the environmental cue indicates a detrimental change (e.g. extreme temperature or desiccation), such regulation would result in negative association between condition and sex. By contrast, sexual reproduction can also be regulated as a response to internal stress cues, allowing within-population variation in sexual reproduction. In such ‘condition-dependent sex’ (figure 1b,d), individuals in poor condition reproduce sexually more often than individuals in better condition, even under the same environmental conditions [9]. Of course, the condition of an individual is determined by the interaction between its genotype and the environment. Thus, a population employing condition-dependent sex could show increased overall levels of sex in stressful environments, due to an increased fraction of stressed individuals who tend towards sexual reproduction (figure 1).

Figure 1.

Figure 1.

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Frequency of sexual reproduction over time under different sexual strategies. (a) Uniform sex, where all the individuals have the same tendency for sexual reproduction, irrespective of condition or environment, and the variance is due to random effects only. (b) Condition-dependent sex, constant environment, where low- and high-quality individuals have high and low frequency of sexual reproduction, respectively (red for low-quality individuals, blue for high-quality ones). The mean frequency of sex (grey) is equal to that of the population with a uniform frequency in (a), but the variance in the frequency of sex is much higher. (c) Environment-dependent sex, where the frequency of sexual reproduction depends on environmental cues (red arrows). The variance in the frequency of sex is low at any given time point, but high over time. (d) Condition-dependent sex in a changing environment. Low- and high-quality individuals have high and low frequency of sexual reproduction, as in (b), but the fraction of low-quality individuals depends on environmental conditions. After an environmental change (red arrow) most of the population is maladapted, or low quality, and reproduces sexually at the high rate (red line). The variance in the frequency of sex is high at any given time point and high over time.

2. The evolution of condition-dependent sex

Evolutionary advantages to condition-dependent variation were first proposed in the context of condition-dependent recombination [10–12] and later extended to condition-dependent sexual reproduction [9,13] and to other mechanisms of genetic variation [11,14–16]. In essence, an allele that regulates a facultative reproductive system could benefit from following the abandon-ship principle [9]: switching to sexual reproduction in maladapted individuals but reproducing asexually in well-adapted ones, thereby associating itself with good genetic backgrounds (figure 2). This advantage can drive the evolution of condition-dependent sex under different scenarios, including mutation-selection balance [9], adaptation [13] and host parasite coevolution [17].

Figure 2.

Figure 2.

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The abandon-ship principle. Considering haploid organisms, whose genotypes consist of two loci: the first is a fitness locus, in which alleles A and a are the high and low fitness alleles, respectively; the second is a facultative sexual reproduction modifier in which U induces a uniform rate of sexual reproduction and C induces a condition-dependent rate of sex. The illustration focuses on the only mating combinations that can alter genotype frequencies via sex: AU × aC and aU × AC. On the left, aC and AU produce all four genotypes, because both aC and AU are likely to reproduce sexually. On the right, AC is unlikely to reproduce sexually, due to the interaction of the high fitness allele A and the condition-dependent modifier C. As a result, AC and aU are over-represented in the F1 generation (middle). That is, A and C become positively associated.

Condition-dependent sex can evolve even when the costs of sex are high. Sexual reproduction can be costly due to production of males and male gametes [18], reduced relatedness between mothers and offspring [19], failure to find suitable mates [20,21], conflict between the sexes [22] and more [23–25]. High costs of sex are restrictive to the evolution of uniform sex in classical models, where all individuals reproduce sexually with the same probability [26]. By contrast, condition-dependent sex is advantageous even under high costs, due to the abandon-ship principle. Intuitively, individuals carrying maladapted genomes can risk costly sexual reproduction because the chances for long-term survival of their genes under asexual reproduction are already low.

Environment-dependent sex can also be advantageous if there is a significant benefit in syncing sexual reproduction across a population, for example, when population density is low. In these cases, switching to sexual reproduction in response to a specific environmental cue (e.g. length of daylight) can be viewed as a social contract rather than an actual response to the condition. On the other hand, organisms in which either the asexual or the sexual form is more resistant to unfavourable environmental conditions [27–29] can be expected to link their reproduction mode to environmental conditions due to direct benefits of survivability or growth. These different factors might combine into a form of environment-dependent sex that does not involve the abandon-ship principle: cases where synchronization of the sexual cycle is cued by a stressful condition, and production of an advantageous stable stage (e.g. spores or seeds) requires sexual reproduction. In these cases, we can expect to see a mostly asexual population experiencing bursts of sexual reproduction and genetic variation during stressful episodes, with potential benefits at the population level (see summary in table 1).

Table 1.

Factors determining dependence of reproduction mode on condition.

factor positive/negative condition dependence evolutionary causes
abandon-ship principle − regulating allele becomes associated with good genetic backgrounds
higher costs of sex under poor condition + maladapted individuals benefit less from sex
sexual selection + fit individuals benefit more from sex due to sexual selection
syncing sexual reproduction across the population +/− synchronization reduces the cost of finding a mate, especially in low density or immobile populations
resistant phenotype +/− the reproductive mode associated with the resistant phenotype would be favoured under stress
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In the rest of this review, we (i) discuss empirical evidence of the phenomenon; (ii) describe the potential implications of condition-dependent sex on adaptation and diversity; (iii) consider the reasons that we do not observe condition-dependent sex more often in nature despite its advantages; (iv) examine the more general phenomenon of condition-dependent variation, which might be beneficial even to obligate sexuals; and (v) call for additional research into some of the questions that remain open.

3. Empirical evidence

The majority of studies of condition-dependent sex consider the amount of sexual reproduction in entire populations under different conditions. Hereafter, we try to emphasize cases where variation in sex, in correlation with individual condition, was observed within populations.

(a). Multicellular organisms

Condition-dependent sex has been observed in several multicellular organisms [1]. The crustacean Daphnia magna mostly reproduces through parthenogenesis when conditions favour growth, but starts producing males and sexual eggs under a variety of stress conditions, including population density, starvation and extreme temperatures [30,31]. Interestingly, during a pathogen epidemic host genotypes that were more susceptible also showed a greater tendency for sex [23].

The nematode Strongyloides ratti is a common rat gut parasite. It is a laboratory analogue of Strongyloides stercoralis, a human parasite that infects 100–200 million people worldwide [32]. S. ratti has a facultative free-living sexual reproduction cycle, and it has been shown that stress caused by host immune responses leads to a higher proportion of sexual reproduction [33,34]. Sex does not lead to a stable or resistant stage in this organism, suggesting a possible advantage to genetic variation under host immune stress. Similarly, in the soil nematode Caenorhabditis elegans, starvation and passage through a dauer stage increased the frequency of males and the frequency of sexual reproduction [35].

Condition-dependent sex was tested in the white clover, Trifolium repens [36]. Indeed, herbivory was found to induce higher investment in sexual reproduction in sensitive plants, but not in resistant ones, showing that condition-dependent sex in this system was induced by the individual condition, and not only by an external cue.

(b). Eukaryote unicellular organisms

It has been suggested that facultative sex is very common in unicellular organisms [2]. In Saccharomyces cerevisiae, initiation of meiosis only occurs when cells are starving for both carbon and nitrogen [37]. A stress signal is also required for sexual differentiation in Schizosaccharomyces pombe [38], and oxidative stress has been shown to increase the percentage of meiotic spores by 4- to 18-fold [39]. Likewise, Aspergillus nidulans fungi produce more of their spores sexually in environments where they are less fit, although asexual spores are more dispersive and equally resistant [40]. The pathogenic fungus Candida albicans does not appear to reproduce sexually, but its parasexual cycle—involving tetraploidy, aneuploidy and genetic variation—has been suggested to be promoted by stress [41,42].

(c). Bacteria: condition-dependent horizontal gene transfer

Although bacteria do not go through meiosis, they do exchange genetic information via horizontal gene transfer or HGT [43], through different mechanisms: transformation, the incorporation of foreign DNA into the genome; conjugation, the horizontal transfer of plasmids; transduction, the transfer of genes carried by infecting phages; and integrons, which facilitate the exchange of gene-cassettes in bacterial populations [44].

Empirical evidence suggests that natural competence for transformation is upregulated by multiple stressors (reviewed in [45]), including DNA damage ([46], but see also [47]) and starvation [48,49]. However, it has also been suggested that stressed microbes take up DNA for reasons other than the generation of genetic variation, such as nutrient consumption and DNA repair [43]. The different explanations are not mutually exclusive: for example, bacteria can benefit from increased transformation under starvation due to both nutrient uptake and genetic variation. Interestingly, the stress of anti-bacterial drugs has also been demonstrated to induce HGT: several antibiotics induce transformation in Streptococcus pneumoniae [50]; ciprofloxacin (but not 10 other drugs) induces homologous recombination in Escherichia coli [51]; and β-lactams have been shown to induce transduction of virulence factors in Staphylococcus aureus [52,53].

4. The effects of condition-dependent sex on adaptation and diversity

When present, condition-dependent sex can have beneficial implications on variation and fitness at the level of the entire population, potentially affecting its long-term survival. Evolutionary models show that condition-dependent sex (and in bacteria, condition-dependent HGT) reduces the time for the fixation of a beneficial mutation when the cost of sex is considerable [13]. This is because under condition-dependent sex, maladapted individuals pay most of the cost of sex, which increases the efficiency of natural selection. By contrast, under uniform sex both adapted and maladapted individuals equally pay the cost of sex. Altogether, we would expect populations performing condition-dependent sex to be more adaptable to new environmental conditions.

Pathogens present interesting adaptation scenarios. From the host perspective, condition is affected by pathogen load, and ‘condition-dependent’ can become ‘infection-dependent’ when pathogen pressure is significant. According to the Red Queen hypothesis [54,55], coevolution of hosts and pathogens produces oscillations in the frequencies of different genotypes and can favour the evolution of sex. In such cases, theoretical models suggest that infection-dependent sex is even more successful than infection-independent sex [17].

From the pathogen perspective, drug stress can greatly affect condition. Epidemiological models suggest that the effect of condition-dependent HGT on the emergence of multiple drug resistance in the clinic must be taken into account when designing treatment policies [56,57]. Similarly, drug-induced superinfection in HIV—which leads to mixing of virion genes and can be considered a form of viral sex—promotes the evolution of drug resistance [58] and facilitates adaption on rugged fitness landscapes [59], where recombination has also been shown to accelerate adaptation [60]. By contrast, sex induced by environmental stress, which is synchronized across the population, can lead to a positive correlation between condition and sexual reproduction, and decrease the rate of adaptation on rugged landscapes [61].

Another relevant case is adaptation to climate change, such as global warming. Species employing condition-dependent sex might be able to adapt better in geographical areas undergoing significant environmental change: if individuals that are well adapted to the new conditions reproduce sexually less often than maladapted individuals, than alleles providing an advantage in the new conditions could spread more rapidly in the population. On the other hand, the cost of sex can also increase with stress. In plants, for example, flowers are particularly sensitive to extreme temperatures [62]. Thus, we could predict that species employing condition-dependent sex would become more common in areas undergoing rapid environmental change, such as desert-edge ecosystems (but see the next two sections for other considerations).

Condition-dependent sex has also been shown to result in increased mean fitness at equilibrium, in comparison with uniform sexual or asexual reproduction [9]. Similarly, computer simulations demonstrate that condition-dependent transformation increases the population mean fitness in asexual unicellular populations [63]. This suggests that condition-dependent sex will also decrease the chance that a new beneficial mutation would appear in a poor genetic background (as those are less common in populations with higher mean fitness) and go to extinction through background selection. These results suggest that species employing condition-dependent sex might have a long-term advantage over species employing other strategies, when competing over the same ecological niche. Note that we do not expect mean fitness advantages to be a major selection force acting on an allele for condition-dependent sex in the short term. Rather, ‘selfish’ alleles for an abandon-ship mechanism, favoured by individual-level selection, might have beneficial long-term side effects for the population as a whole.

5. Why is condition-dependent sex not more common?

The results above highlight a difficult question: if condition-dependent sex is beneficial in the short term and carries an advantage in the long term, why is it not more common in nature? Why, for example, do all mammals and most birds reproduce only through sexual reproduction?

One possibility is that condition-dependent sex is more common than we think, but detecting this plasticity is difficult. Many organisms that were considered strictly asexual were recently discovered to be exchanging DNA, most notably the bdelloid rotifers (the ancient asexual scandal [64]). After many years of intensive research, recent genomic tools allowed the identification of massive genetic exchange [65] through atypical meiosis [66] and/or horizontal gene transfer [67]. Thus, bdelloid rotifers are in a sense facultative sexuals. Moreover, bdelloid rotifer species from desiccating habitats experience HGT more often [68]. Similar results were obtained in the opposite direction too, with the identification of facultative parthenogenesis in various vertebrates in the wild [6,69]. With time and technology, additional asexual and obligate species might prove to be facultative sexuals, and future research might reveal how common condition dependence is among them.

But are there conditions where condition-dependent sex is not expected to evolve (see table 1 for summary)? One important factor is the nature of the poor condition: certain stressful conditions might be associated with increased costs of sex, making sex less advantageous for the stressed individuals. For example, shade stress might be correlated with low pollinator density, and therefore might be a poor cue for switching to sexual reproduction in plants (increased investment in dispersal might be more helpful); similarly, the cost of finding a mate could increase under low population density [20]. When an external stressor affects the condition of the entire population (e.g. temperature or drought, proximity to the boundary of the species' range), it might result in both low population density and poor individual condition. Switching to sexual reproduction precisely when the condition is bad—and the density low—might be detrimental, and reproducing asexually, while ‘waiting out’ for better conditions could be a favourable strategy (see also [70]).

Another critical factor is sexual selection, which produces a positive correlation between the condition of an individual and its mating success [71]. Sexual selection makes sexual reproduction more advantageous specifically for individuals in good condition and can lead to obligatory sex [72,73]. A model considering both environmental changes and sexual selection can further extend the parameter range allowing the evolution of obligate sex [72,73]. When poor condition is induced by pathogens, sexual selection also applies: sexual selection can increase the mating success of hosts that are less infected [74], due to preference for either resistance genes or pathogen avoidance [75]. That form of sexual selection would again make sexual reproduction more beneficial specifically for individuals in good condition, and potentially select for obligate sex. By contrast, sexually transmitted pathogens could have the opposite effect: attractive males would suffer from more pathogens [25], possibly leading females in good condition to prefer asexual reproduction.

Finally, the advantage of sex usually increases with the rate of mutation [76] and with the rate of environmental changes [77], two factors that increase the mismatch between the genotype and the environment. When these rates are too high, most individuals will not be in a really good condition. Under such conditions, obligate sex (or mostly obligate sex) can evolve, in particular, in combination with sexual selection (figure 3).

Figure 3.

Figure 3.

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Hypothetical stages in the evolution of sex. Under this hypothesis, asexual populations evolve condition-dependent sex due to second-order selection (solid arrow) because the modifier allele becomes associated with fitter genotypes (the abandon-ship principle). This stage is expected to occur under a very wide parameter range. At the next stage (dashed arrow), condition-dependent sexual populations might evolve obligate sex due to one or more of the following mechanisms: sexual selection, which benefits fitter genotypes when reproducing sexually; and high-mutation rates or frequent environmental changes, both making ‘good’ genotypes (in a given environment) less common.

6. Generalization: condition-dependent variation

As we have seen, condition-dependent sex is common over a wide range of organisms. However, not all organisms show that association. Species that do not exhibit condition-dependent sex can still benefit from other mechanisms of condition-dependent genetic variation, such as recombination.

There is considerable evidence for condition-dependent recombination: in somatic cells of tobacco plants, several stressors increased the homologous recombination rate [78]; similarly, pathogen stress can stimulate somatic recombination in Arabidopsis [79]. In flies, a negative relationship between fitness and recombination rate was observed for heat and pathogen stress, but not for mating or cold stress [80–82], and deleterious mutations have been shown to alter the recombination rate, but not in a consistent way [83].

Theoretical models show that fitness-associated recombination can evolve in haploids [11,84] but less easily in diploids [12], and that an allele that increases recombination rates in maladapted individuals can evolve through the abandon-ship principle, without repairing DNA or increasing fitness [10,11], similarly to condition-dependent sex [9]. Additionally, in fluctuating environments, an environmentally dependent recombination rate is likely to evolve due to its effect on population mean fitness [85,86]. It has also been demonstrated that if fitter individuals have less recombination, then complex traits evolve faster and the population mean fitness is higher, compared with uniform-rate recombination [87].

Other mechanisms that can also increase genetic variation when condition is poor or during stress include mutagenesis [15,88], loss of heterozygosity [89], genomic rearrangements [90], aneuploidy [91,92], dispersal [14,16], mate choice [93] and even death—resulting in the replacement of an aging individual by a young one, generated through sex and mutation [94].

We suggest that in different species, individuals in poor condition would act to increase genetic variation by some of the above-mentioned mechanisms, according to the costs and benefits of the different mechanisms. For example, we can expect facultative sexuals to switch to sexual reproduction under unfavourable conditions, while organisms reproducing only through sexual reproduction might increase genetic variation in other ways: mutating, dispersing, outcrossing or dying. According to this view, condition-dependent sex is a central mechanism for the generation of genetic variation, but not the only one, and different mechanisms can be favoured by natural selection under different circumstances.

7. Open questions for future research

Two directions that arise from the current review seem particularly interesting to us. First, the actual prevalence of condition-dependent sex in nature is not clear. This calls for testing condition-dependent sex versus environment-dependent sex in different species and for investigating recently discovered facultative sexuals: do they employ condition-dependent sex? Second, the transition from condition-dependent sex to obligate sex is still a puzzle. One approach could be constructing pluralistic models that take into account the abandon-ship principle together with other major factors, such as sexual selection, differential cost of sex and parasites. Finally, different condition-dependent mechanisms might be competing: if an organism is capable of plasticity in the rate of sex, recombination, mutation or dispersal under stress, when would we expect sex to be condition-dependent?

Acknowledgements

We thank Tuvik Beker for comments on the manuscript.

Authors' contributions

Y.R. and L.H. drafted the manuscript and gave final approval for publication.

Competing interests

We have no competing interests.

Funding

The research has been supported by ISF 1568/13 and by The Minerva Center for Lab Evolution.

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