The genetics of sex ratio distortion by cytoplasmic infection under maternal and contagious transmission: An epidemiological study

Nuclear and cytoplasmic determinants jointly influence the sex ratio in several organisms. A mathematical model of a maternally inherited extra-chromosomal agent that affects the fitness of its carriers and distorts the sex ratio in their broods is analyzed. The agent is transmitted through the cytoplasm from mother to daughter, or it may pass contagiously among females of the same generation. It is shown that under natural selection the deviation between the population sex ratio and Fisher's optimum value evolves to a minimum.     

Factors influencing brood sex ratios in polyembryonic Hymenoptera

Copidosoma sp. is a polyembryonic encyrtid wasp which parasitizes isolated hosts. Most broods of this wasp are unisexual, but some contain both sexes and the secondary sex ratio of these is usually highly female biased. The overall population secondary sex ratio is female biased. Walter and Clarke (1992) argue that because the majority of individuals must mate outside the natal patch, the bias in the population secondary sex ratio contradicts predictions made by Hamilton's (1967) theory of local mate competition (LMC). We suggest that the primary sex ratio is unbiased and that Walter and Clarke's results do not cast doubt on LMC. Instead these results imply that ovipositing females make a combined clutch size and sex ratio decision influencing whether individuals developing from a particular brood will outbreed or largely inbreed; for each case the predictions of LMC theory are not violated. If this interpretation is correct, what is of interest is the basis on which this decision is made rather than the population secondary sex ratio. We show that host encounter rate influences the proportions of mixed and single sex broods laid by Copidosoma floridanum, a related polyembryonic parasitoid. Among single-sex broods the primary sex ratio is female biased, but our results are in agreement with LMC theory since offspring developing from these broods will probably mate with siblings from adjacent hosts. We consider the egg load of females to be of major influence on oviposition behaviour, and that the mating structure of parasitoid offspring, potentially differential costs of male and female broods and the natural distributions of hosts both at oviposition and eclosion, require further study.     

A polymorphic effect of sexually differential production costs when one parent controls the sex ratio.

R. A. Fisher's sex ratio theory predicts that if sons and daughters cost fixed amounts of resources to raise and parents have fixed amounts to invest, then the numerical sex ratio of a panmictic population will evolve to be inversely proportional to relative cost. However, the theory assumes control by both parents. We show that allowing one parent to control the sex ratio biases it further from parity than Fisher's theory predicts. Quantitatively, the additional bias towards the cheaper sex depends only very weakly on which sex is in control. Qualitatively, however, the effect is very strong: a monomorphic, mixed-brood strategy evolves only if the more expensive sex is in control. If the controlling sex is cheaper to raise, then the sex ratio is instead achieved through a polymorphism of single-sex broods. Such polymorphisms are seldom observed in nature, generating the prediction that wherever the sexes are not equally costly, sex ratio is usually either under biparental control or under uniparental control by the more expensive sex. However, such polymorphisms do occur, and some of them may be explained by our model.     

Maternal-offspring conflict leads to the evolution of dominant zygotic sex determination

Sex determination in many species involves interactions among maternally expressed genes (eg, mRNA's and proteins placed into the egg) and zygotically expressed genes. Recent studies have proposed that conflicting selective pressures can occur between maternally and zygotically expressed sex determining loci and that these may play a role in shaping the evolution of sex determining systems. Here we show that such genetic conflict occurs under very general circumstances. Whenever sex ratio among progeny in a family affects the fitness of either progeny in that family or maternal fitness, then maternal-zygotic genetic conflict occurs. Furthermore, we show that this conflict typically results in a "positive feedback loop" that leads to the evolution of a dominant zygotic sex determining locus. When males more negatively effect fitness within the family, a male heterogametic (XY male) sex determining system evolves, whereas when females more negatively effect fitness in the family, a female heterogametic (ZW female) system evolves. Individuals with the dominant sex allele are one sex, and the opposite sex is determined by maternally-expressed genes in individuals without the dominant sex allele. Results therefore suggest that maternal-zygotic conflict could play a role in the early evolution of chromosomal sex determining systems. Predictions are made concerning the patterns of expression of maternal and zygotic sex determining genes expected to result from conflict over sex determination.     

Sex ratio and fledging success of supplementary-fed Tengmalm's owl broods

A nest box population of Tengmalm's owls (Aegolius funereus) in northern Sweden was studied to investigate the effects of extra food on the sex ratio between hatching and fledging in this sexually size-dimorphic species. The brood size and brood sex ratio of supplementary-fed and control broods were compared. Newly hatched nestlings were blood sampled and sexed by polymerase chain reaction (PCR) amplification of the sex-linked CHD1Z and CHD1W genes. The brood sex ratio at hatching was strongly male biased (65%); this was also the case in broods where all eggs hatched (72%). There was no relationship between hatch order and sex ratio, and hatching sex ratio did not vary significantly with laying date. Brood size decreased between hatching and fledging, but did not differ between fed and control broods at either stage. Brood sex ratio did not differ between hatching and fledging, and fledging sex ratio did not differ between fed and control broods. It was concluded that, at least during the year in which the study was carried out, feeding had no effect on brood reduction, and that male and female nestlings did not show any differential mortality. The mechanisms behind the male-biased sex ratio at hatching, and any possible adaptive reasons for it, are not known.     

Sex allocation in the sexually monomorphic fairy martin

Offspring sex ratios were examined at the population and family level in the sexually monomorphic, socially monogamous fairy martin Petrochelidon ariel at five colony sites over a 4-year period (1993–1996). The sex of 465 nestlings from 169 broods was determined using sex-specific PCR at the CHD locus. In accordance with predicted sex allocation patterns, population sex ratios at hatching and fledging did not differ from parity in any year and the variance in brood sex ratios did not deviate from the binomial distribution. Further, brood sex ratio did not vary with hatching date during the season, brood number, brood size or colony size. The sex ratio of broods with extra-pair young did not differ from those without, while the sex ratio of broods fathered by males that gained extra-pair fertilizations did not differ from broods fathered by other males. Extra-pair chicks were as likely to be male as female. Neither the total number of feeding visits to the brood nor the relative feeding contribution by the sexes varied significantly with brood sex ratio. Brood sex ratios were also unrelated to paternal size, condition and breeding experience or maternal condition and breeding experience. However, contrary to our prediction, brood sex ratio was negatively correlated with maternal size. Generally, these results were consistent with our expectations that brood sex ratios would not vary with environmental factors or parental characteristics, and would not influence the level of parental provisioning. However, the finding that females with longer tarsi produced an excess of daughters is difficult to reconcile with our current understanding of fairy martin life history and breeding ecology.     

Sex-biased mortality in the Lesser Black-backed Gull Larus fuscus during the nestling stage

Theory predicts that skewed progeny sex ratios should be relatively common in vertebrate populations. In most birds this has proved hard to substantiate due to the difficulties associated with identifying the sex of large samples of chicks. This study reports the success of a new molecular DNA technique in determining the sex of 601 newly-hatched Lesser Black-backed Gulls Larus fuscus
There was no evidence of any adaptive sex ratio within broods. Male chicks were found to be disproportionately large and to grow at a faster rate than females. The overall sex ratio changed significantly from 0.484 (male/male + female) at hatching to 0.399 by fledging, probably due to male susceptibility to starvation. Mortality also increased significantly with hatching order, an effect often observed in species like the Lesser Black-backed Gull where hatching is asynchronous. I discuss the possibility that hatching asynchrony may in fact be a strategy employed to prevent excessive skews developing in progeny sex ratio whenever variable differential mortality is likely.
The results appear to vindicate Fisher's (1930) hypothesis which predicts the overproduction of the 'cheaper' sex. However, as the skewed sex ratio may be determined more by unpredictable environmental factors, such as food supply and weather conditions rather than parental strategy, this interpretation should be treated with caution.     

Sexual selection favors female-biased sex ratios: the balance between the opposing forces of sex-ratio selection and sexual selection

In a verbal model, Trivers and Willard proposed that, whenever there is sexual selection among males, natural selection should favor mothers that produce sons when in good condition but daughters when in poor condition. The predictions of this model have been the subject of recent debate. We present an explicit population genetic model for the evolution of a maternal-effect gene that biases offspring sex ratio. We show that, like local mate competition, sexual selection favors female-biased sex ratios whenever maternal condition affects the reproductive competitive ability of sons. However, Fisherian sex-ratio selection, which favors a balanced sex ratio, is an opposing force. We show that the evolution of maternal sex-ratio biasing by these opposing selection forces requires a positive covariance across environments between the sex-ratio bias toward sons (b) and the mating success of sons (r). This covariance alone is not a sufficient condition for the evolution of maternal sex-ratio biasing; it must be sufficiently positive to outweigh the opposing sex-ratio selection. To identify the necessary and sufficient conditions, we partition total evolutionary change into three components: (1) maternal sex-ratio bias, (2) sexual selection on sons, and (3) sex-ratio selection. Because the magnitude of the first component asymmetrically affects the strength of the second, biasing broods toward females in a poor environment evolves faster than the same degree of bias toward males in a good environment. Consequently, female-biased sex ratios, rather than male-biased sex ratios, are more likely to evolve. We discuss our findings in the context of the primary sex-ratio biases observed in strongly sexually selected species and indicate how this perspective can assist the experimental study of sex ratio evolution.     

Offspring sex ratio variation in relation to brood size and mortality in a promiscuous species: the Aquatic Warbler Acrocephalus paludicola

We analyse nestling sex ratio variation in the Aquatic Warbler Acrocephalus paludicola to test for predictions from sex allocation theory that the brood sex ratio is close to parity. We also tested Fiala's (1980) prediction that there is no difference in sex ratio between broods affected and not affected by mortality, and whether a shift in primary sex ratios or simple differential mortality by sex underlies that difference. Furthermore, we explore additional analytical possibilities for inferring proximate mechanisms through simulation modelling. In the Aquatic Warbler, which is promiscuous, the overall sex ratio determined by molecular sexing of nestlings at 8–11 days of age did not deviate significantly from parity (proportion of females 0.509), nor did we find any predictive effect of brood size, maternal body mass, fat condition, wing and bill length, laying date, mean daily temperature, and multiple-male mating. However, extensive simulation suggested that the whole pattern of sex ratio variation is unlikely to arise purely by chance: (1) there is a diverging sex ratio between complete and partial broods, (2) large broods tended to be female-biased and small broods male-biased, and (3) low ambient temperature prior to the laying period seemed to increase the proportion of female offspring in complete broods. We conclude that most variation in nestling sex ratio is non-adaptive in nature, and results from variation in female nestlings mortality dependent on brood size and sex ratio.     

Pair bond duration influences paternal provisioning and the primary sex ratio of brown thornbill broods

Parents should vary their level of investment in sons and daughters in response to the fitness costs and benefits accrued through male and female offspring. I investigated brood sex ratio biases and parental provisioning behaviour in the brown thornbill, Acanthiza pusilla, a sexually dimorphic Australian passserine. Parents delivered more food to male-biased than female-biased broods. However, factors determining parental provisioning rates differed between the sexes. Female provisioning rates were related to brood sex ratio in both natural and experimental broods with manipulated sex ratios. In contrast, male provisioning rates were not affected by brood sex ratio in either natural or experimental broods. However, males in established pairs provisioned at a higher rate than males in new pairs. Data on the sex ratio of 109 broods suggest that female brown thornbills adjust their primary sex ratio in response to pair bond duration. Females in new pairs produced broods with significantly fewer sons than females in established pairs. This pattern would be beneficial to females if the costs of rearing sons were higher for females in new than established pairs. This may be the case since females in new pairs provisioned experimental all-male broods at elevated rates. The condition of nestlings also tended to decline more in these all-male broods than in other experimental broods. This will have additional fitness consequences because nestling mass influences recruitment in thornbills. Female thornbills may therefore obtain significant fitness benefits from adjusting their brood sex ratio in response to the status of their pair bond. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

The evolution of unusual chromosomal systems in sciarid flies: intragenomic conflict and the sex ratio

A model is presented for the evolution of the sciarid chromosomal system. In this model, a driving X chromosome caused female-biased sex ratios. The drive was exploited by maternal autosomes that segregated with the X at spermatogenesis. Genes in mothers converted some of their XX daughters into sons by eliminating a paternal X from the embryonic soma. L chromosomes were derived from X chromosomes and favored male-biased sex ratios. An X' chromosome arose that suppressed the effects of L chromosomes. The 1:1 sex ratio is a stalemate between the X' and X'X mothers causing all-female broods and the L chromosomes in XX mothers causing all-male broods. Any element (such as an L chromosome) that is preferentially transmitted through one sex will be selected to bias the sex ratio towards this sex.     

The evolution of paternal care with overlapping broods

Most attempts to model the evolution of parental care assume that caring and mating are mutually exclusive activities (i.e., individuals acquire and guard broods "sequentially"). However, in most fish and certain insects, males can keep mating and collecting additional eggs while continuing to guard broods obtained earlier (i.e., males guard "overlapping" broods). We present a model of parental care with overlapping broods in which males can mate and guard simultaneously, even though there is a trade-off between these two activities. Within this framework, we show that male care is favored by short female processing times and high population densities, which minimize the mating cost of care. Relatively low mortality while guarding is also important for the stability of male care. Female care, on the other hand, is favored by long female processing times and low populations densities, which lead to longer intermating intervals. Biparental care is stable only when the cost to benefit ratio of care was not biased toward either sex. We derive quantitative estimates of fitness for different strategies for two species of assassin bugs with male and female uniparental care and show that the model predicts the correct form of care for both species. We believe our model might help explain the prevalence of male uniparental care in certain taxa, such as fish.     

Sex ratio variation in Iberian pigs

Within the area of sex allocation, one of the topics that has attracted a lot of attention is the sex ratio problem. Fisher (1930) proposed that equal numbers of males and females have been promoted by natural selection and it has an adaptive significance. But the empirical success of Fisher's theory remains doubtful because a sex ratio of 0.50 is also expected from the chromosomal mechanism of sex determination. Another way of approaching the subject is to consider that Fisher's argument relies on the underlying assumption that offspring inherit their parent's tendency in biased sex ratio and therefore that genetic variance for this trait exists. Here, we analyzed sex ratio data of 56,807 piglets coming from 550 boars and 1893 dams. In addition to classical analysis of heterogeneity we performed analyses fitting linear and threshold animal models in a Bayesian framework using Gibbs sampling techniques. The marginal posterior mean of heritability was 2.63 x 10(-4) under the sire linear model and 9.17 x 10(-4) under the sire threshold model. The probability of the hypothesis p(h(2) = 0) fitting the last model was 0.996. Also, we did not detect any trend in sex ratio related to maternal age. From an evolutionary point of view, the chromosomal sex determination acts as a constraint that precludes control of offspring sex ratio in vertebrates and it should be included in the general theory of sex allocation. From a practical view that means that the sex ratio in domestic species is hardly susceptible to modification by artificial selection.     

Spiderling sex ratio and maternal investment in the bolas spider Mastophora cornigera (Araneae,Araneidae)

Male Mastophora cornigera exit egg sacs as adults, which allowed us to determine spiderling sex ratios and patterns of maternal investment in this species. We collected 15 egg sacs produced by seven mothers, which yielded 1945 emergent spiderlings which were sexed, 1850 of which were weighed. Two emergent broods were significantly male and female biased and were unaffected by pre-emergence mortality. The weights of male and female spiderlings differed in eight broods, with males and females being heavier in four cases each. Five of these broods were derived from multiple egg sac sets produced by one mother, and in each case, the total mean male and female spiderling weights for all broods in a set were biased in the same direction as the biased brood(s) within that set. Mean emergent spiderling weight was independent of brood size and sex ratio for both males and females. Despite such independence, sex allocation in M. cornigera can favor sons, daughters, or both equally, and by numbers, by weight, or both at once. The proximate mechanisms and adaptive significance of such variability is unknown. We also review evidence for gender-biased allocations in arachnid offspring and suggested mechanisms for their applicability to M. cornigera.     

Maternal adjustment of the sex ratio in broods of the broad-horned flour beetle, Gnathocerus cornutus

We report that females of the broad-horned flour beetle, Gnathocerus cornutus, can plastically adjust the sex ratio in their broods in response to environmental quality. Specifically, females reared in nutritionally poor environments produce broods that are 65% female, on average, with the degree of female-bias in some broods approaching 95%. In addition, females reared in nutritionally poor environments lay significantly more eggs than do females reared on standard medium, which produce broods with an even sex ratio. These effects of the mother's environment on size and sex ratio in broods are manifest even when oviposition occurs in the standard nutritional environment; indeed, the degree of female-bias increases with advancing female age despite the availability of nutritional resources to females at the time of egg laying. Our studies rule out sex-specific differences in viability early in larval development as the mechanism for the bias in sex-ratio of broods, since females reared in nutritionally poor environments have broods with hatchability and larval viability comparable to those of nonstressed females. Our studies also rule out an effect of the sire on the sex ratio in broods, since all male mates were reared on standard medium. We discuss our results in the context of theories for the evolution of plastic sex-ratios in the face of environmental deterioration and discuss how plasticity can resolve a long-standing question about the conditions underlying the evolution of biased sex ratios.     

Queen–worker conflict can drive the evolution of social polymorphism and split sex ratios in facultatively eusocial life cycles*

Hamilton's idea that haplodiploidy favors the evolution of altruism—the haplodiploidy hypothesis—relies on the relatedness asymmetry between the sexes caused by the sex-specific ploidies. Theoretical work on the consequences of relatedness asymmetries has significantly improved our understanding of sex allocation and intracolony conflicts, but the importance of haplodiploidy for the evolution of altruism came to be seen as minor. However, recently it was shown that haplodiploidy can strongly favor the evolution of eusociality, provided additional “preadaptations” are also present, such as the production of multiple broods per season and maternal ability to bias offspring sex ratios. These results were obtained assuming no influence of workers on the sex ratio, even though worker control of the sex ratio is known to occur. Here, we model the evolution of sex-specific fratricide as a mechanism of worker control over the sex ratio. We show that fratricide can facilitate the initial evolution of helping. However, fratricide can also hamper the evolution of unconditional help. Instead, social polymorphism evolves a mixture of helping and dispersing offspring. Finally, we show that the co-evolution of sex-allocation strategies of workers (fratricide) and queens leads to a split production of the sexes, with some colonies specializing in males and others in females. Thus, the model predicts that fratricide spawns a diversity of co-existing life cycles that strongly vary in degree of sociality and sex ratios.     

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.      

Fledgling sex ratios in relation to brood size in size-dimorphic altricial birds

In six species of dimorphic raptors (females larger than males)and one passerine (males larger than females), the sex ratioat fledging varied systematically with brood size at fledging.In all species the strongest bias toward the smaller sex wasestablished in the largest as well as the smallest broods; amore even distribution of males and females was observed inbroods of intermediate size. We explored a specific differentialmortality explanation for this sex ratio variation. Our hypothesispostulates that variation in mortality is caused by differencesin food demand between broods of the same size, due to theirsex composition. Data from the marsh harrier Circus aeruginosuson gender-related food demand and overall nestling mortalitywere used to predict the frequency of surviving males and femalesat fledging, assuming an even sex ratio at hatching and randommortality with respect to both sexes within broods. The modelquantitatively fits the marsh harrier data well, especiallyin broods originating from large dutches. Although we anticipatethat other mechanisms are also involved, the results supportthe hypothesis of sex-ratio-dependent mortality, differentialbetween broods, as the process generating the observed brood-sizedependence of fledgling sex ratios in sexually dimorphic birds.     

Secondary sex ratio covaries with demographic trends and ecological conditions in the barn swallow

Parents are expected to invest more in the sex that benefits most from the local environment. When the quality of breeding sites varies spatially and natal dispersal of males and females differs, parents in high-quality habitats should skew their progeny sex ratio in favor of the less dispersing sex. We tested this prediction in the barn swallow (Hirundo rustica L.), by relating the proportion of male offspring around fledging (secondary sex ratio) of first and second broods to the ecological quality (presence of livestock farming and relative surface of hayfields in the foraging range) and local demographic trends of the farms where the colonies were located. Consistent with our predictions, the proportion of male offspring, which are more philopatric than females, increased with the extent of hayfields, which are high quality, preferred foraging habitats. Moreover, the proportion of male offspring in second broods was smaller in colonies with positive demographic trends, possibly indicating density-dependent effects on sex ratio. Independent of the mechanism generating uneven sex ratio (zygote sex ratio adjustment or sex-related pre-fledging mortality), barn swallows breeding under favorable conditions overproduced the sex that is more likely to benefit from such conditions.     

Sex ratio in relation to timing of breeding, and laying sequence in a dimorphic seabird

When the cost of rearing sons and daughters differs and the subsequent survival and reproductive success of one sex is more dependent than the other, on the amount of parental investment, adult females tend to produce more chicks of the more dependent sex if the females are in good condition themselves. One method of varying the total investment in each sex is through modifying the sex ratio of offspring produced. This study shows that in broods of European Shags Phalacrocorax aristotelis , the sex ratio varied with laying date. Presumably in this species, the lifetime reproductive success of males is more dependent on the level of parental investment. Early breeders are in better condition, the brood sex ratio of early broods was male biased (0.63), while that of late broods was female biased (0.36). The overall difference in sex ratio found between early and late nests could be attributed to manipulation of sex in the first laid egg. In early broods, 77% of the first hatched chicks were male but only 30% of the first hatched chicks in late broods were male. The sex combination of the first two chicks in a brood significantly affected growth as measured by asymptotic mass.