Clutch Sex Ratios Research Articles

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.

The sex‐determination pattern in crocodilians: A systematic review of three decades of research

Sex in crocodilians is not determined by chromosomes, but by egg incubation temperature, where different temperatures produce different clutch sex ratios. Two patterns have been proposed to describe these changes in sex ratios: a 100% female proportion at low and high temperatures with male predominance at intermediate ones (FMF) or a simpler pattern with a single female-to-male transition (FM). Over the last three decades, researchers have provided empirical information to support either of these two patterns in different species; however, no consensus has been reached partly because data have not been analysed as a whole. Here, we aimed at gathering the existing data on these patterns to provide models of temperature-dependent sex determination in those crocodilians studied so far. Potentially relevant publications were searched on Web of Knowledge, Scopus, Scielo and Science Direct. Studies that reported results on the sexual identity of crocodilian hatchlings obtained from constant temperature incubation treatments were considered. Using statistical models varying in their underlying assumptions, we evaluated which sex-determination pattern was best supported for the studied crocodilians and constructed species-specific and latitude-specific models. Based on the 8,458 sexed hatchlings studied throughout 31 studies, we show that the evidence supports a shared FMF pattern in all the crocodilian species for which enough data are available. We find that such pattern changes between species and at different latitudes. These results suggest a lability of the FMF crocodilian sex-determination pattern, a key feature under the present climate change scenario.

Endogenous Corticosterone Elevations Five Hours Prior to Ovulation do not Influence Offspring Sex Ratios in Zebra Finches

Previous research suggests that environmental and social factors can drive female birds to bias offspring sex ratios. The underlying mechanisms controlling these adjustments remain unclear. Results from experimental and correlative research suggest that maternal corticosterone plays an important role in this process. Since females are the heterogametic sex in birds, corticosterone may potentially bias offspring sex ratios during meiotic segregation, through non-random segregation of sex chromosomes. In a previous study, we showed that pharmacological elevations of corticosterone near the time of meiotic segregation exerted an effect on offspring sex ratio, causing female Zebra Finches ( Taeniopygia guttata) to produce significantly more males. Here, we aimed to determine whether endogenous elevations in the physiological range have similar effects on offspring sex. First we examined offspring sex ratio in relation to baseline corticosterone levels to determine if natural variation in circulating corticosterone near the time of meiotic segregation is related to offspring sex ratio. Next, we used a 5-minute bag handling protocol to induce corticosterone elevations 5 hours prior to ovulation. Maternal baseline corticosterone levels did not correlate with average clutch sex ratios. In addition, the sex ratios produced by females exposed to handling stress did not differ from sex ratios produced by unmanipulated females. Together these results suggest that physiological levels of endogenous corticosterone, both baseline and acutely elevated near the time of sex determination may not be involved in the adjustment of primary sex ratios in Zebra Finches.

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.

Cross‐fostering eggs reveals that female collared flycatchers adjust clutch sex ratios according to parental ability to invest in offspring

Across animal taxa, reproductive success is generally more variable and more strongly dependent upon body condition for males than for females; in such cases, parents able to produce offspring in above-average condition are predicted to produce sons, whereas parents unable to produce offspring in good condition should produce daughters. We tested this hypothesis in the collared flycatcher (Ficedula albicollis) by cross-fostering eggs among nests and using the condition of foster young that parents raised to fledging as a functional measure of their ability to produce fit offspring. As predicted, females raising heavier-than-average foster fledglings with their social mate initially produced male-biased primary sex ratios, whereas those raising lighter-than-average foster fledglings produced female-biased primary sex ratios. Females also produced male-biased clutches when mated to males with large secondary sexual characters (wing patches), and tended to produce male-biased clutches earlier within breeding seasons relative to females breeding later. However, females did not adjust the sex of individuals within their clutches; sex was distributed randomly with respect to egg size, laying order and paternity. Future research investigating the proximate mechanisms linking ecological contexts and the quality of offspring parents are able to produce with primary sex-ratio variation could provide fundamental insight into the evolution of context-dependent sex-ratio adjustment.

Oviposition Restraint and Developmental Alterations in the Ectoparasitic Wasp,Nasonia vitripennis, When Utilizing Puparia Resulting From Different Size Maggot Masses ofLucilia illustris,Protophormia terraenovae, andSarcophaga bullata

Adult females of the ectoparasitoid Nasonia vitripennis (Walker) are capable of distinguishing between hosts of different quality, and then correspondingly adjust clutch sizes and sex ratios of the offspring. In this study, we examined whether the size of the maggot mass, and presumably the developmental temperature, influenced the suitability of the resulting fly pupal and pharate adult stages as hosts for N. vitripennis. Three sizes of maggot masses (100; 500; and 1,000 individuals per mass) were selected for use to generate hosts based on previous studies characterizing developmental and heat shock response differences for the flies. For all host species tested (Lucilia illustris, Protophormia terraenovae, and Sarcophaga bullata), the rate of parasitism by N. vitripennis decreased with increasing maggot mass size. When successful parasitism did occur, parasitoid development increased in duration, clutch sizes decreased, mortality from egg hatch to adult emergence elevated, male biased sex ratios were produced, and adult wasp body sizes were truncated with increasing fly larval density. These wasp life history features are consistent with reductions in host quality. Host quality reductions corresponded to production of heat shock proteins 23, 60, and 70. Heat shock protein synthesis appeared to occur at the expense of normal protein production because total hemolymph protein concentrations decreased with increased larval density in maggot masses. These observations argue that use of N. vitripennis in criminal investigations to estimate periods of insect activity or a minimum post mortem interval must take into account the maggot mass history of the hosts used by the wasp.

A tropical oviparous lizard, Calotes versicolor, exhibiting a potentially novel FMFM pattern of temperature‐dependent sex determination

Among squamate reptiles, lizards exhibit an impressive array of sex-determining modes viz. genotypic sex determination, temperature-dependent sex determination, co-occurrence of both these and those that reproduce parthenogenetically. The oviparous lizard, Calotes versicolor, lacks heteromorphic sex chromosomes and there are no reports on homomorphic chromosomes. Earlier studies on this species presented little evidence to the sex-determining mechanism. Here we provide evidences for the potential role played by incubation temperature that has a significant effect (P < 0.01) on gonadal sex and sex ratio. The eggs were incubated at 14 different incubation temperatures. Interestingly, 100% males were produced at low (25.5 ± 0.5 ° C) as well as high (34 ± 0.5 ° C) incubation temperatures and 100% females were produced at low (23.5 ± 0.5 ° C) and high (31.5 ± 0.5 ° C) temperatures, clearly indicating the occurrence of TSD in this species. Sex ratios of individual clutches did not vary at any of the critical male-producing or female-producing temperatures within as well as across the seasons. However, clutch sex ratios were female- or male-biased at intermediate temperatures. Thermosensitive period occurred during the embryonic stages 30-33. Three pivotal temperatures operate producing 1:1 sex ratio. Histology of gonad and accessory reproductive structures provide additional evidence for TSD. The sex-determining pattern, observed for the first time in this species, that neither compares to Pattern I [Ia (MF) and Ib (FM)] nor to Pattern II (FMF), is being referred to as FMFM pattern of TSD. This novel FMFM pattern of sex ratio exhibited by C. versicolor may have an adaptive significance in maintaining sex ratio.

Effective heritability of targets of sex-ratio selection under environmental sex determination

Selection is expected to maintain primary sex ratios at an evolutionary equilibrium. In organisms with temperature-dependent sex determination (TSD), targets of sex-ratio selection include the thermal sensitivity of the sex-determining pathway (hereafter, sex determination threshold) and nest-site choice. However, offspring sex may be canalized for nests located in thermally extreme environments; thus, genetic variance for the sex determination threshold is not expressed and is invisible to direct selection. The concept of 'effective heritability' accounts for this dependence and provides a more realistic prediction of the expected evolutionary response to selection in the wild. Past estimates of effective heritability of the sex determination threshold, which were derived from laboratory data, suggested that the potential for the sex determination threshold to evolve in the wild was extremely low. We re-evaluated original estimates of this parameter by analysing field-collected measures of nest temperatures, vegetation cover and clutch sex ratios from nests in a population of painted turtles (Chrysemys picta). We coupled these data with measurements of broad-sense heritability of the sex determination threshold in C. picta, using an experiment that splits clutches of eggs between a constant temperature (i.e. typical laboratory incubation) and a daily fluctuating temperature (i.e. similar to natural nests) with the same mean. We found that (i) the effective heritability of the sex determination threshold appears to have been historically underestimated and the effective heritability of nest-site choice has been overestimated and (ii) significant family-by-incubation treatment interaction exists for sex for C. picta between constant- and fluctuating-temperature regimes. Our results suggest that the thermal sensitivity of the sex-determining pathway may play a larger, more complex role in the microevolution of TSD than traditionally thought.

Contradictory results in sex ratio studies: populations do not necessarily differ

In avian sex ratio studies, results often differ between species and between populations within species. Some researchers argued that positive results were simply statistical artefacts and that sex ratio adjustment did not exist. However, many of the proposed mechanisms of sex ratio adjustment result in costly laying gaps. In these cases, females laying large clutches may restrict the sex manipulation to the first egg of the clutch. Consequently, detectability of sex ratio adjustment on the level of the clutch can be low. Though obvious, this fact is often neglected in the literature. Using simulations, I show that the proportion of undetected sex manipulation can be surprisingly high when the manipulation is restricted to the first egg. If the sample size is 50 broods, there is 47% and 71% chance in 6- and 12-egg clutches, respectively, that sex manipulation is undetected. Even with large samples (n = 100), the figures are 15% and 46%. These data suggest that nonsignificant results for clutch sex ratios do not necessarily mean that sex is not manipulated in a portion of the brood, e.g. in first-laid eggs. Hence, whenever possible, data on laying order-specific sex manipulation should also be collected. Without such data, contradictory results on brood sex ratios should be interpreted cautiously.

Interclutch Variation in Sex Ratios Produced at Pivotal Temperature in the Red-eared Slider, a Turtle With Temperature-dependent Sex Determination

Many reptiles exhibit temperature-dependent sex determination (TSD) in which the incubation temperature of the egg determines the sex of the embryo. The purpose of the current study was to examine intraspecific variation in temperature sensitivity during TSD. Two aspects of temperature sensitivity were evaluated in the Red-Eared Slider, Trachemys scripta: (1) clutch-specific variation in sex ratios produced at pivotal temperature and (2) variation in clutch sex ratios produced over the nesting season (e.g., early nesting season, midnesting season, late nesting season). Relatively large numbers of clutch sex ratios were examined from two or three time periods (e.g., early nesting season, midnesting season, late nesting season), during each of three nesting seasons. The results indicate that pivotal temperatures vary significantly among clutches, with clutch sex ratios ranging from all male to all female when incubated near the putative pivotal temperature. The results on seasonal variation in clutch sex ratios were more ambiguous. Data from two of the nesting seasons do not reveal significant variation between time periods. During the third nesting season, sex ratios from the first two time periods were not significantly different from one another, but the sex ratios from the very end of the nesting season were significantly different from those of the two earlier time periods. In summary, the results reveal a clutch-specific variation in pivotal temperatures, but the results from the seasonal study of sex ratios did not consistently reveal a shift in sex ratios over each nesting season.

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.

PEREGRINE FALCON EGGS: EGG SIZE, HATCHLING SEX, AND CLUTCH SEX RATIOS

Abstract Eggs (n = 367) collected from wild Peregrine Falcon (Falco peregrinus anatum) nests between 1976 and 1990 in Colorado and New Mexico were artificially incubated and hatched. We retrospectively examined these data for variation in egg length, breadth, and initial mass of hatchlings to resolve questions about relationships among egg size, chick size, and sex; and egg size related to first and second clutches and years. Egg length and breadth were significantly related to chick mass at hatching. Neither egg size nor hatchling mass were related to sex. Egg breadth slightly increased and then decreased over the years eggs were collected, which possibly reflects a re-established and then aging wild falcon population or other environmental variation. We also evaluated clutch sex ratios relative to theory based on sexual size dimorphism and local resource competition. Sex ratios did not significantly differ from 1:1 within first or second clutches separately or when combined. Thus, Peregrine Falcons in t...

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.

Primary and secondary sex ratio manipulation by zebra finches

Wild zebra finches,Taeniopygia guttata, breed opportunistically when there is sufficient food available, often rapidly mobilizing their reproductive systems in response to an ephemeral boom in grass seed production. For females in captivity, fecundity, attractiveness to mates and survival to reproduction are all correlated with their fledging weight. By contrast, for males, only attractiveness is related to fledging weight; the relationship between fledging weight and male mortality is much weaker and that for male fecundity is unknown. Previous work thus suggests that how much food nestlings receive will have a profound impact on their reproductive success, and that this effect may be more marked for females than for males. I manipulated the food available to domesticated breeding zebra finches to test Trivers & Willard's (1973,Science,179,90–92) hypothesis of adaptive sexual investment. When food availability was restricted, clutch sex ratios were significantly more male biased than when food was available in excess. Within clutches, daughters hatched sooner than sons and first-hatched chicks fledged at higher weights than those that hatched last. Chick mortality was female biased when food availability was low but male biased when food availability was unrestricted. I compared the song output of brothers of differing weight at independence, but found no significant difference between them. These data suggest that zebra finches manipulate both their primary and secondary sex ratios in relation to food availability to invest adaptively in sons and daughters, and support Trivers & Willard's hypothesis.

Sex Determination and Sex Ratios inCrocodylus palustris

Incubation temperature determines sex in the mugger crocodile, Crocodylus palustris . Exclusively females are produced at constant temperatures of 28.0°C through 31°C. At 32.5°C, only males are produced. Both sexes are produced in varying proportions at 31.5, 32.0, and 33.0°C. Embryo survival is not affected within this range, but developmental rate and total incubation time are strongly temperature dependent. In natural nests laid in breeding enclosures, cool incubation temperatures produced only females whereas males were produced only in warm nests. Clutch sex ratios were female or male biased. Yearly sex ratios (=percent male) varied from 0.05 to 0.58; overall sex ratio during six nesting seasons was 0.24 (1 male: 3 females). Sex ratio and incubation time vary with nest location and temperature in a manner consistent with the constant temperature results. Incubation time decreases with increasing incubation temperature, and is an accurate predictor of sex ratio in the field and laboratory. To date, temperature-dependent sex determination (TSD) has been reported in five species of Crocodylus and in three species of Alligatorinae; but the TSD patterns in these groups differ. The TSD pattern of C. palustris is similar to that of C. porosus . Nesting in C. palustris is synchronized with the seasonal availability of thermal regimes suitable for incubation. Resultant sex ratios are a consequence of when and where eggs are laid. Early nests are located in warm, sunny sites; in contrast, late season nests are located in the shade. An egg transplant experiment demonstrated that sex ratios could be altered by simple manipulations of nest temperatures in the field. The adaptive significance of TSD in crocodilians may relate to the influence of incubation temperature on various hatchling attributes, particularly growth.