Fitness of alternative modes of reproduction: developmental constraints and the evolutionary maintenance of sex

Parthenogenesis, including facultative parthenogenesis, is common among orthopteroid insects. We investigated the fitness associated with sexual and asexual reproduction within a population of the facultatively parthenogenetic cockroach Nauphoeta cinerea. There is significantly reduced fitness for females reproducing parthenogenetically compared to sexually. Fewer than half of all females can reproduce parthenogenetically. In addition, tenfold fewer offspring are produced by parthenogenesis due to reductions in both the number of offspring produced per clutch and the number of clutches produced. Development and brooding of sexually or parthenogenetically produced first instar nymphs does not differ, although the production of the first parthenogenetic clutch is delayed relative to the first sexually produced clutch. The fitness of parthenogens is also lower than the fitness of sexually produced offspring. Parthenogens are less viable than sexually produced offspring even in the benign conditions of the laboratory. Development to adulthood of parthenogens is slower. Fewer parthenogens survive to adulthood and the adult life span of parthenogens is reduced. Individuals produced by parthenogenetic reproduction are unlikely to reproduce parthenogenetically themselves. Finally, parthenogenetically produced females produce fewer offspring by sexual reproduction than do sexually produced females. Since parthenogenetic reproduction is apomictic in N. cinerea and parthenogens are diploid, we suggest that asexual reproduction is developmentally constrained. Once meiosis has evolved, returning to a mitotic mode of reproduction may be difficult. Nauphoeta cinerea offers a system for testing how asexuality is constrained as modes of reproduction can be compared within a facultative parthenogen.     

Genetic variation and asexual reproduction in the facultatively parthenogenetic cockroach Nauphoeta cinerea: implications for the evolution of sex

Asexual reproduction could offer up to a two‐fold fitness advantage over sexual reproduction, yet higher organisms usually reproduce sexually. Even in facultatively parthenogenetic species, where both sexual and asexual reproduction is sometimes possible, asexual reproduction is rare. Thus, the debate over the evolution of sex has focused on ecological and mutation‐elimination advantages of sex. An alternative explanation for the predominance of sex is that it is difficult for an organism to accomplish asexual reproduction once sexual reproduction has evolved. Difficulty in returning to asexuality could reflect developmental or genetic constraints. Here, we investigate the role of genetic factors in limiting asexual reproduction in Nauphoeta cinerea, an African cockroach with facultative parthenogenesis that nearly always reproduces sexually. We show that when N. cinerea females do reproduce asexually, offspring are genetically identical to their mothers. However, asexual reproduction is limited to a nonrandom subset of the genotypes in the population. Only females that have a high level of heterozygosity are capable of parthenogenetic reproduction and there is a strong familial influence on the ability to reproduce parthenogenetically. Although the mechanism by which genetic variation facilitates asexual reproduction is unknown, we suggest that heterosis may facilitate the switch from producing haploid meiotic eggs to diploid, essentially mitotic, eggs.     

From asexual to eusocial reproduction by multilevel selection by density-dependent competitive interactions

A game theoretical model is developed to illustrate that multilevel selection by density-dependent competitive interactions in mobile organisms might have played a major role in the evolutionary transitions from asexual over sexual to eusocial reproduction. The model has four equilibria with selection occurring among interacting units of respectively one, two, three, and up to infinitely many individuals. The different equilibria are characterised by different levels of competitive interactions among interacting units, and these levels select for different levels of sexual and co-operative reproduction among the individuals of the units. The model predicts: (i) that low-energy organisms with negligible body masses have asexual reproduction; (ii) that high-energy organisms with non-negligible body masses in evolutionary equilibria have sexual reproduction between a female and a male; (iii) that high-energy organisms with non-negligible body masses that increase exponentially at an evolutionary steady state have co-operative reproduction between a sexual pair and a single sexually produced offspring; and (iv) that high-energy organisms with upward constrained body masses have eusocial reproduction between a sexual pair and up to an infinite number of sexually produced offspring workers.     

Genetic variation, disequilibrium and natural selection on reproductive traits in Allium vineale

Bulbils and seeds collected from Allium vineale plants from natural populations were grown under uniform conditions. The bulbil-derived offspring represented the parental generation, whereas the seed-derived offspring represented the sexually produced offspring generation. Molecular markers were used to identify maternal genets. Variation in traits determining the allocation to sexual and asexual reproduction was partitioned among genets and ramet families in the parental and offspring generations. From observations of a release of genetic variation and slippage in the mean phenotype in the offspring generation, we inferred that there exists extensive genetic disequilibrium for reproductive traits in A. vineale populations, that most of the genetic variance is because of dominance effects, and that natural selection favours a reduced allocation to sexual reproduction. No genetic correlation between sexual and asexual allocation traits was found. We discuss the implications of these results with respect to the evolution of a mixed reproductive system in A. vineale.     

LARGE POPULATION SIZE PREDICTS THE DISTRIBUTION OF ASEXUALITY IN SCALE INSECTS

Understanding why some organisms reproduce by sexual reproduction while others can reproduce asexually remains an important unsolved problem in evolutionary biology. Simple demography suggests that asexuals should outcompete sexually reproducing organisms, because of their higher intrinsic rate of increase. However, the majority of multicellular organisms have sexual reproduction. The widely accepted explanation for this apparent contradiction is that asexual lineages have a higher extinction rate. A number of models have indicated that population size might play a crucial role in the evolution of asexuality. The strength of processes that lead to extinction of asexual species is reduced when population sizes get very large, so that the long‐term advantage of sexual over asexual reproduction may become negligible. Here, we use a comparative approach using scale insects (Coccoidea, Hemiptera) to show that asexuality is indeed more common in species with larger population density and geographic distribution and we also show that asexual species tend to be more polyphagous. We discuss the implication of our findings for previously observed patterns of asexuality in agricultural pests.     

Imitating the cost of males: A hypothesis for coexistence of all‐female sperm‐dependent species and their sexual host

All‐female sperm‐dependent species are particular asexual organisms that must coexist with a closely related sexual host for reproduction. However, demographic advantages of asexual over sexual species that have to produce male individuals could lead both to extinction. The unresolved question of their coexistence still challenges and fascinates evolutionary biologists. As an alternative hypothesis, we propose those asexual organisms are afflicted by a demographic cost analogous to the production of males to prevent exclusion of the host. Previously proposed hypotheses stated that asexual individuals relied on a lower fecundity than sexual females to cope with demographic advantage. In contrast, we propose that both sexual and asexual species display the same number of offspring, but half of asexual individuals imitate the cost of sex by occupying ecological niches but producing no offspring. Simulations of population growth in closed systems under different demographic scenarios revealed that only the presence of nonreproductive individuals in asexual females can result in long‐term coexistence. This hypothesis is supported by the fact that half of the females in some sperm‐dependent organisms did not reproduce clonally.     

Asexually produced Cape honeybee queens (Apis mellifera capensis) reproduce sexually

Unmated workers of the Cape honeybee Apis mellifera capensis can produce female offspring including daughter queens. As worker-laid queens are produced asexually, we wondered whether these asexually produced individuals reproduce asexually or sexually. We sampled 11 colonies headed by queens known to be the clonal offspring of workers and genotyped 23 worker offspring from each queen at 5 microsatellite loci. Without exception, asexually produced queens produced female worker offspring sexually. In addition, we report the replacement of a queen by her asexually produced granddaughter, with this asexually produced queen also producing offspring sexually. Hence, once a female larva is raised as a queen, mating and sexual reproduction appears to be obligatory in this subspecies, despite the fact that worker-laid queens are derived from asexual lineages.     

Eco‐evolutionary feedback promotes Red Queen dynamics and selects for sex in predator populations

Although numerous hypotheses exist to explain the overwhelming presence of sexual reproduction across the tree of life, we still cannot explain its prevalence when considering all inherent costs involved. The Red Queen hypothesis states that sex is maintained because it can create novel genotypes with a selective advantage. This occurs when the interactions between species induce frequent environmental change. Here, we investigate whether coevolution and eco‐evolutionary feedback dynamics in a predator‐prey system allows for indirect selection and maintenance of sexual reproduction in the predator. Combining models and chemostat experiments of a rotifer‐algae system we show a continuous feedback between population and trait change along with recurrent shifts from selection by predation and competition for a limited resource. We found that a high propensity for sex was indirectly selected and was maintained in rotifer populations within environments containing these eco‐evolutionary dynamics; whereas within environments under constant conditions, predators evolved rapidly to lower levels of sex. Thus, our results indicate that the influence of eco‐evolutionary feedback dynamics on the overall evolutionary change has been underestimated.     

On the moulding of senescence by natural selection in sexual and partly sexual populations

Under a wide variety of dynamic environmental conditions, natural selection appears to favor reproductive investment in a sexually produced offspring, carrying only half of the mother’s genes, over the investment in an asexually produced offspring, genetically identical to her. It is maintained that the same environmental conditions must affect the evolutionary cost and benefit of an investment in the prolongation of one’s own life versus an investment in sexual reproduction, in favor of the latter. The effects of different environmental conditions on the division of resources among sexual reproduction, asexual reproduction and prolongation of life are studied.     

The consequences of facultative sex in a prey adapting to predation

A species reproductive mode, along with its associated costs and benefits, can play a significant role in its evolution and survival. Facultative sexuality, being able to reproduce both sexually and asexually, has been deemed evolutionary favourable as the benefits of either mode may be fully realized. In fact, many studies have focused on identifying the benefits of sex and/or the forces selecting for increased rates of sex using facultative sexual species. The costs of either mode, however, can also have a profound impact on a population's evolutionary trajectory. Here, we used experimental evolution and fitness assays to investigate the consequences of facultative sexuality in prey adapting to predation. Specifically, we compared the adaptive response of algal prey populations exposed to constant rotifer predation and which had alternating cycles of asexual and sexual reproduction where sexual episodes were either facultative (sexual and asexual progeny simultaneously propagated) or obligate (only sexual progeny propagated). We found that prey populations with facultative sexual episodes reached a lower final relative fitness and suffered a greater trade‐off in traits under selection, that is defence and competitive ability, as compared to prey populations with obligate sexual episodes. Our results suggest that costs associated with sexual reproduction (germination time) and asexual reproduction (selection interference) were amplified in the facultative sexual prey populations, leading to a reduction in the net advantage of sexuality. Additionally, we found evidence that the cost of sex was reduced in the obligate sexual prey populations because increased selection for sex was observed via the spontaneous production of sexual cells. These results show that certain costs associated with facultative sexuality can affect an organism's evolutionary trajectory.     

The genetics and evolution of obligate reproductive parasitism in Trichogramma pretiosum infected with parthenogenesis-inducing Wolbachia

Parthenogenesis-inducing (PI) Wolbachia belong to a class of intracellular symbionts that distort the offspring sex ratio of their hosts toward a female bias. In many PI Wolbachia-infected species sex ratio distortion has reached its ultimate expression-fixation of infection and all-female populations. This is only possible with thelytokous PI symbionts as they provide an alternative form of reproduction and remove the requirement for males and sexual reproduction. Many populations fixed for PI Wolbachia infection have lost the ability to reproduce sexually, even when cured of the infection. We examine one such population in the species Trichogramma pretiosum. Through a series of backcrossing experiments with an uninfected Trichogramma pretiosum population we were able to show that the genetic basis for the loss of female sexual function could be explained by a dominant nuclear effect. Male sexual function had not been completely lost, though some deterioration of male sexual function was also evident when males from the infected population (created through antibiotic curing of infected females) were mated to uninfected females. We discuss the dynamics of sex ratio selection in PI Wolbachia-infected populations and the evolution of non-fertilizing mutations.     

Maintenance of sexually dimorphic preadult traits in Marchantia inflexa (Marchantiacae)

Marchantia inflexa, a dioecious thallose liverwort, is sexually dimorphic in clonal expansion traits. We used selection analyses to measure the magnitude and direction of selection on clonal fitness to uncover possible mechanisms for the maintenance of preadult sexually dimorphic characters. We planted replicates of genotypes of female and male M. inflexa in two light environments in a greenhouse and measured morphological and phenological characters associated with growth and asexual reproduction. Timing to onset of asexual reproduction and plant size early in development were under sex-specific selection in a low light environment. Additionally, females exhibited a sex-specific cost of plasticity in the timing of their onset of asexual reproduction in high light. Selection on asexual fitness tended to shift traits toward monomorphism rather than sexual dimorphism, whereas the expressed phenotype of females was congruent with patterns of selection acting on sexual fitness. We detected negative trade-offs between asexual and sexual fitness components in females in one light environment. Opposing selective forces acting on asexual and sexual fitness components may explain how sexual dimorphisms persist in the face of selection for monomorphism in the preadult phase.     

Maturation costs affect maturation timing: sexual reproduction in a heterogonic hydra

If maturation is more costly for females, they may need more distinct environmental cues to induce sexual reproduction than males. We verified this hypothesis by comparing the indirect costs of maturation to males and females of the heterogonic Hydra oligactis, reproducing both asexually and sexually. The laboratory experiments revealed that males mature 2 weeks earlier than the first females at falling temperatures simulating the natural conditions that precede sexual reproduction. The difference between the energy costs of maturation for males versus females has been considered a likely factor responsible for the observed difference in maturation time. Available food supply positively affected the percentage of sexually mature females, indicating that females are more sensitive to food limitation than males. The number of gonads was correlated positively with the size of mature hydra for both males and females. However, males produced twice as many testes as ovaries produced by females. We postulate that females are induced later than males in order to prevent gonadal development after an unseasonable drop in temperature. As sexual reproduction in H. oligactis interferes with asexual budding, under favorable conditions for asexual proliferation unnecessary gonadal development decreases an individual’s fitness through reduction of the number of produced offspring.     

The sexual selection paradigm: have we overlooked other mechanisms in the evolution of male ornaments?

Extravagant male ornaments expressed during reproduction are almost invariably assumed to be sexually selected and evolve through competition for mating opportunities. Yet in species where male reproductive success depends on the defence of offspring, male ornaments could also evolve through social competition for offspring survival. However, in contrast to female ornaments, this possibility has received little attention in males. We show that a male ornament that is traditionally assumed to be sexually selected—the red nuptial coloration of the three-spined stickleback—is under stronger selection for offspring survival than for mating success. Males express most coloration during parenting, when they no longer attract females, and the colour correlates with nest retention and hatching success but not with attractiveness to females. This contradicts earlier assumptions and suggests that social selection for offspring survival rather than for sexual selection for mating success is the main mechanism maintaining the ornament in the population. These results suggest that we should consider other forms of social selection beyond sexual selection when seeking to explain the function and evolution of male ornaments. An incorrect assignment of selection pressures could hamper our understanding of evolution.     

Sexual reproduction and diversity: Connection between sexual selection and biological communities via population dynamics

Sexual reproduction is a mysterious phenomenon. Most animals and plants invest in sexual reproduction, even though it is more costly than asexual reproduction. Theoretical studies suggest that occasional or conditional use of sexual reproduction, involving facultative switching between sexual and asexual reproduction, is the optimal reproductive strategy. However, obligate sexual reproduction is common in nature. Recent studies suggest that the evolution of facultative sexual reproduction is prevented by males that coerce females into sexual fertilization; thus, sexual reproduction has the potential to enforce costs on a given species. Here, the effect of sex on biodiversity is explored by evaluating the reproductive costs arising from sex. Sex provides atypical selection pressure that favors traits that increase fertilization success, even at the expense of population growth rates, that is, sexual selection. The strength of sexual selection depends on the density of a given species. Sexual selection often causes strong negative effects on the population growth rates of species that occur at high density. Conversely, a species that reduces its density is released from this negative effect, and so increases its growth rate. Thus, this negative density-dependent effect on population growth that arises from sexual selection could be used to rescue endangered species from extinction, prevent the overgrowth of common species and promote the coexistence of competitive species. Recent publications on sexual reproduction provide several predictions related to the evolution of reproductive strategies, which is an important step toward integrating evolutionary dynamics, demographic dynamics and community dynamics.     

Developmental constraints on the mode of reproduction in the facultatively parthenogenetic cockroach Nauphoeta cinerea

Considerable work in evolutionary biology has focused on the question of why sex persists. Both advantages to sex and constraints limiting a return to asexual reproduction are hypothesized to maintain sex once it evolves. Developmental constraints would limit asexual reproduction from a sexual species if it were difficult for females to switch from making eggs that do not develop without fertilization to making zygotes that are capable of developing in the absence of fertilization. Nauphoeta cinerea is an ovoviviparous cockroach in which some females are capable of switching from a sexual mode of reproduction to an asexual mode when isolated from males. Yet, while facultative parthenogenesis can occur in individuals, few females make the switch. Thus, this cockroach provides an ideal system for examining the potential role of developmental constraints in maintaining sex. Here we compare the cytogenetics and embryonic development of sexual and parthenogenetic offspring in N. cinerea. We find that deviations from normal ploidy levels are associated with abnormal development. All viable N. cinerea embryos exhibit typically hemimetabolous insect embryogenesis. Although there is no variation among embryos in development within a sexually produced clutch, we see extreme variation in asexually derived clutches. These results suggest that developmental constraints limit the success of asexual reproduction in this facultatively parthenogenetic cockroach. Our data further suggest that the specific constraint occurs in the switch from a meiotic mode of reproduction requiring fertilization to diploid zygotes that develop in the absence of fertilization.     

Soft selection reduces loss of heterozygosity in asexual reproduction

The adaptive value of sexual reproduction is still debated in evolutionary theory. It has been proposed that the advantage of sexual reproduction over asexual reproduction is to promote genetic diversity, to prevent the accumulation of harmful mutations or to preserve heterozygosity. Since these hypothetical advantages depend on the type of asexual reproduction, understanding how selection affects the taxonomic distribution of each type could help us discriminate between existing hypotheses. Here, I argue that soft selection, competition among embryos or offspring in selection arenas prior to the hard selection of the adult phase, reduces loss of heterozygosity in certain types of asexual reproduction. Since loss of heterozygosity leads to the unmasking of recessive deleterious mutations in the progeny of asexual individuals, soft selection facilitates the evolution of these types of asexual reproduction. Using a population genetics model, I calculate how loss of heterozygosity affects fitness for different types of apomixis and automixis, and I show that soft selection significantly reduces loss of heterozygosity, hence increases fitness, in apomixis with suppression of the first meiotic division and in automixis with central fusion, the most common types of asexual reproduction. Therefore, if sexual reproduction evolved to preserve heterozygosity, soft selection should be associated with these types of asexual reproduction. I discuss the evidence for this prediction and how this and other observations on the distribution of different types of asexual reproduction in nature is consistent with the heterozygosity hypothesis.     

Cytonuclear evidence for hybridogenetic reproduction in natural populations of the Australian carp gudgeon (Hypseleotris: Eleotridae)

Although most vertebrates reproduce sexually, a small number of fishes, amphibians and reptiles are known in which reproduction is asexual, i.e. without meiotic recombination. In fishes, these so-called unisexual lineages usually comprise only females and utilize co-occurring males of a related sexual species to reproduce via gynogenesis or hybridogenesis. Here, we examine patterns of microsatellite and mitochondrial DNA (mtDNA) variation in a widespread group of freshwater fishes (carp gudgeons; Hypseleotris spp.) to investigate a long-standing proposal that this group includes unisexual forms. We show that the mtDNA genome of most carp gudgeons in tributaries of the Goulburn River belongs to one of two deeply divided clades (～10% cyt b divergence) and that nuclear variation divides the same individuals into four distinct groups. Group 1 exhibits the genotypic proportions of a random mating population and has a 1:1 sex ratio. Two other groups are extremely sex-biased (98% male, 96% female), exhibit excess heterozygosity at most loci and share at least one allele per locus with group 1. We propose that these two groups represent 'unisexual' hybridogenetic lineages and that both utilize co-occurring group 1 as sexual host. Interestingly, the fourth distinct group appears to represent hybrid offspring of the two putative hybridogenetic lineages. The propagation of clonal haploid genomes by both males and females and the ability of these clones to unite and form sexually mature diploid hybrid offspring may represent a novel mechanism that contributes to the dynamics of coexistence between hybridogenetic lineages and their sexual hosts.     

The paradox of obligate sex: The roles of sexual conflict and mate scarcity in transitions to facultative and obligate asexuality

The maintenance of obligate sex in animals is a long‐standing evolutionary paradox. To solve this puzzle, evolutionary models need to explain why obligately sexual populations consistently resist invasion by facultative strategies that combine the benefits of both sexual and asexual reproduction. Sexual antagonism and mate availability are thought to shape the occurrence of reproductive modes in facultative systems. But it is unclear how such factors interact with each other to influence facultative invasions and transitions to obligate asexuality. Using individual‐based models, we clarify how sexually antagonistic coevolution and mate availability affect the likelihood that a mutant allele that gives virgin females the ability to reproduce parthenogenetically will invade an obligately sexual population. We show that male coercion cannot stop the allele from spreading because mutants generally benefit by producing at least some offspring asexually prior to encountering males. We find that effects of sexual conflict can lead to positive frequency‐dependent dynamics, where the spread of the allele is promoted by effective (no‐cost) resistance when males are common, and by mate limitation when sex ratios are female‐biased. However, once the mutant allele fixes, effective coercion prevents the complete loss of sex unless linkage disequilibrium can build up between the allele and alleles for effective resistance. Our findings clarify how limitations of female resistance imposed by the genetic architecture of sexual antagonism can promote the maintenance of sexual reproduction. At the same time, our finding of widespread obligate sex when costs of parthenogenesis are high suggests that developmental constraints could contribute to the rarity of facultative reproductive strategies in nature.     

Do males pay for sex? Sex‐specific selection coefficients suggest not

Selection acting on males can reduce mutation load of sexual relative to asexual populations, thus mitigating the twofold cost of sex, provided that it seeks and destroys the same mutations as selection acting on females, but with higher efficiency. This could happen due to sexual selection—a potent evolutionary force that in most systems predominantly affects males. We used replicate populations of red flour beetles (Tribolium castaneum) to study sex‐specific selection against deleterious mutations introduced with ionizing radiation. We found no evidence for selection being stronger in males than in females; in fact, we observed a nonsignificant trend in the opposite direction. This suggests that selection on males does not reduce mutation load below the level expected under the (hypothetical) scenario of asexual reproduction. Additionally, we employed a novel approach, based on a simple model, to quantify the relative contributions of sexual and offspring viability selection to the overall selection observed in males. We found them to be similar in magnitude; however, only the offspring viability component was statistically significant. In summary, we found no support for the hypothesis that selection on males in general, and sexual selection in particular, contributes to the evolutionary maintenance of sex.