Long-lasting fitness consequences of prenatal sex ratio in a viviparous lizard

Maternal effects and early environmental conditions are important in shaping offspring developmental trajectories. For example, in laboratory mammals, the sex ratio during gestation has been shown to influence fitness-related traits via hormonal interaction between fetuses. Such effects have the potential to shape, or constrain, many important aspects of the organism's life, but their generality and importance in natural populations remain unknown. Using long-term data in a viviparous lizard, Lacerta vivipara, we investigated the relationship between prenatal sex ratio and offspring growth, survival, and reproductive traits as adults. Our results show that females from male-biased clutches grow faster, mature earlier, but have lower fecundity than females from female-biased clutches. Furthermore, male reproduction was also affected by the sex ratio during embryonic development, with males from male-biased clutches being more likely to successfully reproduce at age one than males from female-biased clutches. Thus, the sex ratio experienced during gestation can have profound and long-lasting effects on fitness in natural populations of viviparous animals, with important implications for life-history evolution and sex allocation.     

Consistent sex ratio bias of individual female dragon lizards

Sex ratio evolution relies on genetic variation in either the phenotypic traits that influence sex ratios or sex-determining mechanisms. However, consistent variation among females in offspring sex ratio is rarely investigated. Here, we show that female painted dragons (Ctenophorus pictus) have highly repeatable sex ratios among clutches within years. A consistent effect of female identity could represent stable phenotypic differences among females or genetic variation in sex-determining mechanisms. Sex ratios were not correlated with female size, body condition or coloration. Furthermore, sex ratios were not influenced by incubation temperature. However, the variation among females resulted in female-biased mean population sex ratios at hatching both within and among years.     

Manipulation of offspring sex ratio by second-mated female house wrens

In 1973, Trivers and Willard proposed that offspring sex ratio should be associated with the quality of parental care likely to be provided to the offspring. We tested this hypothesis by comparing fledgling sex ratios in nests of first- and second-mated female house wrens (Troglodytes aedon). In our Wyoming population, second-mated females typically receive little or no male parental assistance and fledge fewer and lower-quality young compared with first-mated females. Assuming that being of lower quality has stronger negative effects on the future reproductive success of males than that of females in this polygynous population, we predicted that fledgling sex ratios in the nests of second-mated females would be female-biased compared with the fledgling sex ratios of first-mated females. Additionally, we asked whether any sex bias at fledging could have resulted from male-biased nestling mortality caused by sex-biased parental provisioning. As predicted, mean fledgling sex ratios in nests of second-mated females were more female-biased than fledgling sex ratios in nests of first-mated females. However, we found no evidence of either sex-biased nestling mortality or sex-biased parental provisioning. These findings suggest that females are responding to their status as second-mated females and to the associated low-quality parental care that their young are likely to receive by producing female-biased clutches rather than manipulating the offspring sex ratio through sex-biased nestling mortality.     

Sex ratio variation in female-biased populations of Notostracans

Females from female-biased populations of the notostracan Triops newberryi produce viable eggs when reared in isolation. Clutches produced under such conditions exhibit sex-ratio polymorphism. One category of females (monogenics) produces only female offspring; the second category (amphigenics) produces clutches with a sex ratio of 3 females: 1 male. The relative proportions of the two categories of females varies significantly between populations and is correlated with population sex ratio. This correlation, and the pattern of offspring distribution in amphigenics, suggests that sex is determined by an autosomal Mendelian gene locus for which the male-determining allele is recessive. Limited pedigree analysis of lineages under selfing support the genetic model.     

INDIVIDUAL SEX RATIO ADJUSTMENT IN RESPONSE TO THE OPERATIONAL SEX RATIO IN THE SOUTHERN GREEN STINKBUG

Females of the southern green stinkbug, Nezara viridula (Hemiptera: Pentatomidae), initiating copulation in a female-biased environment produced relatively more sons than females initiating copulation in a male-biased environment. Although families suffering greater mortality yielded more sons, the difference in offspring sex ratio between treatments was not due to differential mortality by sex since the distribution of family size did not vary between treatments. Female condition, indexed by female size and size of the first egg mass laid, did not vary between treatments and, therefore, apparently did not contribute to the results. Thus, it appears that the stinkbug is capable of facultative sex ratio adjustment in response to the operational sex ratio, increasing the production of sons when males are rare. In nature, overlapping generations and female-biased operational sex ratios may occur; conditions under which selection for sex ratio adjustment is most intense.     

Effects of time-dependent competition for oviposition sites on clutch sizes and offspring sex ratios in a fig wasp

Fig wasps have been known as one of the best-documented examples of female-biased sex ratio predicted from the local mate competition (LMC) theory. However, observed sex ratios appear more female-biased than predicted. Before a close match between theory and observation can be claimed, the number and sex ratio of offspring left by each foundress in a multi-foundress syconium need to be determined. We examined the clutch size and sex ratio of individual females of the pollinator fig wasp Blastophaga nipponica (Agaonidae) in experiments using a pair of fertile and sterile females in which sequence and time interval of entering syconia were manipulated. To determine the number and sex ratio of offspring left by each foundress in a multi-foundress syconium, we prepared sterilized females that could oviposit ordinarily but whose offspring could not develop at all, by irradiating the females with ⁶⁰Co gamma rays. Female fig wasps contributed different numbers and sex ratios of offspring to the total brood within a syconium, due to different entry times among them. The variation in clutch sizes with different entry times appeared to be caused by competition for oviposition sites, and sex ratios to be adjusted according to the clutch size.     

Constrained sex allocation in a parasitoid due to variation in male quality

The theory of constrained sex allocation posits that when a fraction of females in a haplodiploid population go unmated and thus produce only male offspring, mated females will evolve to lay a female-biased sex ratio. I examined evidence for constrained sex ratio evolution in the parasitic hymenopteran Uscana semifumipennis. Mated females in the laboratory produced more female-biased sex ratios than the sex ratio of adults hatching from field-collected eggs, consistent with constrained sex allocation theory. However, the male with whom a female mated affected her offspring sex ratio, even when sperm was successfully transferred, suggesting that constrained sex ratios can occur even in populations where all females succeed in mating. A positive relationship between sex ratio and fecundity indicates that females may become sperm-limited. Variation among males occurred even at low fecundity, however, suggesting that other factors may also be involved. Further, a quantitative genetic experiment found significant additive genetic variance in the population for the sex ratio of offspring produced by females. This has only rarely been demonstrated in a natural population of parasitoids, but is a necessary condition for sex ratio evolution. Finally, matings with larger males produced more female-biased offspring sex-ratios, suggesting positive selection on male size. Because the great majority of parasitic hymenoptera are monandrous, the finding of natural variation among males in their capacity to fertilize offspring, even after mating successfully, suggests that females may often be constrained in the sex allocation by inadequate number or quality of sperm transferred.     

Constrained oviposition and female-biased sex allocation in a parasitic wasp

 In haplodiploid organisms such as parasitic wasps, substantial oviposition by females without sperm is predicted to cause mated females to bias their offspring sex ratios towards daughters. The effect of the production of sons by unmated and sperm-depleted (constrained) females on sex allocation by mated females was studied in two populations of the parasitic wasp Bracon hebetor over 3 years. B. hebetor females who depleted their sperm reserves from prior matings rarely remated and became constrained to produce only sons. Constrained females readily oviposited and produced clutches similar in size to those produced by mated females. Although the fraction of constrained females in the population varied considerably between sites and sampling dates, it was usually high enough to favor the production of female-biased sex ratios by mated females. Mated females consistently produced female-biased sex ratios. However, we found no evidence that the sex ratios produced by mated females from the field shifted in relation to the proportion of constrained females in the population. Females held with males or held in isolation also produced female-biased sex ratios. These findings suggest that, in B. hebetor, mated females produce sex ratios that reflect the average fraction of constrained females over evolutionary time. Received: 21 June 1996 / Accepted: 27 August 1996     

Offspring sex ratio in the sequentially polygamous Penduline Tit Remiz pendulinus

Despite the growing literature on facultative sex-ratio adjustment in chromosomal sex-determining vertebrate taxa (birds, mammals), the consistency of results is often low between studies and species. Here, we investigate the primary and secondary offspring sex ratio of a small passerine bird, the Eurasian Penduline Tit (Remiz pendulinus) in three consecutive years. This species has a uniquely diverse breeding system, in which the male (and/or the female) abandons the nest during egg-laying, and starts a new breeding attempt. This allowed us to test (1) whether patterns of parental care, i.e., male-only care, female-only care or biparental desertion, influence offspring sex ratio, and (2) whether the offspring sex ratio is repeatable between successive clutches of males and females. Using molecular markers to sex 497 offspring in 176 broods, we show that (1) offspring sex ratio does not depend on which parent provides care, and (2) the offspring sex ratio is not repeatable between clutches of a given individual. The overall primary and secondary offspring sex ratio at a population level is not different from parity (54 ± 6% males, and 50 ± 3% (mean ± SE), respectively). We suggest that ecological and phenotypic factors, rather than individual traits of parents, may influence offspring’s sex, and conclude that there is currently no evidence for a facultative adjustment of offspring sex ratio in the Penduline Tit.     

Do female parasitoid wasps recognize and adjust sex ratios to build cooperative relationships?

Sex allocation theories provide excellent opportunities to investigate not only the extent to which individuals' behaviour is adaptive, but also how they use relevant information for their decision-making. Here, we investigated whether female parasitoid wasps recognize the sex ratios of other females and adjust their laying sex ratios accordingly. Specifically, we tested the prediction of reciprocal cooperation over sex allocation. Theory predicts more female-biased (cooperative) sex ratios than in the interest of individual benefit, when a restricted number of ovipositing females interact for a long period and their offspring mate within the natal patch. This is because the female-biased sex ratio reduces competition for mates among the male offspring of the females and increases the overall reproductive productivity of the patch. In this case, females would be expected to respond to more even (noncooperative) sex ratios by others and to retaliate by also producing a less female-biased sex ratio to avoid exploitation by defectors. However, contrary to this prediction, our experiment using a sterile male technique showed that female Melittobia australica did not change their offspring sex ratios in response to the sex ratios produced by other females. This suggests that their extremely female-biased sex ratios cannot be explained by reciprocity. A meta-analysis of studies examining sex recognition ability in parasitoid wasps also did not support the predicted pattern of relevant sex ratio adjustment, suggesting that parasitoid females do not possess this ability. Here, we discuss the conditions necessary for the evolution of reciprocity linked to recognition ability.     

Offspring sex is not related to maternal allocation of yolk steroids in the lizard Bassiana duperreyi (Scincidae)

The eggs of birds and reptiles contain detectable levels of several steroid hormones, and experimental application of such steroids can reverse genetically determined sex of the offspring. However, any causal influence of maternally derived yolk steroids on sex determination in birds and reptiles remains controversial. We measured yolk hormones (dihydrotestosterone, testosterone, and 17 beta-estradiol) in newly laid eggs of the montane scincid lizard Bassiana duperreyi. This species is well suited to such an analysis because (1) offspring sex is influenced by incubation temperatures and egg size as well as by sex chromosomes, suggesting that yolk hormones might somehow be involved in the complex pathways of sex determination, and (2) experimental application of either estradiol or fadrozole to such eggs strongly influences offspring sex. We obtained yolk by biopsy, before incubating the eggs at a temperature that produces a 50:50 sex ratio. Yolk steroid levels varied over a threefold range between eggs from different clutches, but there were no significant differences in yolk steroids, or in relative composition of steroids, between eggs destined to become male versus female. Further, yolk steroid concentrations were not significantly related to egg size. Thus, yolk steroid hormones do not appear to play a critical role in sex determination for B. duperreyi.     

Sex ratios of Spalangia endius (Hymenoptera: Pteromalidae), in relation to current theory

Abstract. 1. Spulungiu endius Walker is a solitary parasitoid of house fly puparia.
2. The sex and size of S.endius was not related to host size.
3. In the laboratory the mean sex ratio of all offspring of nine groups, each comprising twenty females, was consistently female-biased (x = 83.5%, range 79–87%). The sex ratio in the field was less female-biased and showed greater fluctuation (61–75%). This may be a consequence of females laying male eggs before mating, some females remaining unmated, possible shorter adult life expectancy in the field than in the laboratory, and, perhaps, the presence of conspecific females.
4. The sex ratio of offspring of individual females varied from 66% to 100% females, and males were deposited early in the oviposition sequence.
5. Although a large number of fly puparia died before adult flies or parasitoids emerged (64.5%; n = 5874), there was no differential mortality of either sex.
6. Our results fit no general sex ratio hypothesis and we conclude that (i) the genetic nature of sex ratios in these insects needs careful examination, and (ii) the prevalence of female-biased sex ratios in solitary parasitoids needs investigation.     

No seasonal sex-ratio shift despite sex-specific fitness returns of hatching date in a lizard with genotypic sex determination

Sex allocation theory predicts that mothers should adjust their sex-specific reproductive investment in relation to the predicted fitness returns from sons versus daughters. Sex allocation theory has proved to be successful in some invertebrate taxa but data on vertebrates often fail to show the predicted shift in sex ratio or sex-specific resource investment. This is likely to be partly explained by simplistic assumptions of vertebrate life-history and mechanistic constraints, but also because the fundamental assumption of sex-specific fitness return on investment is rarely supported by empirical data. In short-lived species, the time of hatching or parturition can have a strong impact on the age and size at maturity. Thus, if selection favors adult sexual-size dimorphism, females can maximize their fitness by adjusting offspring sex over the reproductive season. We show that in mallee dragons, Ctenophorus fordi, date of hatching is positively related to female reproductive output but has little, if any, effect on male reproductive success, suggesting selection for a seasonal shift in offspring sex ratio. We used a combination of field and laboratory data collected over two years to test if female dragons adjust their sex allocation over the season to ensure an adaptive match between time of hatching and offspring sex. Contrary to our predictions, we found no effect of laying date on sex ratio, nor did we find any evidence for within-female between-clutch sex-ratio adjustment. Furthermore, there was no differential resource investment into male and female offspring within or between clutches and sex ratios did not correlate with female condition or any partner traits. Consequently, despite evidence for selection for a seasonal sex-ratio shift, female mallee dragons do not seem to exercise any control over sex determination. The results are discussed in relation to potential constraints on sex-ratio adjustment, alternative selection pressures, and the evolution of temperature-dependent sex determination.     

Sex ratio of mirid populations shifts in response to hostplant co‐infestation or altered cytokinin signaling

Herbivore species sharing a host plant often compete. In this study, we show that host plant-mediated interaction between two insect herbivores-a generalist and a specialist-results in a sex ratio shift of the specialist's offspring. We studied demographic parameters of the specialist Tupiocoris notatus(Hemiptera: Miridae)when co-infesting the host plant Nicotiana attenuata(Solanaceae) with the generalist leafhopper Empoasca sp.(Hemiptera: Cicadellidae). We show that the usually female-biased sex ratio of T. notatus shifts toward a higher male proportion in the offspring on plants coinfested by Empoasca sp. This sex ratio change did not occur after oviposition, nor is it due differential mortality of female and male nymphs. Based on pyrosequencing and PCR of bacterial 16 S rRNA amplicons, we concluded that sex ratio shifts were unlikely to be due to infection with Wolbachia or other known sex ratio-distorting endosymbionts. Finally, we used transgenic lines of N.attenuata to evaluate if the sex ratio shift could be mediated by changes in general or specialized host plant metabolites. We found that the sex ratio shift occurred on plants deficient in two cytokinin receptors(irCHK2/3).Thus, cytokinin-regulated traits can alter the offspring sex ratio of the specialist T.notatus.     

Factors affecting female-biased sex ratio in a trap-nesting wasp, Trypoxylon malaisei

We examined the female-biased sex ratio of a trap-nesting wasp Trypoxylon malaisei considering the following factors: (1) local mate competition (LMC), (2) resource quality, (3) partial bivoltinism, and (4) presence of constrained females. The sex ratio (expressed as male ratio) at emergence was strongly female biased, i.e., 0.30 and 0.19, in terms of the number and investment, respectively. To evaluate the primary sex ratio, we analyzed the data from nests where all the offspring successfully emerged, excluding nests composed of single-sex offspring. The primary sex ratio was also female biased, at 0.33 and 0.21, in terms of the number and investment, respectively. LMC was highly responsible for the female-biased sex ratio because both the nonrandom oviposition sequence [females at inner cells and male(s) at outer cells] and earlier emergence of males allowed sib-matings to occur. In contrast, the other three factors little affected the female-biased sex ratio: the sex ratio was fairly constant when resource quality (nest size) varied, partial bivoltinism was extremely rare or absent, and constrained females were absent or did not reproduce at all. Received: June 19, 1998 / Accepted: January 18, 1999     

Effect of male age structure on reproduction in white-tailed deer

Selective harvest regimes that create female-biased sex ratios can potentially lead to delayed breeding, reduced breeding synchrony, reduced productivity, and a female-biased sex ratio of offspring. These resulting changes in breeding behavior and population dynamics have potential to adversely affect population growth. In 2002, Pennsylvania implemented harvest regulation changes that reduced deer density (increased harvest of antlerless deer) and increased the number and age of antlered deer (implemented antler point restriction regulations) that resulted in a less female-biased sex ratio. We monitored date of conception, productivity (embryos/female), and sex ratio of embryos during 1999–2006 to test if timing of breeding occurred earlier and with greater synchrony, if productivity of females increased, and if the sex ratio of offspring would shift towards more males. Deer density decreased 23% and the adult (≥1.5 yr old) sex ratio declined from 2.30 to 1.95 females/male. The ratio of ≥2.5-year-old to 1.5-year-old males shifted towards more older males (1:3.7 in 2002 to 1:1.59 in 2006) and the ≥2.5-year-old male population increased from 41,853 during 1999–2001 to 54,064 by 2006. We found no evidence of any change in the timing or variability of date of conception, productivity, or offspring sex ratio. We conclude that harvest regulation changes implemented in Pennsylvania, USA, were insufficient to affect timing of breeding or population dynamics and that efforts by managers to identify a desired sex ratio or manipulate sex ratios to achieve management goals on a statewide scale will be challenging. © 2019 The Wildlife Society.     

Sex allocation in haplodiploids is mediated by egg size: evidence in the spider mite Tetranychus urticae Koch

Haplodiploid species display extraordinary sex ratios. However, a differential investment in male and female offspring might also be achieved by a differential provisioning of eggs, as observed in birds and lizards. We investigated this hypothesis in the haplodiploid spider mite Tetranychus urticae, which displays highly female-biased sex ratios. We show that egg size significantly determines not only larval size, juvenile survival and adult size, but also fertilization probability, as in marine invertebrates with external fertilization, so that female (fertilized) eggs are significantly larger than male (unfertilized) eggs. Moreover, females with on average larger eggs before fertilization produce a more female-biased sex ratio afterwards. Egg size thus mediates sex-specific egg provisioning, sex and offspring sex ratio. Finally, sex-specific egg provisioning has another major consequence: male eggs produced by mated mothers are smaller than male eggs produced by virgins, and this size difference persists in adults. Virgin females might thus have a (male) fitness advantage over mated females.     

Maternal influences on offspring phenotypes and sex ratios in a multi‐clutching lizard with environmental sex determination

Maternal and environmental factors are important sources of phenotypic variation because both factors influence offspring traits in ways that impact offspring and maternal fitness. The present study explored the effects of maternal factors (maternal body size, egg size, yolk‐steroid allocation, and oviposition‐site choice) and seasonally‐variable environmental factors on offspring phenotypes and sex ratios in a multi‐clutching lizard with environmental sex determination (Amphibolurus muricatus). Maternal identity had strong effects on offspring morphology, but the nature of maternal effects differed among successive clutches produced by females throughout the reproductive season (i.e. maternal identity by environment interactions). The among‐female and among‐clutch variation in offspring traits (including sex ratios) was not mediated through maternal body size, egg size, or variation in yolk steroid hormones. This lack of nongenetic maternal effects suggests that phenotypic variation may be generated by gene by environment interactions. These results demonstrate a significant genetic component to variation in offspring phenotypes, including sex ratios, even in species with environmental sex determination. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 256–266.     

Stochastic effects in LMC models.

LMC (local mate competition) was first introduced by W. D. Hamilton to explain extraordinary female-biased sex ratios observed in a variety of insects and mites. In the original model, the population is subdivided into an infinite number of colonies founded by a fixed number of inseminated females producing the same very large number of offspring. The male offspring compete within the colonies to inseminate the female offspring and then these disperse at random to found new colonies. An unbeatable sex ratio strategy is found to be female-biased. In this paper, the effects of having colonies of random size and foundresses producing a random finite number of offspring are considered. The exact evolutionarily stable strategy (ESS) sex ratio is deduced and comparisons with previous approximate or numerical results are made. As the mean or the variance of brood size increases, the ESS sex ratio becomes more female-biased. An increase in the variance of colony size increases the ESS proportion of males when the mean brood size and colony size are both small, but decreases this proportion when the mean brood size or the mean colony size is large.     

Female choice for good genes and sex-biased broods in guppies

In a population of guppies Poecilia reticulata females were found to prefer large males and the offspring of these males had a higher survival rate than those sired by smaller males, suggesting that females were selecting their mates on the basis of their good genes. The possibility that females differentially invested in male or female offspring depending on the size or attractiveness of their mate was also investigated, but no relationship was found between a male's attractiveness or body size and the sex ratio of the offspring he sired. However, a strong female-biased sex ratio was detected in the broods and the proportion of males produced decreased with the amount of time that a female was confined with a male. The possible reasons for this are discussed.