Partial local mate competition and the sex ratio: A study on non-pollinating fig wasps

In many species, mating takes place in temporary patches where only a small number of females produce offspring. In this situation Local Mate Competition (LMC) theory predicts that the optimal sex ratio (defined as proportion males) should become increasingly female biased as the number of females contributing offspring to a patch decreases. However, in a large number of these species, some mating is also likely to occur away from the natal patch (termed partial LMC). In this case the degree of LMC is reduced, and theory predicts a relatively less female biased sex ratio. We tested these two predictions with field data from 17 species of New World non-pollinating fig wasps representing three genera. We present a model which suggests that the average number of females ovipositing in a fruit (i.e. patch) is positively correlated with the proportion of fruit of a given tree species in which that species of wasp occurs. Across species, the overall sex ratio was positively correlated with the proportion of fruit in which that species occurs. Furthermore, the males of some species are wingless, and in these species all mating must take place before females disperse from their natal fruit. In contrast, the males of other species are winged, and in these species mating may also take place away from the natal fruit. Species with winged males had less female biased sex ratios than species with wingless males that occurred in a similar proportion of fruit. Finally, the correlation between sex ratio and the proportion of fruit in which a species occurs was also observed within species when comparing between the fruit crops of different trees. This suggests that individual females facultatively adjust the sex ratio of their offspring in response to variable LMC.     

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.     

Mating system and sex allocation in the gregarious parasitoid Cotesia glomerata

The gregarious parasitoid Cotesia glomerata (L.) is often presumed to possess the characteristic attributes of a species that manifests local mate competition (LMC), as it commonly produces female-biased broods. However, our field surveys of sex ratio and laboratory observations of adult behaviour showed that this species is subject to partial local mate competition caused by natal dispersal. On average, 30% of males left their natal patch before mating, with the proportion of dispersing males increasing with an increase in the patch's sex ratio (i.e. proportion of males). Over 50% of females left their natal patch before mating, and only 27.5% of females mated with males emerging from the same natal patch. Although females showed no preference between males that were and were not their siblings, broods from females that mated with siblings had a significantly higher mean brood sex ratio (0.56) than broods from females that mated with nonsiblings (0.39). Furthermore, brood sex ratios increased as inbreeding was intensified over four generations. A field population of this wasp had a mean brood sex ratio of 0.35 over 3 years, which conformed well to the evolutionarily stable strategy sex ratio (r=0.34) predicted by Taylor's partial sibmating model for haplodiploid species. These results suggest that the sex allocation strategy of C. glomerata is based on both partial local mate competition in males and inbreeding avoidance in females. In turn, this mating system plays a role in the evolution of natal dispersal behaviour in this species.Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

The proximate determinants of sex ratio in C. elegans populations

The soil nematode Caenorhabditis elegans is an example of a species in which self-fertilizing hermaphrodites predominate, but functional males continue to persist--allowing outcrossing to persevere at low levels. Hermaphrodites can produce male progeny as a consequence of sex chromosome non-disjunction or via outcrossing with males. Consequently, the genetics of sex determination coupled with the efficiency by which males find, inseminate and obtain fertilizations with hermaphrodites will influence the frequency at which males and outcrossing occurs in such populations. Behavioural and physiological traits with a heritable basis, as well as ecological characters, may influence male reproductive success and therefore sex ratio. Because sex ratio is tied to male reproductive success, sex ratio greatly affects outcrossing rates, patterns of genetic variation, and the ability of natural selection to act within populations. In this paper we explore the determinants of male frequency in C. elegans with a mathematical model and experimental data. We address the role of the genetic machinery of sex determination via sex chromosome non-disjunction on sex ratio and the influence of physiological components of C. elegans' life history that contribute to variation in sex ratio by way of male reproductive success. Finally, we discuss the short-term and long-term factors that are likely to affect sex ratio and breeding system evolution in species like C. elegans.     

When to estimate sex ratio in natural populations of insects? A study on sex ratio variations of gall midges within a generation

Precise estimation of arthropods' sex ratio is an important issue in a wide range of ecological studies and biological control programs. Although, in many cases changes in arthropods' sex ratio may be under the control of parents or some symbiotic microorganisms, biased sex ratios in some other species are caused by some extrinsic factors, neglect of which may lead to under/overestimation of true sex ratio. In this paper, we pursued those factors that cause false estimation of sex ratio in insects' species. We studied the predatory gall midge, Aphidoletes aphidimyza Rondani (Diptera: Cecidomyiidae), an important biological control agent of aphids, that shows protandry (i.e. early male emergence), differential lifespan of sexes, and differential distribution of sexes across habitat. Ten populations of A. aphidimyza were released separately in transparent cages and their sex ratio variations were recorded every 12 hours. The primary sex ratio in this species seems to be slightly male‐biased (52.41% males), however early emergence of males biases the sex ratio up to 72% males in a few hours after emergence. Shortly after the emergence of females, the sex ratio reaches its primary situation, but as a result of male‐biased mortality after mating, the proportion of females increases gradually to 97% by the fourth and fifth days after emergence. These results explicitly suggest that direct estimation of sex ratio in natural populations may be affected by some secondary factors such as differential mortality of sexes, protandry, and differential distribution of males and females over time and/or across habitat.     

Sexual dimorphism, extrapair fertilizations, and operational sex ratio in great frigatebirds (Fregata minor)

Across taxa, the presence of sexual ornaments in one sex isusually correlated with disproportionately great parental effortby the other. Frigatebirds (Fregatidae) are sexually dimorphic,with males exhibiting morphological and behavioral ornaments,but males and females share in all aspects of parental effort.All other taxa in a clade of 237 species exhibit biparentalcare, but only frigatebirds exhibit pronounced sexual dimorphism. We tested for the presence of two factors that could contributeto the evolution of male ornaments in great frigatebirds: ahigh frequency of extrapair fertilizations and a male-biasedoperational sex ratio. In 92 families sampled over two breedingseasons, there was only one extrapair fertilization. However,in both seasons, there were more males than females availablefor mating, and the sex ratio among individuals actively engagedin mate-acquisition behavior was strongly male biased, withtypically five or six males available per female. Our resultssuggest that extrapair fertilizations are not responsible forthe exaggeration of sexual ornaments in male frigatebirds,and that operational sex ratio may be related to sexual dimorphismin this species. Further work is needed to determine whetherthe male-biased operational sex ratio creates the variancein male reproductive success that would be needed to drivethe evolution of male ornaments.     

Different Sex Allocations in Two Related Species: The Case of the Extant Hippopotamus

Social and reproductive systems remain among the main predictors affecting mammalian birth sex ratio. The two extant hippopotamus species differ in their social and reproductive systems. While common hippopotamus (Hippopotamus amphibius) form herds and tend to be polygynous, solitary living pygmy hippopotamus (Choeropsis liberiensis) are promiscuous. Although it is one of the most studied topics, only few empirical studies using large sample sizes have reported distorted birth sex ratio. We examined the birth sex ratio in both hippopotamus species using international studbooks including large data sets exceeding a thousand individuals (1138 for common hippopotamus and 1161 for pygmy ones). In both species, the birth sex ratio differed from 1:1. Whereas more males than females were recorded in common hippopotamus (53.9% males), the opposite was found in pygmy hippopotamus (41.5% males). We also found that the birth sex ratio was affected by individual dams in common hippopotamus, and by individual sires in pygmy hippopotamus. The most plausible explanation for differentially skewed birth sex ratios in both species may be related to differences in social and reproductive systems. Whereas the polygynous, sexually dimorphic common hippopotamus biased the birth sex ratio towards males, the promiscuous and sexually monomorphic pygmy hippopotamus skewed the sex ratio in favour of females. Our results are in line with recent studies showing that not only manipulation by the mother (in common hippopotamus), but also by the father (in pygmy hippopotamus), may be responsible for the birth sex ratio in different species.     

Neither Biased Sex Ratio nor Spatial Segregation of the Sexes in the Subtropical Dioecious Tree Eurycorymbus cavaleriei (Sapindaceae)

Knowledge of sex ratio and spatial distribution of males and females of dioecious species is both of evolutionary interest and of crucial importance for biological conservation. Eurycorymbus cavaleriei, the only species in the genus Eurycorymbus (Saplndaceae), is a dioecious tree endemic to subtropical montane forest in South China. Sex ratios were investigated in 15 natural populations for the two defined ages (young and old). Spatial distribution of males and females was further studied in six large populations occurring in different habitats (fragmented and continuous). The study revealed a slight trend of malebiased sex ratio in both ages of E. cavaleriei, but sex ratio of most populations (13 out of 15) did not display statistically significant deviation from equality. All of the four significantly male-biased populations in the young class shifted to equality or even female-biased. The Ripley's K analysis of the distribution of males with respect to females suggested that individuals of the opposite sexes were more randomly distributed rather than spatially structured. These results suggest that the male-biased sex ratio in E. cavaleriei may result from the precocity of males and habitat heterogeneity. The sex ratio and the sex spatial distribution pattern are unlikely to constitute a serious threat to the survival of the species.     

Sex ratios and sex-biased infection behaviour in the entomopathogenic nematode genus Steinernema

In experimentally infected insects, the sex ratio of first generation nematodes of five species of Steinernema was female-biased (male proportion 0.35-0.47). There was a similar female bias when the worms developed in vitro (0.37-0.44), indicating that the bias in these species is not due to a lower rate of infection by male infective juveniles (IJs). Experimental conditions influenced the proportion of males establishing in insects, indicating that male and female IJs differ in their behaviour. However, there was no evidence that males are the colonising sex in any species, contrary to what has previously been proposed. Time of emergence from the host in which the nematodes had developed influenced sex ratios in experimental infections. In three species (Steinernema longicaudum, Steinernema glaseri and Steinernema kraussei), early emerged nematodes had a higher proportion of males than those that emerged later, with the reverse trend for Steinernema carpocapsae and Steinernema feltiae. In a more detailed in vitro study of S. longicaudum, the proportion of males was similar whether or not the nematodes passed through the developmentally arrested IJ stage, indicating that the female bias is not due to failure of males to exit this stage. The sex ratio in vitro was independent of survival rate from juvenile to adult, and was female-biased even when all juveniles developed, indicating that the bias is not explained by failure of males to develop to adults. The female-biased sex ratio characteristic of Steinernema populations appears to be present from at least the early juvenile stage. We hypothesise that the observed female bias is the population optimal sex ratio, a response to cycles of local mate competition experienced by nematodes reproducing within insect hosts interspersed with periods of outbreeding with less closely related worms following dispersal.     

Sex ratios observed in 80 species of parrots

A number of potential evolutionary and physiological factors may be involved in avian sex ratio bias so that under certain conditions a sex ratio bias may favour males or females within a population. In addition different factors may be important in manipulating sex ratio bias through the different life stages. In this study sex ratio bias was examined in a total of 16 570 captive parrots, representing 80 species, many of which are endangered in the wild, using database records originating form commercial laboratories that offer genetic sexing. Within the species examined 72% showed a male bias this was significant in three species, when adjusted for multiple comparisons. This preliminary study is limited due to lack of data on the age of the individuals sampled. However, the large dataset do suggest that this phenomenon should be further considered by investigators working at a species level where such data can be collected.     

Primary sex ratio adjustment to experimentally reduced male UV attractiveness in blue tits

The study of primary sex ratio adjustment in birds is notoriousfor inconsistency of results among studies. To develop our understandingof avian sex ratio variation, experiments that test a prioripredictions and the replication of previous studies are essential.We tested if female blue tits Parus caeruleus adjust the sexratio of their offspring to the sexual attractiveness of theirmates, as was suggested by a previous benchmark study on thesame species. In 2 years, we reduced the ultraviolet (UV) reflectanceof the crown feathers of males in the period before egg layingto decrease their attractiveness. In contrast to the simpleprediction from sex allocation theory, we found that the overallproportion of male offspring did not differ between broods ofUV-reduced and control-treated males. However, in 1 year, theUV treatment influenced offspring sex ratio depending on thenatural crown UV reflectance of males before the treatment.The last result confirms the pattern found in the previous bluetit study, which suggests that these complex patterns of primarysex ratio variation are repeatable in this bird species, warrantingfurther research into the adaptive value of blue tit sex ratioadjustment to male UV coloration.     

Heritable variation of sex ratio in a polychaete worm

Ophryotrocha labronica is a gonochoristic polychaete worm whose sex determining mechanism and sex ratio control are supposed to be polygenic. From a lab population, whose sex ratio (i.e., proportion of males) was 0.5, the estimate of sex ratio heritability by offspring-father regression was 0.54 ± 0.15 and by offspring-mother regression was not significantly different from 0. Estimate of sex ratio repeatability between successive broods of a pair was 0.64 ± 0.33. Since female parents do not contribute in any way to the variability of sex ratio, sex ratio variation seems to be largely a paternal character. On the basis of these estimates we advance the hypothesis that in this species sex is determined by a multilocus genetic system, allowing the combined effects of a female major sex gene (which could give rise to a form of female heterogamety) and masculinizing modifiers. The hypothesis that the male sex has the least canalised sexual differentiation is supported by the observation that some old males developed oocytes.     

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?     

Sex ratio of some long-lived dioecious plants in a sand dune area

In dioecious plants the fraction of males among flowering plants in the field (the secondary sex ratio) is the result of the fraction of males in the seeds (the primary sex ratio) and the subsequent survival and age at first reproduction of the two genders. It has been assumed that survival and age at first reproduction are the main determinants of biased secondary sex ratio but, especially for long-lived perennials, few data are available. We address this issue for natural populations of four long-lived perennials in a dune area. In Asparagus officinale and Bryonia dioica, the secondary sex ratio was unbiased. In Salix repens the secondary sex ratio was female-biased (0.337). Hippophae rhamnoides populations were male-biased; the average sex ratio of flowering plants was 0.658, while the fraction of males varied between 0.39 near the sea to 0.84 at the inland side of the dunes. The primary sex ratio was estimated by germinating seeds and growing plants under favourable conditions with minimal mortality. In S. repens the primary sex ratio in seeds was variable among mother plants and was, on average, female-biased (0.289). This is close to the secondary sex ratio, suggesting that the female bias already originates in the seed stage. In Hippophae rhamnoides the primary sex ratio was slightly male-biased (0.564). We argue that in this species, apart from the primary sex ratio, higher mortality and a later age at first reproduction for females contribute to the strong male bias among flowering plants in the field.     

Covariance of paternity and sex with laying order explains male bias in extra-pair offspring in a wild bird population

It has been hypothesized that parents increase their fitness by biasing the sex ratio of extra-pair offspring (EPO) towards males. Here, we report a male bias among EPO in a wild population of blue tits (Cyanistes caeruleus). This resulted from a decline in both the proportion of males and EPO over the laying order of eggs in the clutch. However, previous studies suggest that, unlike the decline in EPO with laying order, the relationship between offspring sex ratio and laying order is not consistent between years and populations in this species. Hence, we caution against treating the decline in proportion of males with laying order, and the resulting male bias among EPO, as support for the above hypothesis. Variable patterns of offspring sex and paternity over the laying order may explain inconsistent associations between offspring sex and paternity, between and within species.     

Mating ecology of the nonpollinating fig wasps of Ficus ingens

The males of many fig wasps fight fatally for mating opportunities. The concentration of females in space has been proposed as one factor selecting for their aggressive behaviour. We studied the temporal distribution of receptive females to obtain a clearer impression of the operational sex ratio in figs. Females of nonpollinating species emerged from figs over a protracted period of time and this resulted in an extremely male-biased operational sex ratio, conducive to extreme fighting. Since there were so few receptive females at any one time, a male could defend an eclosing female. Consequently, the largest, Otitesella longicauda male in a fig had a much higher mating success than smaller males. This suggests that larger males have a larger fitness advantage than larger females and a Trivers-Willard effect could have important implications for sex allocation. Apterous and seemingly nondispersing males routinely left their figs. Such dispersal can affect both (1) sex allocation by reducing the degree of local mate competition between brothers and (2) male dimorphism by reducing the mating opportunities of males with a dispersing morphology. We show that the wingless digitata males of the Otitesella digitata species group disperse on to leaves close to their natal fig. An extremely male-biased sex ratio resulted in almost all O. longicauda females being mated. These findings suggest that the classical concept of the fig wasp mating system is too simplistic and that important assumptions of sex allocation models are violated. Copyright 1999 The Association for the Study of Animal Behaviour.     

SEX RATIO VARIATION IN THE LESSONIA NIGRESCENS COMPLEX (LAMINARIALES,PHAEOPHYCEAE): EFFECT OF LATITUDE,TEMPERATURE, AND MARGINALITY1

Little is known about variation of sex ratio, the proportion of males to females, in natural populations of seaweed, though it is a major determinant of the mating system. The observation of sexual chromosomes in kelps suggested that sex is partly genetically determined. However, it is probably not purely genetic since the sex ratio can be modified by environmental factors such as salinity or temperature. In this paper, sex ratio variation was studied in the kelp Lessonia nigrescens Bory complex, recently identified as two cryptic species occurring along the Chilean coast: one located north and the other south of the biogeographic boundary at latitude 29°–30° S. The life cycle of L. nigrescens is characterized by an alternation of microscopic haploid gametophytic individuals and large macroscopic fronds of diploid sporophytes. The sex ratio was recorded in progenies from 241 sporophytic individuals collected from 13 populations distributed along the Chilean coast in order (i) to examine the effect of an environmental gradient coupled with latitude, and (ii) to compare marginal populations to central populations of the two species. In addition, we tested the hypothesis that the sex ratios of the two cryptic species would be affected differently by temperature. First, our results demonstrate that sex ratio seems to be mainly genetically determined and temperature can significantly modify it. Populations of the northern species showed a lower frequency of males at 14°C than at 10°C, whereas populations of the southern species showed the opposite pattern. Second, both species displayed an increased variation in sex ratio at the range limits. This greater variation at the margins could be due either to differential mortality between sexes or to geographic parthenogenesis (asexual reproduction).     

Contrasting patterns of X‐chromosome divergence underlie multiple sex‐ratio polymorphisms in stalk‐eyed flies

Sex‐linked segregation distorters cause offspring sex ratios to differ from equality. Theory predicts that such selfish alleles may either go to fixation and cause extinction, reach a stable polymorphism or initiate an evolutionary arms race with genetic modifiers. The extent to which a sex ratio distorter follows any of these trajectories in nature is poorly known. Here, we used X‐linked sequence and simple tandem repeat data for three sympatric species of stalk‐eyed flies (Teleopsis whitei and two cryptic species of T. dalmanni) to infer the evolution of distorting X chromosomes. By screening large numbers of field and recently laboratory‐bred flies, we found no evidence of males with strongly female‐biased sex ratio phenotypes (SR) in one species but high frequencies of SR males in the other two species. In the two species with SR males, we find contrasting patterns of X‐chromosome evolution. T. dalmanni‐1 shows chromosome‐wide differences between sex‐ratio (X^SR) and standard (X^ST) X chromosomes consistent with a relatively old sex‐ratio haplotype based on evidence including genetic divergence, an inversion polymorphism and reduced recombination among X^SR chromosomes relative to X^ST chromosomes. In contrast, we found no evidence of genetic divergence on the X between males with female‐biased and nonbiased sex ratios in T. whitei. Taken with previous studies that found evidence of genetic suppression of sex ratio distortion in this clade, our results illustrate that sex ratio modification in these flies is undergoing recurrent evolution with diverse genomic consequences.     

Color polymorphism and sex ratio distortion in a cichlid fish as an incipient stage in sympatric speciation by sexual selection

We investigated a Lake Victoria cichlid with a complex colour polymorphism that apparently represents one original species and two incipient species, all of which are sympatric. In laboratory breeding experiments we observed sex ratio distortion in certain matings between original and incipient species. Mate choice experiments show that males of the incipient species exhibit mating preferences against the original species, and males and females of the original species exhibit strong mating preferences against the incipient species. Mating preferences might evolve by sex ratio selection to avoid matings with distorted progeny sex ratios. Phenotype frequencies in nature suggest that mating preferences translate into mating frequencies, thus restricting gene flow and exerting disruptive sexual selection between the original and incipient species. The incipient species do not differ in morphology or ecology from the original species, implying that colour polymorphism, associated with sex ratio distortion, can be an incipient stage in sympatric speciation, and that disruption of gene flow can precede ecological differentiation.     

Reconstruction of paternal genotypes over multiple breeding seasons reveals male green turtles do not breed annually

For species of conservation concern, knowledge of key life-history and demographic components, such as the number and sex ratio of breeding adults, is essential for accurate assessments of population viability. Species with temperature-dependent sex determination can produce heavily biased primary sex ratios, and there is concern that adult sex ratios may be similarly skewed or will become so as a result of climate warming. Prediction and mitigation of such impacts are difficult when life-history information is lacking. In marine turtles, owing to the difficultly in observing males at sea, the breeding interval of males is unknown. It has been suggested that male breeding periodicity may be shorter than that of females, which could help to compensate for generally female-biased sex ratios. Here we outline how the use of molecular-based paternity analysis has allowed us, for the first time, to assess the breeding interval of male marine turtles across multiple breeding seasons. In our study rookery of green turtles (Chelonia mydas), 97% of males were assigned offspring in only one breeding season within the 3-year study period, strongly suggesting that male breeding intervals are frequently longer than 1year at this site. Our results also reveal a sex ratio of breeding adults of at least 1.3 males to each female. This study illustrates the utility of molecular-based parentage inference using reconstruction of parental genotypes as a method for monitoring the number and sex ratio of breeders in species where direct observations or capture are difficult.