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.     

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?     

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.     

Deletion Analysis of the Selfish B Chromosome, Paternal Sex Ratio (Psr), in the Parasitic Wasp Nasonia Vitripennis

Paternal Sex Ratio (PSR) is a ``selfish' B chromosome in the parasitoid wasp Nasonia vitripennis. It is transmitted via sperm, but causes supercondensation and destruction of the paternal chromosomes in early fertilized eggs. Because this wasp has haplodiploid sex determination, the effect of PSR is to convert diploid (female) eggs into haploid (male) eggs that carry PSR. Characterizing its genetic structure is a first step toward understanding mechanisms of PSR action. The chromosome is largely heterochromatic and contains several tandemly repeated DNA sequences that are not present on the autosomes. A deletion analysis of PSR was performed to investigate organization of repeats and location of functional domains causing paternal chromosome destruction. Deletion profiles using probes to PSR-specific repetitive DNA indicate that most repeats are organized in blocks on the chromosome. This study shows that the functional domains of PSR can be deleted, resulting in nonfunctional PSR chromosomes that are transmitted to daughters. A functional domain may be linked with the psr22 repeat, but function may also depend on abundance of PSR-specific repeats on the chromosome. It is hypothesized that the repeats act as a ``sink' for a product required for proper paternal chromosome processing. Almost all deletion chromosomes remained either functional of nonfunctional in subsequent generations following their creation. One chromosome was exceptional in that it reverted from nonfunctionality to functionality in one lineage. Transmission rates of nonfunctional deletion chromosomes were high through haploid males, but low through diploid females.     

Temporal Variation in the Sex Ratio of a Natural Population of a Multivoltine Gall-Inducing Braconid Wasp

Temporal variation in the sex ratio of populations with continuous generations is poorly understood. We report changes in the sex ratio of a tropical gall-inducing braconid wasp throughout the fruiting season of its host plant. At the beginning of the season, fruits produce male biased sex ratios; at the end, female biased sex ratios. This change results from differential sex allocation rather than just earlier male emergence. A male bias followed by female bias is predicted following an increase in recruitment as occurs during the start of the main fruiting season, because males are likely to have the more consistent reproductive value over time. An initial male bias might also result from selection for protandry, or from constrained sex allocation during the low-density non-fruiting season.     

高原鼠兔种群的性比

The sex ratio (♂ / ♀ ) of plateau pika's (Ochotona curzoniae) population was studied by re-captured method in the region of the Haibei Mpine Meadow Ecosystem Research Station, Northwest Institute of Plateau Biology, the Chinese Academy of Sciences from April of 2001 to August of 2002. The result showed that there was no significant difference from 1:1 in adult's sex ratio in whole breeding season, whereas the sex ratio of juvenile had some fluctuations among different age stages. The sex ratio of the second litter varied significantly from embryo to 60-day-old, but no difference at the first and the third litter. We concluded it was caused by conflict between maternal strategy and juvenile's strategy. No significant differences of sex ratio were found both in adult and juvenile between 2001 and 2002. The sex ratio of plateau pika before and after overwintering did not vary. In summary,we proposed that sex ratio of plateau pika's population was not influenced by exogenous factors, but some serf-regulation mechanisms may be involved.     

Wolbachia Infection in a Natural Parasitoid Wasp Population

The maternally transmitted bacterium Wolbachia pipientis is well known for spreading and persisting in insect populations through manipulation of the fitness of its host. Here, we identify three new Wolbachia pipientis strains, wHho, wHho2 and wHho3, infecting Hyposoter horticola, a specialist wasp parasitoid of the Glanville fritillary butterfly. The wHho strain (ST435) infects about 50% of the individuals in the Åland islands in Finland, with a different infection rate in the two mitochondrial (COI) haplotypes of the wasp. The vertical transmission rate of Wolbachia is imperfect, and lower in the haplotype with lower infection rate, suggesting a fitness trade-off. We found no association of the wHho infection with fecundity, longevity or dispersal ability of the parasitoid host. However, preliminary results convey spatial associations between Wolbachia infection, host mitochondrial haplotype and parasitism of H. horticola by its hyperparasitoid, Mesochorus cf. stigmaticus. We discuss the possibility that Wolbachia infection protects H. horticola against hyperparasitism.     

The Sex Ratio of Heterodera glycines at Low Population Densities

The sex ratio of the Arkansas 1 isolate of Heterodera glycines was determined in experiments in which ''Lee'' soybean was inoculated with either one or two larvae. A 3:1 male to female sex ratio was established for this isolate under the test conditions used. No influence of one nematode on the penetration and development to adult of another nematode in the same root was detected in double larval inoculations.     

Unique Features of Odorant-Binding Proteins of the Parasitoid Wasp Nasonia vitripennis Revealed by Genome Annotation and Comparative Analyses

Insects are the most diverse group of animals on the planet, comprising over 90% of all metazoan life forms, and have adapted to a wide diversity of ecosystems in nearly all environments. They have evolved highly sensitive chemical senses that are central to their interaction with their environment and to communication between individuals. Understanding the molecular bases of insect olfaction is therefore of great importance from both a basic and applied perspective. Odorant binding proteins (OBPs) are some of most abundant proteins found in insect olfactory organs, where they are the first component of the olfactory transduction cascade, carrying odorant molecules to the olfactory receptors. We carried out a search for OBPs in the genome of the parasitoid wasp Nasonia vitripennis and identified 90 sequences encoding putative OBPs. This is the largest OBP family so far reported in insects. We report unique features of the N. vitripennis OBPs, including the presence and evolutionary origin of a new subfamily of double-domain OBPs (consisting of two concatenated OBP domains), the loss of conserved cysteine residues and the expression of pseudogenes. This study also demonstrates the extremely dynamic evolution of the insect OBP family: (i) the number of different OBPs can vary greatly between species; (ii) the sequences are highly diverse, sometimes as a result of positive selection pressure with even the canonical cysteines being lost; (iii) new lineage specific domain arrangements can arise, such as the double domain OBP subfamily of wasps and mosquitoes.     

The Dynamics of Sex Ratio Evolution: From the Gene Perspective to Multilevel Selection

The new dynamical game theoretic model of sex ratio evolution emphasizes the role of males as passive carriers of sex ratio genes. This shows inconsistency between population genetic models of sex ratio evolution and classical strategic models. In this work a novel technique of change of coordinates will be applied to the new model. This will reveal new aspects of the modelled phenomenon which cannot be shown or proven in the original formulation. The underlying goal is to describe the dynamics of selection of particular genes in the entire population, instead of in the same sex subpopulation, as in the previous paper and earlier population genetics approaches. This allows for analytical derivation of the unbiased strategic model from the model with rigorous non-simplified genetics. In effect, an alternative system of replicator equations is derived. It contains two subsystems: the first describes changes in gene frequencies (this is an alternative unbiased formalization of the Fisher-Dusing argument), whereas the second describes changes in the sex ratios in subpopulations of carriers of genes for each strategy. An intriguing analytical result of this work is that the fitness of a gene depends on the current sex ratio in the subpopulation of its carriers, not on the encoded individual strategy. Thus, the argument of the gene fitness function is not constant but is determined by the trajectory of the sex ratio among carriers of that gene. This aspect of the modelled phenomenon cannot be revealed by the static analysis. Dynamics of the sex ratio among gene carriers is driven by a dynamic “tug of war” between female carriers expressing the encoded strategic trait value and random partners of male carriers expressing the average population strategy (a primary sex ratio). This mechanism can be called “double-level selection”. Therefore, gene interest perspective leads to multi-level selection.     

Negative Fitness Consequences and Transmission Dynamics of a Heritable Fungal Symbiont of a Parasitic Wasp

Heritable bacterial symbionts are widespread in insects and can have many important effects on host ecology and fitness. Fungal symbionts are also important in shaping their hosts'' behavior, interactions, and evolution, but they have been largely overlooked. Experimental tests to determine the relevance of fungal symbionts to their insect hosts are currently extremely rare, and to our knowledge, there have been no such tests for strictly predacious insects. We investigated the fitness consequences for a parasitic wasp (Comperia merceti) of an inherited fungal symbiont in the Saccharomycotina (Ascomycota) that was long presumed to be a mutualist. In comparisons of wasp lines with and without this symbiont, we found no evidence of mutualism. Instead, there were significant fitness costs to the wasps in the presence of the yeast; infected wasps attacked fewer hosts and had longer development times. We also examined the relative competitive abilities of the larval progeny of infected and uninfected mothers, as well as horizontal transmission of the fungal symbiont among larval wasps that shared a single host cockroach egg case. We found no difference in larval competitive ability when larvae whose infection status differed shared a single host. We did find high rates of horizontal transmission of the fungus, and we suggest that this transmission is likely responsible for the maintenance of this infection in wasp populations.The majority of heritable bacterial symbionts associated with insects either provide nutritional benefits for hosts that feed on nutrient-poor diets, such as blood (e.g., Wigglesworthia sp. [1]) or sap (e.g., Buchnera spp. [33]), or manipulate the hosts'' reproduction to benefit their own transmission (e.g., Wolbachia spp. [38] or Cardinium sp. [40]). Thanks in part to these examples, research efforts have become more diverse, leading to the discovery of additional benefits, such as heat tolerance (29) and protection from parasitism (26).Despite growing interest in the cryptic roles of insect associates, fungal symbionts have largely been overlooked, and their prevalence, ecological importance, and evolutionary implications for hosts are still poorly understood. Yet we have reason to suspect that fungal symbionts may be as diverse and functionally important as bacteria in insects. Buchner''s (5) foundational work on arthropod-microbe symbioses included many fungi, and anecdotal reports of such symbioses are scattered throughout the literature (e.g., fire ants [3]; stingless bees [28]; earwigs, scale insects, flies, andrenid bees, and ants [39]; and leafhoppers [30]). Recent surveys of insects for fungi have resulted in an astonishing diversity, including fungi in beetles (35), a cockroach and five other neuropteran families (24), sap-feeding beetles, and flies and bees (15), and it has been suggested that the majority of unicellular fungal diversity may be in insects (35). It is often suggested that such associations are mutualistic, with the fungus presumably providing enzymes, essential amino acids, vitamins, or sterols (37) and the insect vectoring and providing a habitat for the fungus. Fitness consequences of these associations have been assessed in only a few cases, including associations in planthoppers (31), anobiid beetles (23, 32), and scolytid beetles (2). In most instances the significance of the relationship is not clear, especially in the many cases where the fungi are not obligate associates.In 1985, LeBeck (18) reported a unicellular fungal symbiont in Comperia merceti (Compere) (Hymenoptera: Encyrtidae), a gregarious endoparasitoid wasp that specializes on the egg cases of brown-banded cockroaches [Supella longipalpa (Serville) (Blattaria: Blattellidae)]. The fungus is found throughout the hemocoel in juvenile wasps, in adult males, and in the venom gland of adult females (18). In addition, the fungus is vertically transmitted from mother to offspring via the external surface of wasp eggs during oviposition into cockroach egg cases. Vertical transmission via the egg surface is a common method in other fungal symbiont systems (e.g., planthoppers [19]; lacewings [10]; and wood wasps, anobiid beetles, and cerambycid beetles [5]). LeBeck (18) characterized the fungus as a Candida sp. and suggested that it might alter the nutritional value of the host cockroach egg case for the benefit of the developing wasp larvae. However, this claim has never been tested. Further, the predacious diet of immature parasitic wasps would make them unusual candidates for nutritional symbionts; parasitic wasps consume other insects and do not ordinarily require the complementary nutrients that many fungal and bacterial symbionts provide to insects with unbalanced diets. To our knowledge, our study is the first to specifically test the role of an inherited fungus in an insect with a strictly predacious diet.C. merceti wasps house a single known fungal symbiont belonging to the Ascomycota (Saccharomycotina) and no detectable bacterial symbionts (9). Further, these wasps do not become infected with any of their host cockroaches'' symbionts (9). In in vitro trials of the C. merceti wasp fungus with other microbes there was no evidence of inhibition or any type of interaction (C. M. Gibson, unpublished). The current research tests the hypothesis that the wasps'' fungal symbiont is a mutualist and explores alternative means by which this fungus could be maintained in wasp populations.     

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.     

No Evidence for a Second Evolutionary Stratum during the Early Evolution of Mammalian Sex Chromosomes

Mammalian sex chromosomes originated from a pair of autosomes, and homologous genes on the sex chromosomes (gametologs) differentiated through recombination arrest between the chromosomes. It was hypothesized that this differentiation in eutherians took place in a stepwise fashion and left a footprint on the X chromosome termed “evolutionary strata.” The evolutionary stratum hypothesis claims that strata 1 and 2 (which correspond to the first two steps of chromosomal differentiation) were generated in the stem lineage of Theria or before the divergence between eutherians and marsupials. However, this prediction relied solely on the molecular clock hypothesis between pairs of human gametologs, and molecular evolution of marsupial sex chromosomal genes has not yet been investigated. In this study, we analyzed the following 7 pairs of marsupial gametologs, together with their eutherian orthologs that reside in stratum 1 or 2: SOX3/SRY, RBMX/Y, RPS4X/Y, HSFX/Y, XKRX/Y, SMCX/Y (KDM5C/D, JARID1C/D), and UBE1X/Y (UBA1/UBA1Y). Phylogenetic analyses and estimated divergence time of these gametologs reveal that they all differentiated at the same time in the therian ancestor. We have also provided strong evidence for gene conversion that occurred in the 3′ region of the eutherian stratum 2 genes (SMCX/Y and UBE1X/Y). The results of the present study show that (1) there is no compelling evidence for the second stratum in the stem lineage of Theria; (2) gene conversion, which may have occurred between SMCX/Y and UBE1X/Y in the eutherian lineage, potentially accounts for their apparently lower degree of overall divergence.     

The Evolution of Sex Ratio Distorter Suppression Affects a 25 cM Genomic Region in the Butterfly Hypolimnas bolina

Symbionts that distort their host''s sex ratio by favouring the production and survival of females are common in arthropods. Their presence produces intense Fisherian selection to return the sex ratio to parity, typified by the rapid spread of host ‘suppressor’ loci that restore male survival/development. In this study, we investigated the genomic impact of a selective event of this kind in the butterfly Hypolimnas bolina. Through linkage mapping, we first identified a genomic region that was necessary for males to survive Wolbachia-induced male-killing. We then investigated the genomic impact of the rapid spread of suppression, which converted the Samoan population of this butterfly from a 100∶1 female-biased sex ratio in 2001 to a 1∶1 sex ratio by 2006. Models of this process revealed the potential for a chromosome-wide effect. To measure the impact of this episode of selection directly, the pattern of genetic variation before and after the spread of suppression was compared. Changes in allele frequencies were observed over a 25 cM region surrounding the suppressor locus, with a reduction in overall diversity observed at loci that co-segregate with the suppressor. These changes exceeded those expected from drift and occurred alongside the generation of linkage disequilibrium. The presence of novel allelic variants in 2006 suggests that the suppressor was likely to have been introduced via immigration rather than through de novo mutation. In addition, further sampling in 2010 indicated that many of the introduced variants were lost or had declined in frequency since 2006. We hypothesize that this loss may have resulted from a period of purifying selection, removing deleterious material that introgressed during the initial sweep. Our observations of the impact of suppression of sex ratio distorting activity reveal a very wide genomic imprint, reflecting its status as one of the strongest selective forces in nature.     

Patterns in Size,Sex Ratio and Time at Emergence in a South Swedish Population of Sympetrum sanguineum (Odonata)

Differences between sexes in life history patterns of Sympetrum sanguineum were studied in a small pond in southern Sweden by means of exuviae and adult sampling. Emergence occurred from 4 to 28 July, and mean emergence date was 10 July for both males and females. The sex ratio at emergence (53% females) did not differ from 1:1, but significantly more females emerged during the first 5 days of the emergence period. Size of emerging individuals (immatures) decreased as season progressed and males emerged at a larger size than females. While immature males were heavier than immature females, no such difference was found in mature individuals. We suggest that the sexual differences in size and emergence patterns observed are the result of different optimisation by males and females with respect to the growth-mortality risk trade-off in the larval and adult stages.     

Effects of Elevated Temperature on Sex Ratio in a Population of Hog Slaters (Asellus aquaticus L.)

Seasonal changes in the abundance and sex ratio in the hog slater were monitored in nature throughout the annual cycle. It was shown that the sex ratio was balanced at a relatively low abundance in the autumn-winter period. The number of males could exceed 1.5-fold that of females during the period of mass reproduction in spring and summer. The experimental results suggest that the summer shift of sex ratio towards males was due to their higher tolerance to elevated temperature at the early ontogenetic stages.