Clutch Sex Ratio Research Articles

Exploring contaminants as a disruptor of temperature-dependent sex determination in sea turtle hatchlings

Sea turtle nesting beaches are experiencing increased sand temperatures as climate change progresses. In one major green turtle (Chelonia mydas) nesting beach in the northern Great Barrier Reef, over 99 percent of hatchlings are female. The effects of contaminants on sea turtle hatchling sex determination are not often explored. Liver samples were collected from green turtle hatchlings that were sacrificed for histological sex determination in a parallel study on the effects of sand cooling on sex ratios, and analysed for trace elements via acid digestion and organic contaminants via in vitro cytotoxicity bioassays. Chromium, antimony, barium, and cadmium have previously been demonstrated to be estrogenic, and concentrations of these elements were used to calculate three estrogenic indexes for each clutch: predicted relative estrogenic potency (PEEQA), the sum of percent trace elements above the median of all samples (TEOM), and the sum of percent estrogenic elements above the median of all samples (EstroEOM). Excluding an outlier clutch, cadmium, antimony, and EstroEOM had significant positive relationships with sex ratio deviation. Mean clutch cobalt, lead, antimony and barium, also had a significant positive relationship with clutch sex ratio. There was no relationship between in vitro cytotoxicity of liver extracts and sex ratio, however, 9% of hatchlings had organic contaminants high enough to suggest potential cellular damage. Contaminant effects on sex determination are likely to be caused by a mixture of contaminant interactions as well as temperature. Many trace elements detected in this study have also been linked to negative health effects on hatchlings in previous studies. Considering the risks of feminization due to climate change and potential contaminant effects on hatchling health and sex determination, future studies exploring contaminant effects on sea turtle hatchling sex determination are recommended.

Among us: How to find an optimal clutch sex ratio when the clutch sex ratios of co-foundress wasps are not known beforehand?

A female-biased clutch sex ratio is selected under local mate competition since it reduces competition between male sibs and provides extra mating opportunities for sons. Theoretical models predict that the brood sex ratio of fig wasps becomes less female-biased as the number of wasps laying eggs in the same fig increases. Empirical data have demonstrated that pollinator females lay most of their male eggs first, followed by the female ones in an oviposition bout (males first rule). As oviposition sites are limited in the fig, the brood sex ratio is positively correlated with the number of wasps laying eggs. To understand the strategy of sex ratio adjustment of Sycobia hodites, a non-pollinating fig wasp associated with Ficus benjamina, we compared observed and simulated data. The female wasp starts oviposition shortly after landing on the fig. This process involves the insertion of the ovipositor through the fig surface and into the flower's ovary via the stigma/style. The brood sex ratio of S. hodites did not significantly correlate with the fig brood size. Brood simulations supported the notion that the sex ratio of S. hodites is automatically determined by the male-first rule, involving no control by the mothers. The simulation model best fitting empirical data considered that: (1) females lay few eggs per fig (six or less) and distribute their eggs among several figs, and (2) the probability of an egg producing a male wasp decreases with its position in the egg sequence. Empirical and simulated data showed a wide variation in both brood size and sex ratio, suggesting that selection for an optimal clutch sex ratio is possibly weak. We argue that when selective pressure for sex ratio adjustment is weak, evolution favors male polymorphism as a strategy to cope with mate competition.

Sex ratio varies with egg investment in the red-necked phalarope (Phalaropus lobatus)

Fisher’s sex ratio theory predicts that on average parents should allocate resources equally to the production of males and females. However, when the cost/benefit ratio for producing males versus females differs, the theory predicts that parents may bias production, typically through underproduction of the sex with greater variation in fitness. We tested theoretical predictions in the red-necked phalarope, a polyandrous shorebird with sex-role reversal. Since females are larger and therefore potentially more expensive to produce and may have greater variation in reproductive success, we predicted from Fisher’s hypothesis a male bias in population embryonic sex ratio, and from sex allocation theory, female biases in the clutches of females allocating more resources to reproduction. We measured eggs and chicks and sexed 535 offspring from 163 clutches laid over 6 years at two sites in Alaska. The embryonic sex ratio of 51.1 M:48.9 F did not vary from parity. Clutch sex ratio (% male) was positively correlated with clutch mean egg size, opposite to our prediction. Within clutches, however, egg size did not differ by sex. Male phalarope fitness may be more variable than previously thought, and/or differential investment in eggs may affect the within-sex fitness of males more than females. Eggs producing males were less dense than those producing females, possibly indicating they contained more yolk relative to albumen. Albumen contributes to chick structural size, while yolk supports survivorship after hatch. Sex-specific chick growth strategies may affect egg size and allocation patterns by female phalaropes and other birds.

Multigenerational response to artificial selection for biased clutch sex ratios in Tigriopus californicus populations.

Polygenic sex determination (PSD) is relatively rare and theoretically evolutionary unstable, yet has been reported across a range of taxa. Evidence for multilocus PSD is provided by (i) large between-family variance in sex ratio, (ii) paternal and maternal effects on family sex ratio and (iii) response to selection for family sex ratio. This study tests the polygenic hypothesis of sex determination in the harpacticoid copepod Tigriopus californicus using the criterion of response to selection. We report the first multigenerational quantitative evidence that clutch sex ratio responds to artificial selection in both directions (selection for male- and female-biased families) and in multiple populations of T. californicus. In the five of six lines that showed a response to selection, realized heritability estimated by multigenerational analysis ranged from 0.24 to 0.58. Divergence of clutch sex ratio between selection lines is rapid, with response to selection detectable within the first four generations of selection.

Assessing multiple endpoints of atrazine ingestion on gravid northern watersnakes (Nerodia sipedon) and their offspring

Ecotoxicological studies that focus on a single endpoint might not accurately and completely represent the true ecological effects of a contaminant. Exposure to atrazine, a widely used herbicide, disrupts endocrine function and sexual development in amphibians, but studies involving live-bearing reptiles are lacking. This study tracks several effects of atrazine ingestion from female Northern Watersnakes (Nerodia sipedon) to their offspring exposed in utero. Twenty-five gravid N. sipedon were fed fish dosed with one of the four levels of atrazine (0, 2, 20, or 200 ppb) twice weekly for the entirety of their gestation period. Endpoints for the mothers included blood estradiol levels measured weekly and survival more than 3 months. Endpoints for the offspring included morphometrics, clutch sex ratio, stillbirth, and asymmetry of dorsal scales and jaw length. Through these multiple endpoints, we show that atrazine ingestion can disrupt estradiol production in mothers, increase the likelihood of mortality from infection, alter clutch sex ratio, cause a higher proportion of stillborn offspring, and affect scale symmetry. We emphasize the need for additional research involving other reptile species using multiple endpoints to determine the full range of impacts of contaminant exposure.

Mind the gap: the ratio of yolk androgens and antioxidants varies between sons and daughters dependent on paternal attractiveness

Females are expected to partition resources between offspring in a context-dependent way to maximise total fitness returns from a reproductive attempt. Female zebra finches (Taeniopygia guttata) vary the allocation of yolk androgens and antioxidants among offspring. Importantly, the balance between androgens and antioxidants in yolks may be more important than their independent absolute amounts in terms of fitness consequences for developing young. Therefore, we tested whether the relative allocation of these two resources in yolks varies according to either the Trivers–Willard, positive or compensatory maternal investment hypothesis. We manipulated male attractiveness using coloured leg bands (red-banded males appear attractive; green-banded males, unattractive) and measured yolk androgens and antioxidants in each egg, egg sex, clutch sex ratio and female condition. While female zebra finches manipulated the balance of androgens and antioxidants within and between clutches in response to mate attractiveness, offspring sex and their own condition, they did not do so in a way that consistently followed any of the hypotheses. Mothers paired with unattractive males allocated a larger antioxidant/androgen ratio to daughters than sons. This pattern was reversed when paired to an attractive male; sons received a larger antioxidant/androgen ratio than daughters. We also found offspring sex ratio decreased with increasing female condition for unattractive males, but not for attractive males. However, without knowing the fitness consequences of the balance of different egg constituents, it is difficult to interpret the patterns consistently in terms of the Trivers–Willard, compensatory and positive investment hypotheses.

Strong but variable associations between social dominance and clutch sex ratio in a colonial corvid

We studied primary sex ratio of clutches in relation to social dominance for 6 years in a colony of free-living jackdaws, a small corvid. Social dominance was strongly associated with clutch sex ratio, with the difference in clutch sex ratio between the most and least dominant pairs being 30-40%. To our knowledge, this is the first demonstration of an association between social dominance and sex allocation in birds. However, the direction of this effect varied between years. Dominant jackdaws produced more sons during the first years of the study but fewer sons during the last years. Offspring sex was not related to laying order within a clutch, and the effect of social dominance on sex ratio was similar on eggs laid first, middle, or last. We investigated the effect of 2 factors (laying date and parental condition) that could have mediated the shift in the effect of social dominance on sex allocation in the course of the study. Laying date was positively associated with the proportion of males, but this effect was independent of social dominance. Maternal condition (residual mass over tarsus and egg volume) was related to social dominance but not to clutch sex ratio. Paternal condition (residual mass over tarsus) was not related to clutch sex ratio. We discuss how spatial or temporal variation in effects of variables such as social dominance on sex allocation can contribute to our understanding of the evolution of sex allocation in species with complex life histories.

Colour variation and alternative reproductive strategies in females of the common lizard Lacerta vivipara

Within-sex colour variation is a widespread phenomenon in animals that often plays a role in social selection. In males, colour variation is typically associated with the existence of alternative reproductive strategies. Despite ecological conditions theoretically favourable to the emergence of such alternative strategies in females, the social significance of colour variation in females has less commonly been addressed, relative to the attention given to male strategies. In a population of the common lizard, females display three classes of ventral colouration: pale yellow, orange and mixed. These ventral colours are stable through individual's life and maternally heritable. Females of different ventral colourations displayed different responses of clutch size, clutch hatching success and clutch sex-ratio to several individual and environmental parameters. Such reaction patterns might reflect alternative reproductive strategies in females. Spatial heterogeneity and presence of density- and frequency-dependent feedbacks in the environment could allow for the emergence of such alternative strategies in this population and the maintenance of colour variation in females.

No sexual differences in embryonic period in jackdawsCorvus monedulaand black‐headed gullsLarus ridibundus

Offspring survival probability usually decreases with hatching order, especially in species with brood reduction. Brood reduction in combination with a sex difference in embryonic period (the time between laying and hatching of an egg) can potentially have a profound effect on sex allocation, with higher investment in chicks of the early hatching sex because they are more likely to survive to fledge. Two recent studies reported sex differences in the embryonic period, but compared embryonic period between, rather than within, clutches, which does not control for possible environmental effects on both clutch sex ratio and embryonic period. We compared the embryonic period of sons and daughters within clutches in jackdawsCorvus monedulaand black‐headed gullsLarus ridibundus, two species with frequent brood reduction, and found no sexual difference in embryonic period. This suggests that sex allocation is not affected by sex differences in embryonic period in these species, but more studies are required to verify whether this is a general pattern.

Increased male sex ratio among brachypterous progeny in Melittobia femorata, a sib-mating parasitoid wasp (Hymenoptera: Eulophidae)

Abstract Melittobia are gregarious ectoparasitoid wasps that primarily attack various solitary bees and wasps. Characterized by high levels of inbreeding and an extremely female-biased sex ratio, these wasps appear to satisfy Hamilton's criteria for local mate competition. However, previous studies of sex ratio have failed to take into account an important aspect of Melittobia life history, namely that every clutch represents the combined reproductive output of the initial foundress female plus as many as 37 non-disperser short-winged daughters. Melittobia femorata Dahms is unique among the 13 species of Melittobia in that adults emerge as two temporally distinct clutches. While the overall sex ratio of the combined progeny from both clutches (0.025 ± 0.01) is typical for that for other Melittobia species (between 0.02 - 0.04 for single foundress cultures of the five other species included in this study), the sex ratio for the brachypterous first clutch of M. femorata from field-parasitized hosts averaged about 10 times greater (0.303 ± 0.10). Laboratory experiments with single foundress M. femorata cultures on the same host species (Trypoxylon politum Say) maintained at 25°C or 30°C produced smaller first clutch sizes compared to the field-infested hosts. While the number of brachypterous first clutch daughters was similar, significantly reduced first clutch sex ratios relative to field-parasitized hosts (0.07 - 0.10) were due to significantly fewer males being produced. Possible reasons for these differences and the elevated first clutch sex ratio in this species are discussed.

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.

Maternal body condition and plasma hormones affect offspring sex ratio in peafowl

In theory, females that can afford to do so may increase their fitness by investing in offspring of the sex with the greater probability of attaining high reproductive success. This has been observed in a wide variety of mammalian, reptilian and avian species although the proximate mechanism remains a mystery. Using a captive population of peafowl, Pavo cristatus, we investigated the relation between maternal quality, offspring sex ratio and plasma concentrations of the reproductive hormones testosterone and 17β-oestradiol and the principal avian stress hormone corticosterone. Each peacock was paired with three peahens that differed with respect to their relative body condition, creating a condition and dominance hierarchy within each pen and thus a situation in which we would predict investment in offspring to vary between hens. We found significant intercorrelations between maternal body condition (but not dominance rank or clutch size), maternal plasma levels of corticosterone and testosterone (but not 17β-oestradiol) and clutch sex ratio, such that good maternal condition, low plasma corticosterone and high levels of testosterone were associated with male biases in the sex ratio and increased investment in male eggs. The observed biases were probably present at laying, and thus add to the growing number of studies showing primary sex ratio adjustment in response to maternal body condition, and furthermore may indicate a role for corticosterone and testosterone in the avian sex manipulation process.

The impact of behavioral and physiological maternal effects on offspring sex ratio in the common snapping turtle, Chelydra serpentina

Theory suggests that maternal effects are especially important in organisms with environmentally-sensitive sex-determining mechanisms. However, there is no substantive body of empirical evidence to confirm this conjecture. We integrated field and laboratory studies to jointly evaluate the significance of behavioral (nest-site choice) and physiological (yolk hormone allocation) maternal effects on offspring sex ratio in the common snapping turtle (Chelydra serpentina), a species with temperature-dependent sex determination (TSD). Of the 16 microhabitat variables measured, only three (south, east, and total overstory vegetation cover) were significantly correlated with nest temperature: cooler nests were located under more vegetation cover. In turn, these microhabitat predictors of nest temperature, and nest temperature itself, may influence nest sex ratio: shadier, cooler nests were more likely to produce a higher proportion of male offspring than less shady, warmer nests. Analysis of eggs from these same nests incubated in a common garden design in the laboratory revealed that clutch sex ratio was unaffected by levels of yolk estradiol, yolk testosterone, or their interaction. Examination of both behavioral and physiological maternal effects revealed no concordant impact on offspring sex ratio. However, eggs from nests that produced male-biased sex ratios in the field yielded higher proportions of males under constant-temperature conditions in the laboratory. Our study confirms the importance of behavioral maternal effects in nature on offspring sex ratios in species with TSD, while also revealing the potential presence of a predisposition for sex-ratio production underlying TSD in this system.

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

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

Egg sex ratio and paternal traits: using within-individual comparisons

Empirical studies of sex ratios in birds have been limited due to difficulties in determining offspring sex. Since molecular sexing techniques removed this constraint, the last 5 years has seen a great increase in studies of clutch sex ratio manipulation by female birds. Typically these studies investigate variation in clutch sex ratios across individuals in relation to environmental characteristics or parental traits, and often they find no relationships. In this study we also found that clutch sex ratios did not vary in relation to a number of biological and environmental factors for 238 great tit Parus major nests. However, interesting sex ratio biases were revealed when variation in clutch sex ratios was analyzed within individual females breeding in successive years. There was a significant positive relationship between the change in sex ratio of a female's clutch from one year to the next and the relative body condition of her partner. Females mating with males of higher body condition in year x + 1 produced relatively male-biased sex ratios, and the opposite was true for females mated with lower condition males. Within-individual analysis also allowed investigations of sex ratio in relation to partner change. There was no change in sex ratios of females pairing with the same male; however, females pairing with a new male produced clutches significantly more female biased. Comparisons of clutch sex ratios within individuals may be a powerful method for detecting sex ratio variation, and perhaps female birds may indeed manipulate egg sex but require personal contextual experience for such decisions. Copyright 2002.

Pre-ovulation control of hatchling sex ratio in the Seychelles warbler.

Females of some bird species have a high degree of control over the sex ratio of their offspring at laying. Although several mechanisms have been put forward to explain how females might control the sex of their eggs, virtually nothing is known. As females are the heterogametic sex in birds, adjustment of the clutch sex ratio could arise either by pre- or post-ovulation control mechanisms. The Seychelles warbler (Acrocephalus sechellensis) exhibits extreme adaptive egg sex ratio bias. Typically, warblers produce only single-egg clutches, but by translocating pairs to vacant habitat of very high quality, most females were induced to produce two-egg clutches. Overall, females skewed clutch sex ratios strongly towards daughters (86.6%). This bias was evident in the first egg, but critically, also in the second eggs laid a day apart, even when all absent, unhatched, or unsexed second eggs were assumed to be male. Although a bias in the first egg may arise through either pre- or post-ovulation mechanisms, the skew observed in second eggs could only arise through pre-ovulation control. Post-ovulation adjustment may also contribute to skewed hatchling sex ratios, but as sex-biased release of gametes is likely to be a more efficient process of control, pre-ovulation mechanisms may be the sole means of adjustment in this species. High fitness differentials between sons and daughters, as apparent in the Seychelles warblers, may be necessary for primary sex ratio adjustment to evolve.

Molecular Determination of Sex-Ratio in Yellowhammer Emberiza citrinella Offspring

Theory predicts skewed offspring sex-ratios in a range of situations in which the economics of producing the two sexes differ. Offspring sex-ratio skews in birds are relatively scarcely observed compared to other taxa. This could be because avian molecular sexing techniques, which allow young birds to be sexed, have only recently become available. Alternatively, birds may be largely constrained from adaptively manipulating the sex-ratio of their offspring. We used a recently-developed molecular sexing technique for birds to sex 420 Yellowhammer Emberiza citrinella offspring from 168 clutches found in Oxfordshire. Clutch sex-ratio of the population did not depart from the expected binomial distribution, and there was no variation in clutch sex-ratio with laying date, breeding attempt, or a variety of habitat variables which were predicted to differentially affect the survival and future reproductive success of offspring of the two sexes. There was no difference in size or growth rate of the sexes and nestling mortality was not sex-biased. Hence, although we can identify possible advantages of manipulating the sex-ratio in this species, it seems not to be used as a breeding strategy. Given the lack of consistent evidence for skewed avian offspring sex-ratios, more experimental work is required to determine whether, and how, birds may adaptively manipulate their offspring sex-ratio.

Offspring allocation in externally ovipositing fig wasps with varying clutch size and sex ratio

The simultaneous optimization of clutch size and sex ratio is a tricky problem. Unless parameters such as host size or fecundity exist to pin down the optimal clutch size, this problem remains elusive to analytical analysis. This is because the fitness landscape with respect to dutch size and sex ratio does not have one single evolutionarify stable peak toward which the population can evolve. To solve this problem, I used a computer emulation to optimize both dutch size and sex ratio using externally ovipositing fig wasps as a model taxon. The simulation approach allows the use of integer numbers of eggs rather than assuming that females can produce any sex ratio between 0 and 1. When females have no information about the patches on which they oviposit, they produce either large dutches with a strong female bias or clutches of a single male egg. When females have complete knowledge of their oviposition site, a set of conditional substrategies is evohitionarih/ stable. Again, these substrategies are either large dutches with a female bias or dutches consisting of a single male egg. This dichotomous oviposition pattern results in unrelated males sharing a fig, a condition conducive to the evolution of fatal fighting. Selection on female oviposition strategies may therefore be an important driving force behind high levels of fighting observed between male fig wasps.

Sex Allocation and Sexual Asymmetries in Intra-Brood Competition in the Parasitic Wasp Bracon hebetor

1. Bracon hebetor is a gregarious parasitoid with a female-biased sex ratio. While female-biased sex ratios are often indicative of local mate competition (LMC), B. hebetor outbreeds, making LMC an unlikely explanation for biased sex ratios in this species. In this study we examined an alternative hypothesis that may explain female-biased sex ratios: competitive asymmetries between larval sons and daughters. 2. We measured two types of competitive asymmetries: asymmetric density responses (differential responses to clutch size), and asymmetric composition responses (responses to change in clutch sex ratio). We measured competitive asymmetries in terms of their effects on body size, development time, survivorship, longevity, and daily and lifetime fecundity or mating ability. 3. Males and females emerged as smaller adults, developed more quickly and experienced higher rates of larval mortality when they developed in larger clutches. The effect of clutch size on body size and survivorship was similar for males and females. Increasing clutch size decreased male larval development time more than female development time, although the effect was marginal. 4. Male and female body sizes increased as within-clutch sex ratios became more male-biased, indicating that females, not males, are stronger competitors. This should lead to male-biased sex ratios, rather than the female-biased sex ratios that exist in B. hebetor. Sex ratio had no influence on developmental time or survivorship of either sex. 5. Larger males and females lived longer than smaller individuals, whether they fed on hosts or honey. Larger females had higher daily and lifetime fecundities than smaller females. Larger males copulated with more females and sired more daughters both per day and per lifetime than did smaller males. These body size effects were only detectable when hosts were abundant. At low host densities, differences between large and small wasps were absent. 6. Although we detected asymmetric composition responses in terms of body size, the effects were slight. Therefore, we conclude that competitive asymmetries are unlikely to have important effects on male and female fitness or on the sex allocation decisions of B. hebetor.

Nest-Site Selection and Offspring Sex Ratio in Painted Turtles, Chrysemys picta

We studied the influence of nest-site selection on nest temperature and clutch sex ratio in a northern population of painted turtles (Chrysemys picta). Comparison of characteristics of pairs of nests of individual females, within and between years, provided no evidence that these females followed a simple pattern in choosing nest sites and no indication that they influenced sex ratio by choosing sites with specific characteristics. Microhabitat features of nests were compared to the same characteristics of randomly chosen sites in the nesting area and in contrast to randomly chosen sites, nests were significantly warmer and more likely to occur on slopes. Sex ratios produced in nests were not correlated with any measured nest characteristic except temperature, and nest temperatures were more dependent on yearly variations in climate than on variations in site characteristics. Nest-temperature distributions were unimodal, suggesting that fe- males selected nest sites to maximize the probability that eggs would complete development, rather than to influence offspring sex ratio.