Selection in plant populations of effectively infinite size VI. Overlapping generations

A selection model for iteroparous, monoecious, or hermaphroditic plant populations is considered which encompasses viabilities, pollen fertilities, ovule fertilities, and rates of self-fertilization which may arbitrarily depend on both age and genotype. The general conditions for establishment (which are also those for protectedness) of an allele are derived. The classical conjecture that the conditions of protectedness are the same for separated and overlapping generations if the intrinsic rates of increase are applied is discussed. For this purpose it is necessary to introduce two new intrinsic values: the intrinsic rate of self-fertilization and the intrinsic pollen-to-ovule ratio. The significance of the intrinsic values is demonstrated for complete self-fertilization, selection restricted to differential, partial self-fertilization, and sexual asymmetry (absence of proportionality between pollen and ovule production), including selection restricted to one sex. With the exception of asymmetric selection in both sexes, it turns out that the intrinsic values suffice to state the conditions for protectedness, but more information about the life histories is required to determine the exact speed of establishment. For asymmetric selection in both sexes, the concept of intrinsic value is inadequate for investigating the problem of establishment and thus the evolution of life histories. Since sexual asymmetry is rather the rule than the exception and selfing is common in plants, the consequences for finding optimal life histories are outlined.     

The optimal sex ratio for age-structured populations

A new nonlinear age-dependent model for age-structured sexual populations is introduced, based on two assumptions: (1) the birth function depends on the ages of the two parents; and (2) the death functions of the two sexes are composed of two types of additive terms depending on age and sex and on time evolution of population densities, respectively. Formal arguments are given that suggest that time-persistent age profiles may exist and that the intrinsic rate of growth for the two sexes is the same. If the ratio between the number of newborn females and the number of newborn males is equal to the square root of the ratio of the corresponding per capita birth rates, then the intrinsic rate of growth has an optimal value. The optimal sex ratio for the whole population is equal to the reciprocal value of the sex ratio at birth.     

Sex‐specific recombination rates and allele frequencies affect the invasion of sexually antagonistic variation on autosomes

The introduction and persistence of novel, sexually antagonistic alleles can depend upon factors that differ between males and females. Understanding the conditions for invasion in a two‐locus model can elucidate these processes. For instance, selection can act differently upon the sexes, or sex linkage can facilitate the invasion of genetic variation with opposing fitness effects between the sexes. Two factors that deserve further attention are recombination rates and allele frequencies – both of which can vary substantially between the sexes. We find that sex‐specific recombination rates in a two‐locus diploid model can affect the invasion outcome of sexually antagonistic alleles and that the sex‐averaged recombination rate is not necessarily sufficient to predict invasion. We confirm that the range of permissible recombination rates is smaller in the sex benefitting from invasion and larger in the sex harmed by invasion. However, within the invasion space, male recombination rate can be greater than, equal to or less than female recombination rate in order for a male‐benefit, female‐detriment allele to invade (and similarly for a female‐benefit, male‐detriment allele). We further show that a novel, sexually antagonistic allele that is also associated with a lowered recombination rate can invade more easily when present in the double heterozygote genotype. Finally, we find that sexual dimorphism in resident allele frequencies can impact the invasion of new sexually antagonistic alleles at a second locus. Our results suggest that accounting for sex‐specific recombination rates and allele frequencies can determine the difference between invasion and non‐invasion of novel, sexually antagonistic alleles in a two‐locus model.     

Effective size of fluctuating populations with two sexes and overlapping generations

We derive formulas that can be applied to estimate the effective population size N(e) for organisms with two sexes reproducing once a year and having constant adult mean vital rates independent of age. Temporal fluctuations in population size are generated by demographic and environmental stochasticity. For populations with even sex ratio at birth, no deterministic population growth and identical mean vital rates for both sexes, the key parameter determining N(e) is simply the mean value of the demographic variance for males and females considered separately. In this case Crow and Kimura's generalization of Wright's formula for N(e) with two sexes, in terms of the effective population sizes for each sex, is applicable even for fluctuating populations with different stochasticity in vital rates for males and females. If the mean vital rates are different for the sexes then a simple linear combination of the demographic variances determines N(e), further extending Wright's formula. For long-lived species an expression is derived for N(e) involving the generation times for both sexes. In the general case with nonzero population growth and uneven sex ratio of newborns, we use the model to investigate numerically the effects of different population parameters on N(e). We also estimate the ratio of effective to actual population size in six populations of house sparrows on islands off the coast of northern Norway. This ratio showed large interisland variation because of demographic differences among the populations. Finally, we calculate how N(e) in a growing house sparrow population will change over time.     

Sex chromosome evolution: life,death and repetitive DNA

Innate immunity is essential for the survival of organisms across the evolutionary spectrum. Drosophila is well studied as a model of innate immunity and has been instrumental in establishing principles of defense and gene signaling pathways that are shared with humans. Previous studies in Drosophila have not focused on differences between the sexes, and in this report we present evidence that it is essential to include differences between the sexes. Survival rates post-infection, after a fungal or bacterial infection, varied according to the combination of signaling pathway (Toll and Imd) and sex tested. We also found that antimicrobial protein gene mRNA levels for Drosomycin and Metchnikowin showed both similarities and differences between the sexes. These studies highlight the need to include both sexes in studies of immune function as well as the associated opportunities for advancing our understanding of immunity.     

Host immune response and differential survival of the sexes in Drosophila

Innate immunity is essential for the survival of organisms across the evolutionary spectrum. Drosophila is well studied as a model of innate immunity and has been instrumental in establishing principles of defense and gene signaling pathways that are shared with humans. Previous studies in Drosophila have not focused on differences between the sexes, and in this report we present evidence that it is essential to include differences between the sexes. Survival rates post-infection, after a fungal or bacterial infection, varied according to the combination of signaling pathway (Toll and Imd) and sex tested. We also found that antimicrobial protein gene mRNA levels for Drosomycin and Metchnikowin showed both similarities and differences between the sexes. These studies highlight the need to include both sexes in studies of immune function as well as the associated opportunities for advancing our understanding of immunity.     

An Allelocentric View of Life-history Evolution

For the case of weak selection, random assortment of gametes, and density-independent population regulation, we here establish the conditions under which an allele will spread in a population, with particular reference to the life-history effects of the allele, its level of dominance, and sex differences in its effects. Our treatment is simpler than that of Charlesworth (1980), but the results are essentially the same. We show that two quantities govern the selective dynamics of a two-allele single-locus system; these are level of dominance, and the difference between the per copy rates of increase of the alleles in homozygous populations. Our main conclusion is that the eventual outcome of evolution is unaffected by an allele's level of dominance, or sex differences in its effects, provided there is no overdominance. However, speed of progress to fixation is, of course, affected by these factors, and equations are derived to show how level of dominance affects speed of progress to fixation. When a dominant allele only affects the life history of one sex, its rate of spread is half that if both sexes are affected.The relationship between actual and intrinsic rates of increase is discussed and formulae are given showing the relationship for the case of weak selection.     

Sex: differences in mutation, recombination, selection, gene flow, and genetic drift

In many instances, there are large sex differences in mutation rates, recombination rates, selection, rates of gene flow, and genetic drift. Mutation rates are often higher in males, a difference that has been estimated both directly and indirectly. The higher male mutation rate appears related to the larger number of cell divisions in male lineages but mutation rates also appear gene- and organism-specific. When there is recombination in only one sex, it is always the homogametic sex. When there is recombination in both sexes, females often have higher recombination but there are many exceptions. There are a number of hypotheses to explain the sex differences in recombination. Sex-specific differences in selection may result in stable polymorphisms or for sex chromosomes, faster evolutionary change. In addition, sex-dependent selection may result in antagonistic pleiotropy or sexually antagonistic genes. There are many examples of sex-specific differences in gene flow (dispersal) and a number of adaptive explanations for these differences. The overall effective population size (genetic drift) is dominated by the lower sex-specific effective population size. The mean of the mutation, recombination, and gene flow rates over the two sexes can be used in a population genetics context unless there are sex-specific differences in selection or genetic drift. Sex-specific differences in these evolutionary factors appear to be unrelated to each other. The evolutionary explanations for sex-specific differences for each factor are multifaceted and, in addition, explanations may include chance, nonadaptive differences, or mechanistic, nonevolutionary factors.     

Wives' and husbands' expected costs and benefits of childbearing as predictors of pregnancy.

This paper examines the usefulness of 1-sex and 2-sex utility models of reproductive behavior in predicting births as consequences of wives' and husbands' perceptions of the costs and benefits of another child. We used longitudinal data on a sample of 280 white and 69 black young urban American couples. For whites, the female models proved more useful than the male models. 2-sex models generally predict more variance than do female models. It was shown that the white wife's utility considerations dominate the predictions, with husband as a junior partner and partial redundancy in female and male models. We conclude that neither sex incorporates completely the spouse's utility considerations into its own utility structure. Because some male models are surprisingly strong, researchers cannot omit males without running the risk of excluding an important component of the determinants of fertility.     

Maintenance of the sexes and persistence of a clonal organism in spatially complex metapopulations

Clonal organisms persist at a range of population sex ratios, from equal numbers of males and females to single-sex systems. When intersexual competition is strong enough to drive one sex locally extinct, the maintenance of the sexes is facilitated by the semi-independent dynamics of populations within a metapopulation. These semi-independent dynamics are influenced by dispersal and recolonization rates, which are affected by the spatial arrangement of populations. To establish the quantitative relationship between spatially complex metapopulations and the maintenance of the sexes, we used a mathematical model of the liverwort Marchantia inflexa. This clonal organism is found in discrete patches on rocks and along the banks of streams, which form single-sex and two-sex metapopulations. In this system, asexual propagules mainly disperse short distances. Long-distance between-patch dispersal and recolonization mainly occurs via sexual propagules, which require both sexes to be present. Dispersal of these two types of propagules could interact with the spatial arrangement of populations to affect the maintenance of the sexes. With our mathematical model, we found that at intermediate distances between populations, metapopulations maintained both sexes, and the spatial arrangement of populations changed the threshold at which one sex was lost. On the other hand, when populations were close to one another, one sex was lost and the single-sex metapopulation persisted through dispersal of asexual propagules. When populations were far apart, one sex was lost, and the metapopulation either went extinct due to lack of recolonization by asexual propagules or persisted because clumped populations facilitated recolonization. These idealized spatial arrangements help clarify the effects of the spatial arrangement on the maintenance of the sexes and the persistence of metapopulations of clonal organisms, which can help explain geographic parthenogenesis and the distribution of asexual populations, the persistence of asexual species, and inform the conservation of clonal organisms.     

Assessing the extent of genome-wide intralocus sexual conflict via experimentally enforced gender-limited selection

Intralocus sexual conflict, which occurs when a trait is selected in opposite directions in the two sexes, is a taxonomically widespread phenomenon. The strongest genetic evidence for a gender load due to intralocus sexual conflict comes from the Drosophila melanogaster laboratory model system, in which a negative genetic correlation between male and female lifetime fitness has been observed. Here, using a D. melanogaster model system, we utilize a novel modification of the 'middle class neighbourhood' design to relax selection in one sex, while maintaining selection in the other. After 26 generations of asymmetrical selection, we observed the expected drop in fitness of the non-selected sex compared to that of the selected sex, consistent with previous studies of intralocus sexual conflict in this species. However, the fitness of the selected sex also dropped compared to the base population. The overall decline in fitness of both the selected and the unselected sex indicates that most new mutations are harmful to both sexes, causing recurrent mutation to build a positive genetic correlation for fitness between the sexes. However, the steeper decay in the fitness of the unselected sex indicates that a substantial number of mutations are gender-limited in expression or sexually antagonistic. Our experiment cannot definitively resolve these two possibilities, but we use recent genomic data and results from previous studies to argue that sexually antagonistic alleles are the more likely explanation.     

The coevolution of sexual imprinting by males and females

Sexual imprinting is the learning of a mate preference by direct observation of the phenotype of another member of the population. Sexual imprinting can be paternal, maternal, or oblique if individuals learn to prefer the phenotypes of their fathers, mothers, or other members of the population, respectively. Which phenotypes are learned can affect trait evolution and speciation rates. “Good genes” models of polygynous systems predict that females should evolve to imprint on their fathers, because paternal imprinting helps females to choose mates that will produce offspring that are both viable and sexy. Sexual imprinting by males has been observed in nature, but a theory for the evolution of sexual imprinting by males does not exist. We developed a good genes model to study the conditions under which sexual imprinting by males or by both sexes can evolve and to ask which sexual imprinting strategies maximize the fitness of the choosy sex. We found that when only males imprint, maternal imprinting is the most advantageous strategy. When both sexes imprint, it is most advantageous for both sexes to use paternal imprinting. Previous theory suggests that, in a given population, either males or females but not both will evolve choosiness in mating. We show how environmental change can lead to the evolution of sexual imprinting behavior by both sexes in the same population.     

Size-dependent sex change can be the ESS without any size advantage of reproduction when mortality is size-dependent

Almost all models of sex change evolution assume that reproductive rate increases with body size. However, size-dependent sex changing plants often show size-independent reproductive success, presumably due to pollen limitation. Can the observed size-dependent sex change pattern be the ESS in this case? To answer this question, we analyze a game model of size-dependent sex expression in plants. We assume: (1) reproductive rate is perfectly independent of size; (2) mortality decreases with size in the same way for both sexes; (3) growth rates decrease at maturity, more for females than males. We show that the ESS is size-dependent sex expression: small individuals are vegetative, intermediate individuals are male, and large individuals are female. These results demonstrate that mortality is important in size-dependent sex allocation even when mortality rate is independent of sex. They also offer an explanation of why we see populations in poor environments to have sex ratios more biased toward the first sex relative to high quality environments.     

Sexual bimaturation and sexual size dimorphism in animals with asymptotic growth after maturity

Many animal taxa exhibit a positive correlation between sexual size dimorphism and sex differences in age at maturity, such that members of the larger sex mature at older ages than members of the smaller sex. Previous workers have suggested that sexual bimaturation is a product of sex differences in growth trajectories, but to date no one has tested this hypothesis. The current study uses growth-based models to study relationships between sexual size dimorphism and sexual bimaturation in species with asymptotic growth after maturity. These models show that sex differences in asymptotic size would produce sexual bimaturation even if both sexes approach their respective asymptotic sizes at the same age, mature at the same proportion of asymptotic size and have otherwise equivalent growth and maturation patterns. Furthermore, our analyses show that there are three ways to reduce sexual bimaturation in sexually size-dimorphic species: (1) higher characteristic growth rates for members of the larger sex, (2) larger size at birth, hatching or metamorphosis for members of the larger sex or (3) smaller ratio of size at maturity to asymptotic size (relative size at maturity) for members of the larger sex. Of these three options, sex differences in relative size at maturity are most common in size-dimorphic species and, in both male-larger and female-larger species, members of the larger sex frequently mature at a smaller proportion of their asymptotic size than do members of the smaller sex. Information about the growth and maturation patterns of a taxon can be used to determine relationships between sexual size dimorphism and sexual bimaturation for the members of that taxon. This process is illustrated for Anolis lizards, a genus in which both sexes exhibit the same strong correlation (r 0.97) between size at maturity and asymptotic size, and in which the relative size at maturity is inversely related to asymptotic size for both sexes. As a result, sexually size-dimorphic species of anoles exhibit the expected pattern of a smaller relative size at maturity for members of the larger sex. However, for species in this genus, sex differences in the relative size at maturity are not strong enough to produce the same age at maturity for both sexes in sexually size-dimorphic species. Members of the larger sex (usually males) are still expected to mature at older ages than members of the smaller sex in Anolis lizards.     

Why is mutual mate choice not the norm? Operational sex ratios,sex roles and the evolution of sexually dimorphic and monomorphic signalling.

Biases in the operational sex ratio (OSR) are seen as the fundamental reason behind differential competition for mates in the two sexes, and as a strong determinant behind differences in choosiness. This view has been challenged by Kokko and Monaghan, who argue that sex-specific parental investment, mortalities, mate-encounter rates and quality variation determine the mating system in a way that is not reducible to the OSR. We develop a game-theoretic model of choosiness, signalling and parental care, to examine (i) whether the results of Kokko and Monaghan remain robust when its simplifying assumptions are relaxed, (ii) how parental care coevolves with mating strategies and the OSR and (iii) why mutual mate choice is observed relatively rarely even when both sexes vary in quality. We find qualitative agreement with the simpler approach: parental investment is the primary determinant of sex roles instead of the OSR, and factors promoting choosiness are high species-specific mate-encounter rate, high sex-specific mate-encounter rate, high cost of breeding (parental investment), low cost of mate searching and highly variable quality of the opposite sex. The coevolution of parental care and mating strategies hinders mutual mate choice if one parent can compensate for reduced care by the other, but promotes it if offspring survival depends greatly on biparental care. We argue that the relative rarity of mutual mate choice is not due to biases in the OSR. Instead, we describe processes by which sexual strategies tend to diverge. This divergence is prevented, and mutual mate choice maintained, if synergistic benefits of biparental care render parental investment both high and not too different in the two sexes.     

Sex-specific variation in the genome-wide recombination rate

In most species that reproduce sexually, successful gametogenesis requires recombination during meiosis. The number and placement of crossovers (COs) vary among individuals, with females and males often presenting the most striking contrasts. Despite the recognition that the sexes recombine at different rates (heterochiasmy), existing data fail to answer the question of whether patterns of genetic variation in recombination rate are similar in the two sexes. To fill this gap, we measured the genome-wide recombination rate in both sexes from a panel of wild-derived inbred strains from multiple subspecies of house mice (Mus musculus) and from a few additional species of Mus. To directly compare recombination rates in females and males from the same genetic backgrounds, we applied established methods based on immunolocalization of recombination proteins to inbred strains. Our results reveal discordant patterns of genetic variation in the two sexes. Whereas male genome-wide recombination rates vary substantially among strains, female recombination rates measured in the same strains are more static. The direction of heterochiasmy varies within two subspecies, Mus musculus molossinus and Mus musculus musculus. The direction of sex differences in the length of the synaptonemal complex and CO positions is consistent across strains and does not track sex differences in genome-wide recombination rate. In males, contrasts between strains with high recombination rate and strains with low recombination rate suggest more recombination is associated with stronger CO interference and more double-strand breaks. The sex-specific patterns of genetic variation we report underscore the importance of incorporating sex differences into recombination research.     

Longevity in Bovids Is Promoted by Sociality,But Reduced by Sexual Selection

Selection on intrinsic lifespan depends on both external factors affecting mortality and inherent tradeoffs in resource allocation between viability traits and other fitness-related traits. Longevity is therefore likely to vary between species in a sex-specific manner due to interspecific and intersexual differences in behavioural ecology. Here I focus on the bovid family to test two central hypotheses on longevity selection using the comparative method: firstly, that a reduction of extrinsic mortality in social species strengthens selection on intrinsic lifespan, and secondly, that mortality costs associated with intense sexual selection lead to shorter intrinsic lifespan. The results show that longevity (i) increases with sociality in both sexes and (ii) decreases with male-biased sexual size-dimorphism, but in males only. These discoveries suggest that sociality, a key ungulate strategy to reduce predation-related mortality, selects for inherently longer-lived organisms, and that strong sexual selection, which is known to compromise survival rates in the wild, can constrain also intrinsic lifespan. The contrasting results for males and females indicate that selection on longevity in the two sexes is partly uncoupled.     

The absence of sex-biased dispersal in the cooperatively breeding grey-crowned babbler

1. Cooperatively breeding birds are thought to be especially vulnerable to habitat fragmentation, in part because dispersal is typically restricted for one sex, increasing the likelihood of inbreeding. Knowledge of dispersal is essential to conservation efforts, but is often hampered by our inability to measure its frequency and distance when dispersal is infrequent and difficult to observe. 2. Disrupted dispersal is a purported cause of decline in the Australian grey-crowned babbler (Pomatostomus temporalis). Both sexes of offspring delay dispersal for up to several years to help parents raise subsequent broods, yet little else is known about the dispersal of this cooperatively breeding woodland bird. 3. As both sexes appear to help, but only male helpers boost fledgling production, we hypothesized that males would be the more philopatric sex in this species, and that female grey-crowned babblers would disperse over greater distances. 4. To ensure reliable determination of sex and minimize bias towards detecting short-distance dispersal events, we combined molecular-based sexing and analyses of population genetic structure using polymorphic microsatellite loci with observational data obtained over multiple field seasons. 5. Observations of banded birds showed only infrequent fission of groups or short-distance dispersal (mean=854 m), but no apparent sex-bias in these patterns. 6. There was significant genetic differentiation between social groups, but not between the sexes. Spatial genetic autocorrelation analysis of breeders revealed a random distribution of genotypes across the study area for both sexes. Thus, contrary to expectations, we found no genetic evidence for restricted dispersal or for sex-biased dispersal over the 85-km scale of this study, indicating that effective dispersal occurs over greater distances and more frequently than recoveries of banded birds indicated. 7. We conclude that while constraints on independent breeding encourage high rates of philopatry, incest avoidance nonetheless drives high rates of dispersal by both sexes. In fragmented habitat, the dispersal dynamics of this cooperatively breeding species are unlikely to render them particularly vulnerable to genetic consequences such as inbreeding, but may lead to increased group dissolution.     

Sex differences in infant mortality in Spitalfields, London, 1750-1839

This study examines sex differences in infant mortality in Spitalfields, London, and the estimated contribution of endogenous and exogenous factors to neonatal and infant mortality using the biometric model from 1750 to 1839. There was a marked decline in the risk of death during infancy and the neonatal period for both sexes during the study period. There was significant excess male infant mortality compared with that of females in the 1750-59 cohort, estimated from baptism and burial registers, but not in later cohorts. Similarly, males had higher neonatal mortality rates than females in 1750-59 but not in later cohorts. Biometric analyses suggest that the observed decrease in neonatal mortality in both sexes was caused by a reduction in both endogenous and exogenous causes of death. The contribution of maternal health and breast-feeding practices to the observed patterns of mortality is discussed in the light of available evidence.