The Comparative Biology of Genetic Variation for Conditional Sex Ratio Behavior in a Parasitic Wasp, Nasonia Vitripennis

Using genetic markers, we tracked the sex ratio behavior of individual females of the parasitic wasp, Nasonia vitripennis, in foundress groups of size 1, 2, 4, 8 and 16. Comparison of 12 isofemale strains extracted from a natural population reveals significant between-strain heterogeneity of sex ratios produced in all sizes of foundress group. Under simple assumptions about population structure, this heterogeneity results in heterogeneity of fitnesses. The strains differ in their conditional sex ratio behavior (the sex ratio response of a female to foundress groups of different sizes). Females of some strains produce more males as foundress group size increases (up to size eight). Females of another strain produce more males when not alone but do not respond differentially to group size otherwise. Females of two other strains show no conditional sex ratio behavior. Females of only two strains behave differently in foundress groups of size 8 and 16. Correlation and regression analyses indicate that the strains differ significantly in their fit to the predictions of an evolutionarily stable strategy (ESS) model of conditional sex ratio behavior. Such heterogeneity contradicts the notion that females of this species possess conditional sex ratio behavior that is optimal in the ESS sense. The results imply that this ESS model is useful but not sufficient for understanding the causal basis of the evolution of this behavior in this species. This is the first report on the sex ratio behavior of individual females in multiple foundress groups in any species of parasitic wasp. Data of this type (and not foundress group or ``patch'''' sex ratios) are essential for testing evolutionary models that predict the sex ratio behaviors of individuals. We suggest that a test for an ESS model include the answers to two important questions: 1) is the model quantitatively accurate? and 2) is there reasonable evidence to indicate that natural selection has caused individuals to manifest the ESS behavior?     

Genetic Variation for Sex Ratio Traits within a Natural Population of a Parasitic Wasp, Nasonia Vitripennis

By analyzing isofemale strains extracted from a natural population of Nasonia vitripennis, we detected variation for the sex ratios produced in fresh hosts (first sex ratios) and in previously parasitized hosts (second sex ratios). Under simple assumptions of population structure, this between-strain heterogeneity of first sex ratios results in heterogeneity of fitnesses. There is approximately ten percent difference in average fitnesses between the strains. (The fitnesses of second sex ratios are analyzed in the accompanying paper.) Average first and average second sex ratios are uncorrelated. There is significant between-female heterogeneity within some strains for first sex ratios but not for second sex ratios. In addition, the average direct-developing and diapause first sex ratios (but not second sex ratios) are significantly correlated. There are significant correlations between the direct-developing and diapause sex ratios produced by the same female. The strains differ in their effects on the sex ratio and size of another female's brood in the same host. Data on these types of variation for sex ratio traits are essential for further progress in the study of sex ratio evolution.     

Quantitative Genetics of Sex Ratio Traits in the Parasitic Wasp, Nasonia Vitripennis

We detected significant parent-offspring regressions for the first sex ratio (the sex ratio produced by a female in a fresh host) and the second sex ratio (the sex ratio produced by a female in a previously parasitized host) in the parasitic wasp, Nasonia vitripennis. For both traits, estimates of the narrow-sense heritability range from &0.05 to &0.15 (depending on how the data are analyzed). The study population was derived from isofemale strains created from wasps captured in a single bird nest. The same population exhibited no significant parent-offspring regression for the brood sizes associated with the first and second sex ratios. There may be a significant negative parent-offspring regression for diapause proportion in the first sex ratio broods. The estimates of the genetic correlations between first and second sex ratios are positive although almost all are not significantly different from 0.0. To our knowledge, this study is the first ``fine-scale' analysis of genetic variation for sex ratio traits in any species of insect. Such studies are an essential part of the assessment of the validity of claims that sex ratio traits are locally optimal.     

Plasmid macro-evolution: selection of deletions during adaptation in a nutrient-limited environment

A study was made of the intra-and inter-population variability of the main traits involved in Trichogramma (T. brassicae and T. cacoeciae) efficiency in host exploitation: longevity, fecundity, progeny viability, progeny sex ratio and progeny allocation. The analysis of isofemale strains shows that differences in progeny viability, progeny sex ratio and progeny allocation are transmissible and relatively stable over two successive generations. Comparison of three strains of T. brassicae originating from different locations, demonstrates differences in fecundity, progeny sex ratio and progeny allocation. Differences in host exploitation strategies also exist between two sympatric populations of T. brassicae and T. cacoeciae. No significant correlation appears between the traits which discriminate populations. The ecological and evolutionary significance and the agronomical importance of the results are discussed.     

Sorting out the effects of Wolbachia, genotype and inbreeding on life-history traits of a spider mite

Wolbachia bacteria manipulate host reproduction by inducing cytoplasmic incompatibility (CI) and sex ratio distortion. Wolbachia are transmitted from mother to offspring through the cytoplasm of the egg. Therefore, reproduction of Wolbachia is tightly coupled to reproduction of its host. Mathematical analysis predicts that in the course of evolution, traits that reduce the physiological costs of the infection will be selectively favored. For a Wolbachia-host system to evolve, traits under selection must have some genetic component and variation must be present in the population. We have previously established that highly inbred isofemale lines of the two-spotted spider mite Tetranychus urticae may differ regarding the effects of infection by Wolbachia, and that at least some of the traits affected had a genetic component. However, the effects measured could have been affected by the fact that the lines were severely inbred prior to the experiments. In this paper we attempt to distinguish between the effects of Wolbachia, isofemale line, and inbreeding. We show that Wolbachia did not affect longevity but infected females produced smaller clutch sizes, more daughter-biased sex ratios and had decreased F1 mortality; between-line variation was found for clutch size, F1 mortality and sex ratio; finally, inbreeding resulted in an overall reduction of clutch sizes, and a change in survival curves and mean longevity. This revised version was published online in July 2006 with corrections to the Cover Date.     

Population dynamics of a vertically transmitted, parasitic sex ratio distorter and its amphipod host

We investigate the population dynamics of a vertically transmitted, parasitic sex ratio distorter ( Nosema granulosis ) and its amphipod host ( Gammarus duebeni ), using field measurements to quantify and test alternative theoretical models of the interaction. We measure parasite, host population and transmission parameters at four locations on the Isle of Cumbrae, Scotland at monthly intervals for two years. We develop a simple infinite population model and test its predictions for parasite prevalence using field measurements of the parameters. Parasite prevalence is maintained at relatively low levels at all four sites (20–42%), consistently below that predicted. The parasite imposes a slight fitness cost on its host by reducing female fecundity, but this cost cannot account for the relatively low prevalences observed. We also investigate the importance of population structure, comparing parasite prevalence across sites and sampling intervals to look for evidence of spatial and temporal asynchrony as predicted by metapopulation models. We find significant temporal and spatial heterogeneity in parasite prevalence although there was also evidence that parasite dynamics were synchronous across sites. These data suggest that the parasite is unlikely to drive local population dynamics through cycles of extinction and recolonization at the scale measured. As the host (adult) population sex ratio was male-biased, local population crashes are unlikely to be induced by the parasite, contrary to theoretical predictions.     

The Crossveinless Polygenes in an Iowa Population

A natural population of Drosophila melanogaster was tested for the presence of crossveinless (cve) alleles over the course of a summer. Approximately 8% of the wild-caught females tested carried enough cve alleles to produce true-breeding crossveinless lines. In some cases, different isofemale lines produced identical cve strains. Also, differences were sometimes observed among independently selected cve sublines of a given isofemale line.-The cv-2 allele was found to occur with a frequency of about 1% to 2%.     

Brood sex ratio variation in a cooperatively breeding bird

In cooperatively breeding species, the fitness consequences of producing sons or daughters depend upon the fitness impacts of positive (repayment hypothesis) and negative (local competition hypothesis) social interactions among relatives. In this study, we examine brood sex allocation in relation to the predictions of both the repayment and the local competition hypotheses in the cooperatively breeding long-tailed tit Aegithalos caudatus. At the population level, we found that annual brood sex ratio was negatively related to the number of male survivors across years, as predicted by the local competition hypothesis. At an individual level, in contrast to predictions of the repayment hypothesis, there was no evidence for facultative control of brood sex ratio. However, immigrant females produced a greater proportion of sons than resident females, a result consistent with both hypotheses. We conclude that female long-tailed tits make adaptive decisions about brood sex allocation.     

Lack of seasonal changes in mitochondrial DNA variability of a Drosophila subobscura population

Restriction site analysis of mtDNA of 550 isofemale lines corresponding to different seasonal samples of a single geographic population of Drosophila subobscura was carried out. The distribution pattern of haplotypes was similar to that observed for the entire range of the species on the European continent: two haplotypes were equally and highly frequent, and a set of sporadic haplotypes were almost never present in more than one seasonal sampling. No statistically significant evidence was found for between-population heterogeneity across time, and the mean within-population variation was similar to other mtDNA restriction site analyses previously reported for D. subobscura populations. These observations could be interpreted in terms of the neutral mutation hypothesis where the entire population has not yet reached an equilibrium. The causes of this non-equilibrium are most likely periodic winter bottlenecks, phenomena that particularly affect the distribution of mtDNA haplotypes across time.     

Spatial dynamics of adaptive sex ratios

According to Fisherian sex allocation theory, parents that can adjust their offspring sex ratio in response to skews in population sex ratio will maximize their fitness over parents lacking this ability. There is good evidence that adaptive sex ratio adjustment occurs in many natural populations, but deviations from theoretical predictions have also been observed. These anomalies may be more apparent than real. When the spatial dimension of sex ratio variation is ignored, then a mismatch between empirical data and theoretical predictions based on panmictic mating is to be expected. We illustrate this with data on human sex ratio variation in 21 preindustrial populations, and with a cellular automaton model built to obey Fisherian sex allocation rules. The results from the model generally match with the data. When information about the ambient sex ratio is limited, then the sex allocation decisions may appear locally maladaptive. In general, the results indicate that Fisher's sex-ratio theory may have greater explanatory power than previously thought.     

Estimation of the Allele Number in a Natural Population by the Method of Isofemale Lines

The number of alleles present in a natural population of unknown structure is estimated using a sequential sampling procedure applied to isofemale lines. Two questions are raised: how many individuals per isofemale line must be assayed and how many isofemale lines must be sampled to get an adequate sample to estimate the number of alleles, at a given risk, of the natural population? On the one hand, we show that when wild females are inseminated once, only two individuals per line are required. On the other hand, the number of isofemale lines that must be sampled depends on the risk chosen of losing an allele, on the number of alleles present in the population and on their drawing probabilities. When the population structure is known, an accurate answer can be provided. For an unknown population structure, one general sequential sampling previously described by J. Rouault and P. Capy is proposed to estimate the number of alleles in the population from data on isofemale lines.     

Sex ratio, life-history invariants, and patterns of sex change in a family of protandrous gastropods

Application of optimality theory to the evolution of life histories has been broadly successful in predicting the conditions favoring sex change, the type of change, and the timing of such changes. The size advantage hypothesis predicts that the optimal size at which an individual should change sex is a function of its size and the size and sex of its potential mates. I collected data on the size, sex, and grouping of individuals of 27 populations of 19 species of the calyptraeids, a family of protandrous marine gastropods that includes Crepidula. These data are used to test the following predictions about variation in size at sex change: (1) sex ratio is biased toward the first sex; (2) the ratio of the size at sex change to the maximum size is a life-history invariant; and (3) species that form variable-sized groups or stacks have more variation in size at sex change than species that show less variation in stack formation. Across all 19 species, sex ratio was not significantly more often biased toward the first sex than it was toward the second sex, although sex ratios were significantly male biased more often than they were significantly female biased. Sex ratios ranged from 0.05 to 0.91, and this variation was related to mode of development, skew in size distribution, and frequency of stacking, but not with maximum body size. There was little evidence that the ratio of size at sex change and maximum size is invariant. There is evidence that one of the main underlying assumptions of this life-history invariant, that male fertility increases with the same function of size in all species, is invalid for calyptraeids and probably for other animals. Finally, species that form larger stacks or mating groups had more variation in size at sex change within a population than species that were generally solitary. These results suggest that information about individual groupings should be included in predictions of life-history theory and that more information about the relationship between male fitness and size is also needed.     

A spatially explicit model of sex ratio evolution in response to sex-biased dispersal

Sex-biased dispersal occurs in all seed plants and many animal species. Theoretical models have shown that sex-biased dispersal can lead to evolutionarily stable biased sex ratios. Here, we use a spatially explicit chessboard model to simulate the evolution of sex ratio in response to sex-biased dispersal range and sex-biased dispersal rate. Two life cycles are represented in the model: one in which both sexes disperse before mating (DDM), the other in which males disperse before mating and mated females or zygotes disperse after mating (DMD). Model parameters include factors like dispersal rate, dispersal range, number of individuals per patch, and habitat heterogeneity.When dispersal range is sex biased, we find that, in a homogeneous environment, the sex ratio is generally biased towards the sex that disperses more widely (sex ratio range: 0.47–0.52). In a heterogeneous environment, the sex ratio is generally biased towards the more dispersive sex in good habitats, and towards the less dispersive sex in poor habitats (sex ratio range: 0–1). This is opposite to the effect of sex-biased dispersal rate, which favours the production of the more dispersive sex in poor habitats and the less dispersive sex in good habitats (sex ratio range: 0–1). To allow for a comparison with theoretical predictions, data concerning sex-biased dispersal and habitat-dependent sex ratios should thus incorporate information about the spatial scale of both dispersal and environmental heterogeneity.     

Adaptive strategies in natural populations of Drosophila

Summary Adult tolerance of ethanol vapour in a closed system containing 12% ethanol in solution, decreases in a cline from southern to northern Australia. However a Darwin population is more tolerant than predicted from its latitude. Ethanol tolerance races in Australia have almost certainly evolved within the last 100–150 years, because of resource unavailability prior to that time. Within populations, variation among isofemale strains is lowest in the climatically extreme southern Melbourne (37°S) and northern Darwin and Melville I. (11–12°S) populations. This suggests low resource diversity within extreme populations compared with the climatically less extreme Brisbane (28°S) and especially Townsville (19°S) populations. For desiccation resistance, the population rankings are: Darwin Melbourne > Townsville > Brisbane Melville I. and for development time, rankings are similar: Darwin Melbourne < Townsville < Brisbane Melville I.Therefore resource utilization heterogeneity is greatest in populations not greatly stressed by desiccation and where development times are extended. In total therefore, the utilization of a diversity of resources is a feature of populations tending somewhat towards a K-strategy; this is emphasized by the relative heterogeneity among isofemale strains of these populations for desiccation resistance and to a lesser extent development times.The D. melanogaster gene pool can be viewed as made up of climate-associated races. Since the ethanol tolerances of adjacent (and climatically similar) Darwin and Melville I. are very different, resource utilization races may occur within climatic races. Such a mosaic of resource utilization races are more likely in climatically extreme than in optimal habitats.     

Sex allocation by a mite parasitic on insects: local mate competition,host quality and operational sex ratio

The aim of this study was to test the predictions of local mate competition (LMC), host quality (HQ) and operational sex ratio (OSR) models, using a non-arrhenotokous parasitic mite, Hemisarcoptes coccophagus (Astigmata: Hemisarcoptidae). The life-history pattern of this mite meets the assumptions of these sex allocation models. Mating group size (LMC model), HQ and OSR affected the sex allocation of H. coccophagus females. Only young mite females adjusted the sex ratio of their progenies according to the predictions of LMC and HQ models; the sex allocation of old females was contrary to these predictions. We explain these patterns by the dynamic nature of the mite's population structure. When parents are young, their population distribution is patchy and progeny matings are local; hence sex allocation is in accordance with LMC theory. When parents become older, their populations shift towards panmixis; factors which had operated previously no longer exist. Consequently, females adjust the sex ratio of late progenies so that it can compensate for the earlier sex allocation, in order to make their total sex ratio unbiased, as expected in panmictic populations. Our data, expressed as the cumulative sex ratio, support this hypothesis.     

Sex-ratio evolution in sex changing animals

Sex allocation theory is often able to make clear predictions about when individuals should facultatively adjust their offspring sex ratio (proportion male) in response to local conditions, but not the consequences for the overall population sex ratio. A notable exception to this is in sex changing organisms, where theory predicts that: (1) organisms should have a sex ratio biased toward the "first" sex: (2) the bias should be less extreme in partially sex changing organisms, where a proportion of the "second" sex matures directly from the juvenile stage; and (3) the sex ratio should be more biased in protogynous (female first) than in protandrous (male first) species. We tested these predictions with a comparative study using data from 121 sex changing animal species spanning five phyla, covering fish, arthropods, echinoderms, molluscs, and annelid worms. We found support for the first and third predictions across all species. The second prediction was supported within the protogynous species (mainly fish), but not the protandrous species (mainly invertebrates).     

Contest versus scramble competition for mates: The composition and spatial structure of a population of gray mouse lemurs (Microcebus murinus) in North-west Madagascar

The modes of intrasexual competition interacting in many dispersed societies of nocturnal solitary foragers are still poorly understood. In this study we investigate the spatial structure within a free-living population of gray mouse lemurs (Microcebus murinus) in order to test for the first time the predictions from two contrasting models of male intrasexual competition on the population level. The contest competition model predicts an uneven distribution of the sexes in a population nucleus with a female biased sex ratio in the center and a male biased sex ratio in the periphery. In contrast the scramble competition model predicts males and females being distributed evenly throughout their habitat with a constant sex ratio. Nine capture/recapture periods within three consecutive mating seasons revealed a continuous male biased sex ratio in the adult population with even trapping rates for the sexes. The male biased sex ratio could either be explained with postnatal female biased mortality or with a male biased natal sex ratio. This male biased sex ratio was apparent in all parts of the study site, indicating that the population was not subdivided into a female biased core and a male biased periphery. Furthermore, the majority of adult males have been captured at the same site as or in vicinity to females. Consequently, a large proportion of males had spatial access to females during the mating season. No signs of monopolization of females by certain dominant males could be detected. These data support the predictions from the scramble competition model and the concept of a promiscuous mating system for this species.     

Patterns and mechanisms of sex ratio distortion in the Collaborative Cross mouse mapping population

In species with single-locus, chromosome-based mechanisms of sex determination, the laws of segregation predict an equal ratio of females to males at birth. Here, we show that departures from this Mendelian expectation are commonplace in the 8-way recombinant inbred Collaborative Cross (CC) mouse population. More than one-third of CC strains exhibit significant sex ratio distortion (SRD) at wean, with twice as many male-biased than female-biased strains. We show that these pervasive sex biases persist across multiple breeding environments, are stable over time, and are not mediated by random maternal effects. SRD exhibits a heritable component, but QTL mapping analyses fail to nominate any large effect loci. These findings, combined with the reported absence of sex ratio biases in the CC founder strains, suggest that SRD manifests from multilocus combinations of alleles only uncovered in recombined CC genomes. We explore several potential complex genetic mechanisms for SRD, including allelic interactions leading to sex-biased lethality, genetic sex reversal, chromosome drive mediated by sex-linked selfish elements, and incompatibilities between specific maternal and paternal genotypes. We show that no one mechanism offers a singular explanation for this population-wide SRD. Instead, our data present preliminary evidence for the action of distinct mechanisms of SRD at play in different strains. Taken together, our work exposes the pervasiveness of SRD in the CC population and nominates the CC as a powerful resource for investigating diverse genetic causes of biased sex chromosome transmission.     

Colony structure, provisioning and sex allocation in the sweat bee Halictus ligatus (Hymenoptera: Halictidae)

Population and colony-level sex allocation and nest productivity in the eusocial sweat bee Halictus ligatus Say were studied by excavating nests during one season. The emphasis was on measuring the provision masses, which differ in size and shape depending on the sex of the egg to be laid on them (male-producing provision masses are smaller and more or less round, whereas gyne-producing provision masses are larger and 'loaf-shaped). The primary aim of this study was to test theoretical predictions about female-bias of the sex ratio in the summer brood, both on the population level and on the colony level.
The overall sex ratio of the summer brood was moderately biased towards gynes. A significant positive correlation between the overall size of provision masses (as an estimate for the degree of female bias of the nest sex ratio) and the number of eusocial workers was found. This relationship further improved in partial analyses in which the provision mass weights were adjusted for sampling date, removing the effect of protandry. Foundress size, however, had no effect on the second brood provision masses and neither was there an effect of worker number on the size of gynes and males separately. In the first brood only the size of the foundress had a consistently positive effect on the size of the provision masses and on the size of the emerging daughter workers.
The observed increase of female bias in the nest sex ratio with increasing numbers of eusocial worker bees conforms to optimization predictions following from kin-selection theory.     

Local resource competition and local resource enhancement shape primate birth sex ratios

Sex ratio theory provides a powerful source of testable predictions about sex allocation strategies. Although studies of invertebrates generally support predictions derived from the sex ratio theory, evidence for adaptive sex ratio biasing in vertebrates remains contentious. This may be due to the fact that most studies of vertebrates have focused on facultative adjustment in relation to maternal condition, rather than processes that might produce uniform sex biases across individuals. Here, we examine the effects of local resource enhancement (LRE) and local resource competition (LRC) on birth sex ratios (BSRs). We also examine the effects of sex differences in the costs of rearing male and female offspring on BSRs. We present data from 102 primate species and show that BSRs are skewed in favour of the dispersing sex in species that do not breed cooperatively, as predicted by the LRC model. In accordance with the LRE model, BSRs are generally skewed in favour of the more beneficial sex in cooperatively breeding primate species. There is no evidence that BSRs reflect the extent of sexual size dimorphism, an indirect measure of the costs of rearing male and female offspring. These analyses suggest that adaptive processes may play an important role in the evolution of BSRs in vertebrates.