Timing of foetal growth spurts can explain sex ratio variation in polygynous mammals

The prediction from sex ratio theory that natural selection on sexually dimorphic mammals should favour an excess of male offspring only when mothers are in good condition, has been tested extensively but with little consistency in results. Although recent studies have shown that environmental variations may cause some of the discrepancy, there have also been reports of contrasting sex ratios under similar environmental settings. Here it is suggested that variation in timing of environmental stress and sex-specific differences in foetal growth pattern in relation to maternal condition, may explain such seeming contradictions in sex ratio variation of polygynous mammals.     

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.     

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.     

Birth-sex ratios and local resource competition in roe deer, Capreolus capreolus

We investigated variation in the primary sex ratio within andbetween 14 populations of roe deer (Capreolus capreolus) inrelation to maternal body condition. The sex ratio was increasinglymale biased as average maternal body weight decreased. Thisrelationship did not vary according to the population consideredand was not affected by the litter size produced. This relationshipwas also apparent within populations. These results indicatethat, where environmental conditions are limiting, roe doestend to produce male-biased litters. Dispersal is more commonand occurs at an earlier age among male juveniles in this species,particularly as density increases and resources become increasinglyscarce. Thus, we suggest that where females experience environmentalstress, they tend to produce male kids to avoid potential futurelocal resource competition posed by female offspring. [BehavEcol 7: 461–464 (1996)]     

Female common lizards (Lacerta vivipara) do not adjust their sex-biased investment in relation to the adult sex ratio

Sex allocation theory predicts that facultative maternal investment in the rare sex should be favoured by natural selection when breeders experience predictable variation in adult sex ratios (ASRs). We found significant spatial and predictable interannual changes in local ASRs within a natural population of the common lizard where the mean ASR is female-biased, thus validating the key assumptions of adaptive sex ratio models. We tested for facultative maternal investment in the rare sex during and after an experimental perturbation of the ASR by creating populations with female-biased or male-biased ASR. Mothers did not adjust their clutch sex ratio during or after the ASR perturbation, but produced sons with a higher body condition in male-biased populations. However, this differential sex allocation did not result in growth or survival differences in offspring. Our results thus contradict the predictions of adaptive models and challenge the idea that facultative investment in the rare sex might be a mechanism regulating the population sex ratio.     

Adaptive biases in offspring sex ratios established before birth in a marsupial, the common brushtail possum Trichosurus vulpecula

Offspring sex ratios in the common brushtail possum are malebiased in many populations, and there is evidence that inter-populationdifferences in sex ratios represent adaptive responses to localconditions. However, how these biases are produced is not known.Using comparisons between populations with and without biasedoffspring sex ratios, we show that biases in this species arenot produced by sex-differential mortality between birth andweaning or sex-selective termination of pregnancy. Rather,adjustment in the sex ratio of offspring are evidently dueto shifts in the probability of conceiving male and femaleoffspring.     

Female ambrosia beetles adjust their offspring sex ratio according to outbreeding opportunities for their sons

Recent studies on the effect of local mate competition (LMC) on sex ratios have focused on the effect of post-dispersal mating success by males. A higher proportion of males is expected to be produced as the potential for outbreeding increases. Here we demonstrate that males of a haplodiploid ambrosia beetle with LMC disperse to seek additional matings, and brood sex ratios increase with outbreeding opportunities in the field. Manipulations in the laboratory confirm that females produce more sons when the post-dispersal mating prospects of their sons are experimentally increased. This is the first study showing that male dispersal options may influence individual female sex allocation decisions in species with strong LMC.     

Seed sex ratio in dioecious plants depends on relative dispersal of pollen and seeds: an example using a chessboard simulation model

Two principles are important for the optimal sex ratio strategy of plants. (1) Sib mating. Because seed dispersal is restricted, sib mating may occur which selects for a female bias in the seed sex ratio. (2) Local resource competition (LRC). If a plant produces pollen its nuclear genes are dispersed in two steps: first through the pollen and then, if the pollen is successful in fertilizing an ovule on another plant, through the seed. If the plant produces an ovule, its genes are dispersed only through the seed. By making pollen instead of ovules the offspring of a single plant is then spread out over a wider area. This reduces the chance that genetically related individuals are close together and need to compete for the same resource. The effect is the strongest if pollen is dispersed over a much wider area than seeds. Less LRC for paternally vs. maternally derived offspring selects for a male bias in sex allocation. We study the above‐mentioned opposite effects in dioecious plants (with separate male and female individuals), with maternal control over the sex ratio (fraction males) in the seeds. In a two‐dimensional spatial model female‐biased sex ratios are found when both pollen and seed dispersal are severely restricted. If pollen disperses over a wider area than seeds, which is probably the common situation in plants, the seed sex ratio becomes male‐biased. If pollen and seeds are both dispersed over a wide area, the sex ratio approaches 0.5. Our results do not change if the offspring of brother–sister matings are less fit because of inbreeding depression.     

Sex-specific sibling interactions and offspring fitness in vertebrates: patterns and implications for maternal sex ratios

Vertebrate sex ratios are notorious for their lack of fit to theoretical models, both with respect to the direction and the magnitude of the sex ratio adjustment. The reasons for this are likely to be linked to simplifying assumptions regarding vertebrate life histories. More specifically, if the sex ratio adjustment itself influences offspring fitness, due to sex-specific interactions among offspring, this could affect optimal sex ratios. A review of the literature suggests that sex-specific sibling interactions in vertebrates result from three major causes: (i) sex asymmetries in competitive ability, for example due to sexual dimorphism, (ii) sex-specific cooperation or helping, and (iii) sex asymmetries in non-competitive interactions, for example steroid leakage between fetuses. Incorporating sex-specific sibling interactions into a sex ratio model shows that they will affect maternal sex ratio strategies and, under some conditions, can repress other selection pressures for sex ratio adjustment. Furthermore, sex-specific interactions could also explain patterns of within-brood sex ratio (e.g. in relation to laying order). Failure to take sex-specific sibling interactions into account could partly explain the lack of sex ratio adjustment in accordance with theoretical expectations in vertebrates, and differences among taxa in sex-specific sibling interactions generate predictions for comparative and experimental studies.     

Effect of paternal age on the birth sex ratio in captive populations of aye‐aye (Daubentonia madagascariensis (Gmelin))

For the management of captive populations of zoo animals, it is important to elucidate factors that affect the offspring birth sex ratio. On the basis of the sex allocation theory, the Trivers–Willard and mate attractive/quality hypotheses predict that maternal and paternal conditions affect offspring birth sex ratios. We examined these predictions for the birth sex ratio of aye‐aye Daubentonia madagascariensis (Gmelin) by analyzing the pedigree information in the International Studbook. We found that the birth sex ratio of the aye‐aye was affected by the paternal age, but not maternal age and other environmental factors (birth year, season, and institution). The younger the sire, the more the offspring sex ratio was biased toward males. These results are useful for the effective population management of captive aye‐aye and illustrated the usefulness of the sex allocation theory in the sex ratio management of zoo animals.     

Patterns of sex ratio, virginity and developmental mortality in gregarious parasitoids

Theory considering sex ratio optima under ‘strict local mate competition with offspring groups produced by a single foundress’ makes a suite of predictions, one of which is a mean female bias. Treating individual offspring as discrete units, theory further predicts sex ratios to have low variance (precise sex ratio) and to equal the reciprocal of clutch size (one male per clutch). The maternal decision may be complicated by imperfect control of sex allocation, limited insemination capacity of sons and offspring developmental mortality: each can lead to virgin daughters (with zero fitness) and consequently select for less biased sex ratios. When clutches are small and/or developmental mortality is common, appreciable proportions of virgins are expected, even when control of sex allocation is perfect and the mating capacity of males is unlimited. This suite of predictions has been only partially tested. We provide further tests by examining sex ratios and developmental mortalities within and across species of locally mating parasitoids. We find a wide range of mean developmental mortalities (6–67%), but mortality distributions are consistendy overdispersed (have greater than binomial variance) and sexually differential mortality appears to be absent. Sex ratios are female biased and have low variance, but are not perfectly precise and variance is increased by mortality within species and (equivocally) across species. Sex ratios less biased than the reciprocal of clutch size are observed; probably due to a maternal response to developmental mortality in one species, and to limited insemination capacity in others. Cross species comparisons indicate that mean proportions of mortality and virginity are positively correlated. Virginity is more prevalent than predicted among species with higher mortalities but not among lower mortality species. Predicted relationships between virginity and clutch size are supported in species with lower mortalities but only partially supported when mortality rates are higher.     

Mating frequency, genetic structure, and sex ratio in the intermorphic female producing ant species Myrmecina nipponica

1. Myrmecina nipponica has two types of colonies: a queen colony type, in which the reproductive females are queens and new colonies are made by independent founding, and an intermorphic female colony type, in which reproductive females belong to a wingless intermediate morphology between queen and worker, and where colonies multiply through colonial budding. 2. The mating frequencies of reproductive females in both types indicate monoandry. The relatedness among nestmates in both types was almost 0.75, however relatedness between mother and daughter in intermorphic female colonies was slightly higher than that of queen colonies. 3. The sex ratio (corrected investment female ratio) was 0.70 at the population level, suggesting that the sex ratio is controlled by workers in this species, however the ratio differed greatly between the two types of colonies. Queen colonies (n = 37) had a female‐biased sex ratio of 0.77 while intermorphic female colonies (n = 33) had a ratio of 0.56. 4. Each reproductive intermorphic female was accompanied by an average of 2.9 workers (including virgin intermorphic females) in the colonial budding, and when the investment to those workers was added to the female investment, the sex ratio reached 0.81. 5. The frequency distribution of sex ratio was bimodal, with many colonies producing exclusively males or females, however mean estimated relatedness within colonies was almost 0.75. These data are inconsistent with the genetic variation hypothesis, which is one of the predominant hypotheses accounting for the between‐colony variation in sex ratio.     

Genetic diversity of captive binturongs (Arctictis binturong, Viverridae, Carnivora): implications for conservation

The binturong Arctictis binturong is a threatened carnivore (Mammalia) that ranges throughout the forests of South-east Asia. This study evaluates the genetic diversity of captive binturong populations in European zoos and attempts to assess their geographic origin. We sequenced the hypervariable region 1 of the mitochondrial control region of 56 binturongs, among which 20 had a known geographic origin. We showed that at least two distinct geographic clades exist and were able to assess the geographic clade to which captive individuals belong. Moreover, a low genetic diversity was observed among the captive population of European zoos. Although our results are preliminary, zoo managers should consider the evolutionary significant units identified by this study, and which correspond to recognized sub-species, when planning binturong reproduction programs.     

Dispersal and mating structure of a parasitoid with a female-biased sex ratio: Implications for theory

Summary Species of parasitic Hymenoptera that manifest female-biased sex ratios and whose offspring mate only with the offspring of the natal patch are assumed to have evolved biased sex ratios because of Local Mate Competition (LMC). Off-patch matings, i.e. outcrossing, are inconsistent with the conditions favouring biased sex ratios because they foster a mating structure approaching panmixia. Such a mating structure favours parents who invest equally in daughters and sons, assuming the production of each sex is of equal cost.Pachycrepoideus vindemiae (Rondani) is a solitary pupal parasitoid of patchily distributed frugivorousDrosophila, whose offspring manifest a female-biased sex ratio. Thus this species appears to manifest a population structure and progeny sex ratio consistent with LMC. However, preliminary observations and subsequent greenhouse experiments suggest that the males participate in off-patch matings and that this propensity is unlikely to be an experimental artefact. FemaleP. vindemiae dispersed from patches in which either the males were lacking (12% of the emigrant females), both resident (sibling) and immigrant males were present (23% of the females), only immigrant males were present (14% of the females), or their opportunity to mate could not be determined (14% of the females). Of the 12% that emigrated from a patch lacking males, an estimated 7% mated at an oviposition site and 5% remained unmated, presumably because they arrived at an oviposition site that lacked males before they were dissected to determine whether they were inseminated. Thus the degree of bias in the sex ratios of the progeny (18% males), coupled with the suggested outcrossing potential from the experiments (26–37%), is inconsistent with the assumptions of LMC or variants of it, i.e. asynchronous brood maturation. Thus the explanation for a biased sex ratio in the offspring ofP. vindemiae remains a conundrum. More importantly,P. vindemiae does not appear to be an isolated example.     

The Shape of the Female Fitness Curve for Cynoglossum officinale: Quantifying Seed Dispersal and Seedling Survival in the Field

Abstract: When hermaphroditic plants shift their sex allocation to produce more seeds and less pollen, it is frequently assumed that the female component of fitness is strictly proportional to the number of seeds produced. However, if producing more seeds results in more competition between seedlings, the female fitness gain curve levels off with high investments in seeds. The shape of this curve is relevant for sex allocation theory, but rarely have data been collected. For Cynoglossum officinale we described the relationship between the number of seeds produced on the mother plant and the number and weight of seedlings in September of the following year. As expected, around large plants of C. officinale more seedlings were retrieved after the germination period in March. The seedlings of large plants were dispersed over an area similar to that of small plants. As a result, seedlings around large plants had a significantly higher chance to have a neighbouring sibling within one dm². Survival and growth of single or grouped (density > 2) seedlings did not differ significantly. As a result, total dry weight of seedlings in September was a linear function of the number of seeds on the parent plant. Our data indicate a linear female fitness gain curve.     

More highly female-biased sex ratio in the fig wasp,Blastophaga nipponica Grandi (Agaonidae)

The sex ratio of the pollinator fig wasp,Blastophaga nipponica Grandi (Agaonidae), was examined in an experiment manipulating the number of foundresses. The sex ratio ofB. nipponica was conditional on the number of foundresses and corresponded to the qualitative prediction of the local mate competition (LMC) theory that the proportion of males increases as foundress number increases. However, the sex ratio ofB. nipponica was consistently more female-biased than predicted by extended LMC theories that incorporated effects of inbreeding, and these deviations were statistically significant. Plausible factors that would make predictions more female-biased are discussed.     

Experimental manipulation of maternal effort produces differential effects in sons and daughters: implications for adaptive sex ratios in the blue-footed booby

Sex allocation theory predicts that mothers in good conditionshould bias their brood sex ratio in response to the differentialbenefits obtained from increased maternal expenditure in sonsand daughters. Although there is well-documented variationof offspring sex ratios in several bird species according tomaternal condition, the assumption that maternal condition has different fitness consequences for male and for female offspringremains unclear. The blue-footed booby (Sula nebouxii) is asexually size-dimorphic seabird, with females approximately31% heavier than males. It has been reported that the sex ratiois male biased in years with poor feeding conditions, whichsuggests that either females adjust their sex ratio in accordancewith their condition or that they suffer differential brood mortality before their sex can be determined. In this studyI tested whether the condition of mothers affected their daughters'fitness more than their sons' fitness. I manipulated maternalinvestment by trimming the flight feathers and thereby handicappingfemales during the chick-rearing period. Adult females in thehandicapped group had a poorer physical condition at end ofchick growth, as measured by mass and by the residuals of masson wing length compared to control birds. Female chicks wereaffected by the handicapping experiment, showing a lower massand shorter wing length (reduced approximately 8% in both measures)than controls. However, this effect was not found in male chicks.Hatching sex ratios were also related to female body conditionat hatching. The brood sex ratio of females in poor conditionwas male biased but was female biased for females in good condition.Overall, these results suggest that the variation in the sexratio in blue-footed boobies is an adaptive response to thedisadvantage daughters face from being reared under poor conditions.