X-linked meiotic drive can boost population size and persistence

X-linked meiotic drivers cause X-bearing sperm to be produced in excess by male carriers, leading to female-biased sex ratios. Here, we find general conditions for the spread and fixation of X-linked alleles. Our conditions show that the spread of X-linked alleles depends on sex-specific selection and transmission rather than the time spent in each sex. Applying this logic to meiotic drive, we show that polymorphism is heavily dependent on sperm competition induced both by female and male mating behavior and the degree of compensation to gamete loss in the ejaculate size of drive males. We extend these evolutionary models to investigate the demographic consequences of biased sex ratios. Our results suggest driving X-alleles that invade and reach polymorphism (or fix and do not bias segregation excessively) will boost population size and persistence time by increasing population productivity, demonstrating the potential for selfish genetic elements to move sex ratios closer to the population-level optimum. However, when the spread of drive causes strong sex-ratio bias, it can lead to populations with so few males that females remain unmated, cannot produce offspring, and go extinct. This outcome is exacerbated when the male mating rate is low. We suggest that researchers should consider the potential for ecologically beneficial side effects of selfish genetic elements, especially in light of proposals to use meiotic drive for biological control.     

POLLEN PERFORMANCE AND SEX-RATIO EVOLUTION IN A DIOECIOUS PLANT

There has been a proliferation of studies, in a variety of taxa, that have detected sex-linked or cytoplasmic genes that enhance their own transmission via sex-ratio distortion. One of the most important parameters influencing the dynamics of these elements is the magnitude of their transmission advantage. In many systems, the mechanism of sex-ratio distortion is to abort X- or Y-bearing gametes. With this mechanism, the transmission advantage associated with sex-ratio distortion is diminished when the production of male gametes limits offspring production or when competition among the gametes of different males is intense. In this study, we analyzed the outcome of pollen competition between males that produced different sex ratios in the dioecious plant, Silene alba, and estimated how the sex-ratio bias influenced the transmission properties of the sex chromosomes. We varied the intensity of pollen competition by controlling the quantity of pollen used in crosses and used a combination of single-male pollinations and pollen mixtures to evaluate the effects of multiple paternity. Paternity in pollen mixtures was estimated using allozymes. Sex-ratio bias was directly influenced by the quantity of pollen, but the magnitude of this effect was small. The relative performance of pollen from different males varied substantially, especially when there was multiple paternity. Specifically, males with biased sex ratios sired far fewer offspring of either sex in pollen mixtures. In crosses involving single males, however, these “sex-ratio” males produced the same number of offspring as other males, so the female bias caused a significant transmission advantage for X-linked genes. X-linked genes could enhance their transmission via sex-ratio distortion in Silene populations, but the magnitude of this transmission advantage will depend on the ecological circumstances that influence the opportunity for multiple paternity.     

JIL-1 kinase, a member of the male-specific lethal (MSL) complex, is necessary for proper dosage compensation of eye pigmentation in Drosophila

The upregulation of the JIL-1 kinase on the male X chromosome and its association with the male-specific lethal (MSL) complex suggest that JIL-1 may play a role in regulating dosage compensation. To directly test this hypothesis we measured eye pigment levels of mutants in the X-linked white gene in an allelic series of JIL-1 hypomorphic mutants. We show that dosage compensation of w(a) alleles that normally do exhibit dosage compensation was severely impaired in the JIL-1 mutant backgrounds. As a control we also examined a hypomorphic white allele w(e) that fails to dosage compensate in males due to a pogo element insertion. In this case the relative pigment level measured in males as compared to females remained approximately the same even in the most severe JIL-1 hypomorphic background. These results indicate that proper dosage compensation of eye pigment levels in males controlled by X-linked white alleles requires normal JIL-1 function.     

A mutation in the rett syndrome gene, MECP2, causes X-linked mental retardation and progressive spasticity in males

Heterozygous mutations in the X-linked MECP2 gene cause Rett syndrome, a severe neurodevelopmental disorder of young females. Only one male presenting an MECP2 mutation has been reported; he survived only to age 1 year, suggesting that mutations in MECP2 are male lethal. Here we report a three-generation family in which two affected males showed severe mental retardation and progressive spasticity, previously mapped in Xq27.2-qter. Two obligate carrier females showed either normal or borderline intelligence, simulating an X-linked recessive trait. The two males and the two obligate carrier females presented a mutation in the MECP2 gene, demonstrating that, in males, MECP2 can be responsible for severe mental retardation associated with neurological disorders.     

Lethal combat and sex ratio evolution in a parasitoid wasp

Sex allocation theory provides excellent opportunities for testinghow behavior and life histories are adjusted in response toenvironmental variation. One of the most successful areas fromthis respect is Hamilton's local mate competition theory. Aspredicted by theory, a large number of animal species have beenshown to adjust their offspring sex ratios (proportion male)conditionally, laying less female-biased sex ratios as the numberof females that lay eggs on a patch increases. However, recentstudies have shown that this predicted pattern is not followedby 2 parasitoid species in the genus Melittobia, which alwaysproduce extremely female-biased sex ratios. A possible explanationfor this is that males fight fatally and that males producedby the first female to lay eggs on a patch have a competitiveadvantage over later emerging males. This scenario would negatethe advantage of later females producing a less female-biasedsex ratio. Here we examine fatal fighting and sex ratio evolutionin another species, Melittobia acasta. We show that femalesof this species also fail to adjust their offspring sex ratioin response to the number of females laying eggs on a patch.We then show that although earlier emerging males do have anadvantage in winning fights, this advantage 1) can be reducedby an interaction with body size, with larger males more likelyto win fights and 2) only holds for a brief period around thetime at which the younger males emerge from their pupae. Thissuggests that lethal male combat cannot fully explain the lackof sex ratio shift observed in Melittobia species. We discussalternative explanations.     

Reproductive compensation and human genetic disease

The effects of reproductive compensation on the population genetics of sex-linked recessive lethal mutations are investigated. Simple equations are presented which describe these effects, and so complement existing population genetic theory. More importantly, this type of mutation is responsible for several severe human genetic diseases such as Duchenne muscular dystrophy. It is argued that the applications of three modern reproductive technologies--effective family planning, in utero diagnosis with termination, and embryo sexing--will lead to reproductive compensation. The adoption of any of these technologies may rapidly elevate the frequencies of those mutations which are lethal in childhood. This increase is large, in the order of 33% upwards, and occurs rapidly over two to five generations. It also depends on the source of mutations, the effect being larger if most mutations are paternal. In utero diagnosis and/or embryo sexing increase the frequency of the mutation, but simultaneously decrease disease incidence by preventing the birth of affected offspring. In contrast, effective family planning may rapidly increase both mutation frequency and disease incidence.     

Developmental flexibility and the effect of social environment on fertility and fecundity in parthenogenetic reproduction

One specialized environment that can influence development arises in the context of social interactions, including the environment contributed by a sexual partner during sexual reproduction. It is often difficult, however, to separate out the effect of mating (fertilization) from the effect of social environment. In the study reported here we examine the effect of social environment mediated by a pheromonal signal on the fertility and fecundity of the facultatively parthenogenetic cockroach Nauphoeta cinerea. By examining parthenogenetically reproducing females, we isolate the effects of social environment in the absence of mating or fertilization. Females exposed to male odors are more likely to produce parthenogenetic offspring. Further, increased exposure to the male pheromone increases the number of offspring produced. Variation in timing of reproduction is also dependent on the male. Thus, social environments are a mechanism by which males contribute to the development of their offspring, resulting in variation in development. This study illustrates the potential evolutionary importance of social environments in development, because a requirement for male-contributed environments may be a constraint to evolving asexual reproduction from a sexually reproducing species.     

Turtle mating patterns buffer against disruptive effects of climate change

For organisms with temperature-dependent sex determination (TSD), skewed offspring sex ratios are common. However, climate warming poses the unique threat of producing extreme sex ratio biases that could ultimately lead to population extinctions. In marine turtles, highly female-skewed hatchling sex ratios already occur and predicted increases in global temperatures are expected to exacerbate this trend, unless species can adapt. However, it is not known whether offspring sex ratios persist into adulthood, or whether variation in male mating success intensifies the impact of a shortage of males on effective population size. Here, we use parentage analysis to show that in a rookery of the endangered green turtle (Chelonia mydas), despite an offspring sex ratio of 95 per cent females, there were at least 1.4 reproductive males to every breeding female. Our results suggest that male reproductive intervals may be shorter than the 2-4 years typical for females, and/or that males move between aggregations of receptive females, an inference supported by our satellite tracking, which shows that male turtles may visit multiple rookeries. We suggest that male mating patterns have the potential to buffer the disruptive effects of climate change on marine turtle populations, many of which are already seriously threatened.     

Rapid de novo evolution of X chromosome dosage compensation in Silene latifolia, a plant with young sex chromosomes

Silene latifolia is a dioecious plant with heteromorphic sex chromosomes that have originated only ～10 million years ago and is a promising model organism to study sex chromosome evolution in plants. Previous work suggests that S. latifolia XY chromosomes have gradually stopped recombining and the Y chromosome is undergoing degeneration as in animal sex chromosomes. However, this work has been limited by the paucity of sex-linked genes available. Here, we used 35 Gb of RNA-seq data from multiple males (XY) and females (XX) of an S. latifolia inbred line to detect sex-linked SNPs and identified more than 1,700 sex-linked contigs (with X-linked and Y-linked alleles). Analyses using known sex-linked and autosomal genes, together with simulations indicate that these newly identified sex-linked contigs are reliable. Using read numbers, we then estimated expression levels of X-linked and Y-linked alleles in males and found an overall trend of reduced expression of Y-linked alleles, consistent with a widespread ongoing degeneration of the S. latifolia Y chromosome. By comparing expression intensities of X-linked alleles in males and females, we found that X-linked allele expression increases as Y-linked allele expression decreases in males, which makes expression of sex-linked contigs similar in both sexes. This phenomenon is known as dosage compensation and has so far only been observed in evolutionary old animal sex chromosome systems. Our results suggest that dosage compensation has evolved in plants and that it can quickly evolve de novo after the origin of sex chromosomes.     

Trends in Population Sex Ratios May be Explained by Changes in the Frequencies of Polymorphic Alleles of a Sex Ratio Gene

A test for heritability of the sex ratio in human genealogical data is reported here, with the finding that there is significant heritability of the parental sex ratio by male, but not female offspring. A population genetic model was used to examine the hypothesis that this is the result of an autosomal gene with polymorphic alleles, which affects the sex ratio of offspring through the male reproductive system. The model simulations show that an equilibrium sex ratio may be maintained by frequency dependent selection acting on the heritable variation provided by the gene. It is also shown that increased mortality of pre-reproductive males causes an increase in male births in following generations, which explains why increases in the sex ratio have been seen after wars, also why higher infant and juvenile mortality of males may be the cause of the male-bias typically seen in the human primary sex ratio. It is concluded that various trends seen in population sex ratios are the result of changes in the relative frequencies of the polymorphic alleles of the proposed gene. It is argued that this occurs by common inheritance and that parental resource expenditure per sex of offspring is not a factor in the heritability of sex ratio variation.     

Direct Male Care and Hominin Evolution: Why Male–Child Interaction Is More Than a Nice Social Idea

ABSTRACT  Early members of the genus Homo experienced heightened absolute metabolic costs, partially owing to increases in body size. However, as is characteristic of modern humans, they also likely began reproducing with shortened interbirth intervals. Male investment in offspring may help explain how this life history shift occurred. Evolutionary models of hominin male investment in offspring have traditionally focused on provisioning of females and young, yet the extent to which direct male care of offspring was evolutionarily important, from an energetic perspective, is largely unaddressed. I propose an evolutionary model of direct male care, demonstrating that males could have helped reduce the energetic burden of caregiving placed on mothers by carrying young. In doing so, males would have assisted females in achieving and maintaining an energetic condition sufficient for reproduction, thereby hastening the advent of shortened interbirth intervals that played a formative role in the success of our genus.     

Females allocate differentially to offspring size and number in response to male effects on female and offspring fitness

Female investment in offspring size and number has been observed to vary with the phenotype of their mate across diverse taxa. Recent theory motivated by these intriguing empirical patterns predicted both positive (differential allocation) and negative (reproductive compensation) effects of mating with a preferred male on female investment. These predictions, however, focused on total reproductive effort and did not distinguish between a response in offspring size and clutch size. Here, we model how specific paternal effects on fitness affect maternal allocation to offspring size and number. The specific mechanism by which males affect the fitness of females or their offspring determines whether and how females allocated differentially. Offspring size is predicted to increase when males benefit offspring survival, but decrease when males increase offspring growth rate. Clutch size is predicted to increase when males contribute to female resources (e.g. with a nuptial gift) and when males increase offspring growth rate. The predicted direction and magnitude of female responses vary with female age, but only when per-offspring paternal benefits decline with clutch size. We conclude that considering specific paternal effects on fitness in the context of maternal life-history trade-offs can help explain mixed empirical patterns of differential allocation and reproductive compensation.     

Pest control by the introduction of a conditional lethal trait on multiple loci: potential, limitations, and optimal strategies

Advances in genetics have made it feasible to genetically engineer insect strains carrying a conditional lethal trait on multiple loci. We model the release into a target pest population of insects carrying a dominant and fully penetrant conditional lethal trait on 1-20 loci. Delaying the lethality for several generations after release allows the trait to become widely spread in the target population before being activated. To determine effectiveness and optimal strategies for such releases, we vary release size, number of generations until the conditional lethality, nonconditional fitness cost resulting from gene insertions, and fitness reduction associated with laboratory rearing. We show that conditional lethal releases are potentially orders of magnitude more effective than sterile male releases of equal size, and that far smaller release sizes may be required for this approach than necessary with sterile males. For example, a release of male insects carrying a conditional lethal allele that is activated in the F4 generation on 10 loci reduces the target populatioin to 10(-4) of no-release size if there are initially two released males for every wild male. We show how the effectiveness of conditional lethal releases decreases as the nonconditional fitness reduction (i.e., fitness reduction before the trait becomes lethal) associated with the conditional lethal genes increases. For example, if there is a 5% nonconditional fitness cost per conditional lethal allele, then a 2:1 (released male:wild male) release with conditional lethal alleles that are activated in the F4 generation reduces the population to 2-5% (depending on the degree of density dependence) of the no-release size. If there is a per-allele reduction in fitness, then as the number of loci is increased there is a trade-off between the fraction of offspring carrying at least one conditional lethal allele and the fitness of the released insects. We calculate the optimal number of loci on which to insert the conditional lethal gene given various conditions. In addition, we show how laboratory-rearing fitness costs, density-dependence, and all-male versus male-female releases affect the efficiency of conditional lethal releases.     

MECP2 mutation in male patients with non-specific X-linked mental retardation

In contrast to the preponderance of affected males in families with X-linked mental retardation, Rett syndrome (RTT) is a neurological disorder occurring almost exclusively in females. The near complete absence of affected males in RTT families has been explained by the lethal effect of an X-linked gene mutation in hemizygous affected males. We report here on a novel mutation (A140V) in the MECP2 gene detected in one female with mild mental retardation. In a family study, the A140V mutation was found to segregate in the affected daughter and in four adult sons with severe mental retardation. These results indicate that MECP2 mutations are not necessarily lethal in males and that they can be causative of non-specific X-linked mental retardation.