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.     

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.     

Can the extremely female‐biased sex ratio of the social spider mites be explained by Hamilton’s local mate competition model?

Abstract.  1. Extremely female-biased sex ratios are known in the social spider mite species, Stigmaeopsis longus and S. miscanthi . Whether Hamilton's local mate competition (LMC) theory can explain such sex ratios was investigated.
2. Significant changes of the progeny sex ratios in the direction predicted by the LMC model were found in both species when the foundress number changed. Therefore, LMC can partly explain the skewed sex ratios in these species.
3. When the foundress number increased, the progeny sex ratio was still female biased and significantly different from the prediction of the LMC model for haplodiploidy. Relatedness between foundresses could not fully explain the female-biased sex ratios. Therefore, these results suggest that there are factors other than LMC skewing the sex ratios of these species toward female.     

Sex dimorphism of life-history traits and their response to environmental factors in spider mites

Sex dimorphism is ubiquitous in the animal kingdom and can be influenced by environmental factors. However, relatively little is known about how the degree and direction of sex difference vary with environmental factors, including food quality and temperature. With the spider mites from the family Tetranychidae as subjects, the sex difference of life-history traits in responses to host plant and temperature were determined in this meta-analytic review. Across the 42 studies on 26 spider mite species (N?=?8057 and 3922 for female and male mites, respectively), female spider mites showed longer developmental duration than the males in all except two species. The direction of sex difference in development was consistent regardless of temperature and host plant. The 16 spider mite species in 33 studies generally showed female-biased longevity, with an overall effect size of 0.6043 [95%CI = 0.4054–0.8031]. Host plant significantly influenced the sex difference in longevity, where the males lived longer than females below 22.5 ℃, but the reverse was true at higher and fluctuating temperature. Host plant also influenced the magnitude of sex difference in longevity, with females living longer than males when reared on herbs but not on trees. This study indicated that life-history traits are highly variable between sexes under temperature and host plant influence, highlighting that environmental conditions can significantly shape the direction and magnitude of sexual dimorphism of life-history traits.

     

The effect of interspecific mating on sex ratios in the twospotted spider mite and the Banks grass mite (Acarina: Tetranychidae)

Mixed populations of the twospotted spider mite (TSM),Tetranychus urticae (Koch), and the Banks grass mite (BGM),Oligonychus pratensis (Banks), occur on corn and sorghum plants in late summer in the Great Plains. Interspecific matings between these arrhenotokous species occur readily in the laboratory but yield no female offspring. The effect of interspecific mating on female: male sex ratios was measured by examining the F₁ progeny of females that mated with both heterospecific and conspecific males in no-choice situations. TSM females that mated first with BGM males and then with TSM males produced a smaller percentage of female offspring than TSM females that mated only with TSM males (43.1±5.8 and 78.9±2.8% females, respectively). Similarly, BGM females mated with heterospecific males and then with conspecific males produced fewer female offspring than females mated only with BGM males (55.7±5.2 and 77.5±2.5%, respectively). Lower female: male sex ratios were produced also by BGM females that mated with TSM males after first mating with conspecifics (62.4±3.4%). In mixed populations containing males of both species, females also produced lower female: male sex ratios, but these ratios were not as low as expected based on mating propensities and progeny sex ratios observed in no-choice tests. These data suggest that interspecific mating may substantially reduce female fitness in both mite species by reducing the output of female offspring, but in mixed populations this effect is mitigated by unidentified behavioral mechanisms.     

Temperature-induced changes in spider mite fitness: offsetting effects of development time, fecundity, and sex ratio

Temperature affects many life history parameters in poikilotherms. Temperature clearly affects development time and fecundity, which affect the intrinsic rate of increase. In haplodiploid mites, ambient temperature may also affect offspring sex ratio which, in turn, affects intrinsic rate of increase. The combined effect of all these processes determines the fitness of individual females. However, sex ratio also affects mating structure and, potentially, rate of local adaption. We investigated the direct effect of temperature variation on sex ratio, development time, and fecundity in the twospotted spider mite (Tetyranychus urticae), and calculated the effect of their interaction on mite intrinsic rate of increase. We conducted experiments at 2 temperatures and designed the experiment to separate pre-adult and adult sensitivity to temperature variation. Mites were reared from eggs to adult ecdysis at either 22°C or 32°C. Upon emergence as adults, these 2 groups were each split between 22°C and 32°C and allowed to oviposit. Not surprisingly, development from egg to adult was accelerated when mites were exposed to the higher temperature during offspring development, regardless of the temperature experienced by the mother during her development. Fecundity and the proportion of female offspring were affected by temperature only when mothers were exposed during both development and oviposition. About 12 offspring were gained and female bias was increased by 26% when the mother's development occurred at 22°C, whereas oviposition at 22°C added only 6 more offspring and increased female bias by only 7%. There was no correlation between sex ratio and fecundity; both were related to temperature but not to each other. Furthermore, development time, not fecundity or sex ratio, appeared to the main factor affecting the intrinsic rate of increase. Our results support other evidence that sex ratio varies independently of development time and fecundity.     

Precise, highly female-biased sex ratios in a social spider

It has been recognized for some time that the risk of producing maleless clutches should select for a lower than binomial variance in the sex ratio of organisms with female-biased sex ratios, small clutches and breeding groups containing the clutch of a single female. However, to date, precise sex ratios have only been reported for organisms with haplodiploid sex determination, a system which allows direct control of the sex of individual offspring. In contrast, under heterogametic sex determination chance is expected to play a crucial role in determining the sex composition of any one family, in particular when males are the heterogametic sex. Here, we present evidence of precise or underdispersed primary sex ratios in the Neotropical social spider Anelosimus domingo Levi. We show that this diplodiploid species with male heterogamety has not only beaten the odds of meiosis by producing mostly daughters, but has also attained relative precision in the proportion of sons and daughters produced in any one clutch. The latter finding suggests the existence of mechanisms that allow sorting of the two types of sperm in this spider species.     

Cold storage of the predatory mite Neoseiulus californicus is improved by pre-storage feeding on the diapausing spider mite Tetranychus urticae

Low air temperature accompanied with high humidity is effective for long-term cold storage of the predatory mite Neoseiulus californicus (McGregor) (Acari: Phytoseiidae). To further improve this storage method, we investigated the effect of pre-storage nutrition on survival during storage and on post-storage quality in terms of survival, oviposition, and progeny viability. The predatory mite was fed from the egg to adult stage on the diapausing two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), non-diapausing spider mites, or Japanese pear pollen, Pyrus pyrifolia Nakai. Newly emerged N. californicus adult females and males were mated, and then both were stored at 7.5 °C and a vapor pressure deficit of 0.0 kPa for up to 75 days. Survival during storage and post-storage quality was significantly better with the diapausing spider mite diet than with the other diets. No effects on the survival or sex ratio of the progeny of the stored adults were observed, regardless of diet or storage duration. Providing diapausing spider mites as a pre-storage diet therefore significantly improves the long-term storage of N. californicus. We discuss the possibility that ingestion of the cryoprotectants, antioxidants, and energy reserves that are present in rich amounts in diapausing spider mites mitigates chilling injury.     

Maternal correlates of brood sex ratio variation in the lekking lance-tailed manakin Chiroxiphia lanceolata

Theory predicts that overall population sex ratios should be around parity. But when individual females can receive higher fitness from offspring of one sex, they may benefit by biasing their brood sex ratios accordingly. In lekking species, higher variance in male reproductive success relative to that of females predicts that male offspring gain disproportionately from favorable rearing conditions. Females should therefore produce male-biased broods when they are in a position to raise higher quality offspring: i.e., in better body condition or when they reproduce earlier in the breeding season. To investigate these hypotheses, we studied brood sex ratios of lance-tailed manakins Chiroxiphia lanceolata . We found that overall sex ratios and mean brood sex ratios were not different from random expectation. Brood sex ratios were not related to laying date or female body condition. However, we detected a quadratic relationship between brood sex ratios and maternal age: both young (1–2 years) and old (8+ years) females produced female-biased brood sex ratios. This relationship was most clear in a year also distinguished by early rainy and breeding seasons. We suggest that breeding inexperience in young females and senescence in older females is the most plausible explanation for these results, and that the relationship between female age and brood sex ratio is mediated by environmental conditions.     

Male demographic constraints to extreme sex ratio in the twospotted spider mite

Summary Twospotted spider mites, Tetranychus urticae Koch are arrhenotokous. As a result of this genetic structure, primary and secondary sex ratios diverge from the 1:1 female:male ratio commonly found in diploid systems. Ratios vary, but 3:1 is the most common. The influence of life history parameters on spider mite sex ratio is unclear, although maternal genetic effects, resource quality and maternal age are known to play a role. An area that has not been studied is the relationship between male reproductive capabilities and spider mite sex ratio. A prior study on male reproduction in spider mites suggests that males have far too high a reproductive capacity to explain sex ratio patterns, but that study was not conducted under realistic mating conditions. Thus, this study was conducted to determine if there is a link between male reproduction and spider mite sex ratio. This was done by exposing males to various exposure regimes of females and recording the number of copulations, inseminations and daughters fathered by each male. Results include the following: i) males are most virile when one day old; ii) virgin males become nearly completely devoid of sperm (or other copulatory products) after about 15 matings and then take about four days to recover; and iii) the optimal number of matings per day (defined as that which produces the greatest number of daughters in the least number of inseminations) is four females per day. The principle conclusion is that although males have a high potential reproductive output, insemination quality is only high for the first four or five matings each day. Therefore, to ensure full inseminations of all daughters by sons, females are constrained to producing primary sex ratios of about 5:1 or less.     

Sex-specific effects of hybridization on reproductive fitness in Mytilus

Blue mussels of the genus Mytilus form extensive hybrid zones in the North Atlantic and elsewhere where the distributions of different species overlap. Mytilus species transmit both maternal and paternal mtDNA through egg and sperm, respectively, a process known as doubly uniparental inheritance (DUI), and some females produce offspring with extremely biased sex ratios. These two traits have been shown to be linked and maternally controlled, with sex determination involving nuclear–cytoplasmic interactions. Hybridization has been shown to disrupt DUI mitochondrial inheritance and sex ratio bias; however, the effect of hybridization on reproductive fitness has not previously been examined. We investigated this effect in M. edulis × M. trossulus crosses through histological examination of mature F1 progeny, and spawning of F1 hybrids to monitor survival of their progeny through to the D stage of larval development. For progeny produced from mothers with a strong bias toward female offspring (often 100%) in pure-bred crosses, there was a clear breakdown in female dominance of progeny and significantly more hermaphrodites in the hybrid crosses produced from sperm with the M-tr1 mitotype. We also found significant sex-specific differences among hybrid progeny, with females producing normal eggs while males and hermaphrodites evidenced impaired gonadal development with significantly greater numbers of Sertoli cells, phagocytic hemocytes, and degenerating germ cells, all associated with gonad resorption. Males from crosses where DUI was disrupted and where male progeny were homoplasmic for the female mtDNA were the most severely compromised. Allelic incongruity between maternal and paternal mitotypes in hybrid crosses was associated with significant disruption of male gonadal development.     

Host parasitoid interactions affecting reproduction and oviposition byBrachymeria intermedia [Hym.: Chalcididae]

A maximum number of 6 parasitoid progeny are produced byBrachymeria intermedia (Nees) females, in a 24 h period, even when more than 6 hosts are available. The number of progeny produced by ovipositing females kept at a high temperature or high light intensity is greater than that of females kept at low temperatures or low light intensity. Host size and age of female parasitoids affect the sex ratio or progeny. Parasitism of small pupal hosts results in the production of a greater proportion of male progeny. Increasing maternal age appears to increase the proportion of males.     

Calcium Availability Influences Litter Size and Sex Ratio in White-Footed Mice (Peromyscus leucopus)

The production of offspring typically requires investment of resources derived from both the environment and maternal somatic reserves. As such, the availability of either of these types of resources has the potential to limit the degree to which resources are allocated to reproduction. Theory and empirical studies have argued that mothers modify reproductive performance relative to exogenous resource availability and maternal condition by adjusting size, number or sex of offspring produced. These relationships have classically been defined relative to availability of energy sources; however, in vertebrates, calcium also plays a critical role in offspring production, as a considerable amount of calcium is required to support the development of offspring skeleton(s). We tested whether the availability of calcium influences reproductive output by providing female white-footed mice with a low-calcium or standard diet from reproductive maturity to senescence. We then compared maternal skeletal condition and reproductive output, based on offspring mass, offspring number and litter sex ratio, between dietary treatments. Mothers on the low-calcium diet exhibited diminished skeletal condition at senescence and produced smaller and strongly female-biased litters. We show that skeletal condition and calcium intake can influence sex ratio and reproductive output following general theoretical models of resource partitioning during reproduction.     

GENETIC AND ENVIRONMENTAL BASIS OF VARIABLE SEX RATIOS IN LABORATORY STRAINS OF POECILIOPSIS LUCIDA

Skewed sex ratios are common among several species of Poeciliopsis, a viviparous fish from northwestern Mexico. Since previous, unrelated studies from this laboratory (Angus and Schultz, 1983) suggested that deviation from a 1:1 sex ratio might be influenced by temperature, two inbred strains of P. lucida were tested for temperature-dependent sex determination by comparing sex ratios of offspring from pregnant females held at different water temperatures. Different sex ratios were produced by the two strains at the same temperature: one strain produced almost all-male offspring at 30°C and female-biased sex ratios at 24°C, while the other strain produced a 1:1 sex ratio at both temperatures. At intermediate temperatures, the labile strain produced sequentially fewer males with decreasing temperatures. The other strain produced a consistent sex ratio regardless of temperature. Poeciliopsis lucida apparently has a genetic polymorphism for temperature-influenced sex determination. An hypothesis is offered for the evolutionary origin of environmental sex determination.     

Effects of 17-beta-estradiol treatment of female zebra finches on offspring sex ratio and survival

Treatment of female zebra finches (Taeniopygia guttata) with 17-beta-estradiol leads to a female-biased sex ratio in their offspring at the age of independence [Horm. Behav. 35 (1999) 135]. It is unclear whether this is due to a bias of the primary sex ratio or to sex-specific survival. We replicated this experiment and found again a significantly higher total number of daughters than sons at independence in the estradiol-treated group. This was due to higher embryonic survival of daughters compared with sons in the estradiol-treated group and the reverse in the control group. There was no effect of the hormone treatment on the primary sex ratio. Treatment with 17-beta-estradiol led to a significantly shorter hatching time and to heavier offspring at day 7 after hatching. This weight was correlated with maternal plasma estradiol levels on the day of the first egg, which were significantly higher in the estradiol-treated group than in the control group. The results do not support the idea that maternal estradiol levels influence the primary sex ratio. They indicate that maternal estradiol differentially affects survival of sons and daughters via an influence on the embryonic environment, possibly enhancing offspring growth.     

Effects of 17-β-estradiol treatment of female zebra finches on offspring sex ratio and survival

Treatment of female zebra finches (Taeniopygia guttata) with 17-beta-estradiol leads to a female-biased sex ratio in their offspring at the age of independence [Horm. Behav. 35 (1999) 135]. It is unclear whether this is due to a bias of the primary sex ratio or to sex-specific survival. We replicated this experiment and found again a significantly higher total number of daughters than sons at independence in the estradiol-treated group. This was due to higher embryonic survival of daughters compared with sons in the estradiol-treated group and the reverse in the control group. There was no effect of the hormone treatment on the primary sex ratio. Treatment with 17-beta-estradiol led to a significantly shorter hatching time and to heavier offspring at day 7 after hatching. This weight was correlated with maternal plasma estradiol levels on the day of the first egg, which were significantly higher in the estradiol-treated group than in the control group. The results do not support the idea that maternal estradiol levels influence the primary sex ratio. They indicate that maternal estradiol differentially affects survival of sons and daughters via an influence on the embryonic environment, possibly enhancing offspring growth.     

Sex ratio, mating behaviour and Wolbachia infections in a sheetweb spider

The solitary sheetweb spider Pityohyphantes phrygianus has a female-biased primary sex ratio. Earlier studies have indicated that female post-copulatory position may influence the degree of bias, but the adaptive significance of the departure from a Fisherian 1 : 1 sex ratio is not known. In this study we show that there is a significant relationship between abdominal position and offspring sex ratio in undisturbed females. Moreover, female mating behaviour (and thus sex ratio) is correlated with female size, but this relationship may shift from negative to positive depending on the presence of the maternally acquired endosymbiotic bacterium Wolbachia in both sexes. A survey of wild-caught individuals shows that the incidence of Wolbachia infection in natural populations is high. This indicates that Wolbachia may be a significant factor influencing female post-copulatory behaviour and sex ratio in natural populations. We discuss various adaptive reasons for sex-ratio bias and behavioural plasticity in females.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 181–186.     

Loss of sex-allocation plasticity in the predatory mite Metaseiulus occidentalis and possible triggering cues

In two recent studies, we showed that females from a long-established Metaseiulus (Typhlodromus or Galendromus) occidentalis laboratory colony reared under crowded conditions for approximately 27 years produced equal numbers of male and female progeny. This contrasts with our previous results that showed the females from the same colony produced progeny with a female-biased sex ratio. These discrepant findings raised the possibility that dense rearing conditions can affect the sex-allocation plasticity in this important biological control agent. In the current study, we show that females from a newly collected M. occidentalis colony initially were capable of producing progeny with a female-biased sex ratio, but lost this ability over a 12-month period (43 generations) when reared under dense rearing conditions and provided with damaged prey. We demonstrate that females from this newly collected colony initially could adjust offspring sex ratio in response to both conspecific cues and cues produced by their damaged prey. The results suggest that dense rearing conditions, which are often used in commercial rearing facilities, may have detrimental effects on the reproductive fitness of M. occidentalis and, possibly, other predatory mites.     

Temperature-dependent fumigant activity of essential oils against twospotted spider mite (Acari: Tetranychidae)

Fumigant activity of 34 commercial essential oils was assessed on female adults and eggs of twospotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae) at three temperatures (5, 15, and 25 degrees C). Common thyme, cinnamon, and lemongrass oils were equally effective on twospotted spider mite adults showing 85.8-100% mortality at 5 and 10 microl/liter air at 25 degrees C. At a lower temperature of 15 degrees C, lemongrass and peppermint resulted in > or =90% mortality of adults at 10 microl/liter air. Only lemongrass was relatively active at 5 microl/liter air, at 15 degrees C. At 5 degrees C, lemongrass and peppermint caused significantly higher adult mortality than controls but only at 10 microl/liter air. Common thyme oil showed the highest ovicidal activity at 5 microl/liter air at 25 degrees C. Among the main components of common thyme and lemongrass oils, citral was lethal to twospotted spider mite adults at all tested temperatures. Carvacrol, thymol, and citral caused the same inhibitory effects on the hatch of twospotted spider mite eggs at 25 degrees C. However, citral was more active than other compounds to twospotted spider mite eggs at 15 degrees C. Therefore, we conclude that citral has the best potential for development as a fumigant against twospotted spider mite on agricultural products harvested late in the growing season.     

Population sex ratios under differing local climates in a reptile with environmental sex determination

Populations that experience different local climates, such as those along a latitudinal gradient, must match life history traits to local environmental conditions. In species with temperature-dependent sex determination, such as many reptiles, population sex ratio is strongly influenced by local climate, yet local climate differs substantially among populations in geographically-widespread species. We studied the painted turtle at three sites across the species’ geographic range to gain a mechanistic understanding of how sex ratios are produced under different local climates. We combined data on maternal nest-site choice, nest incubation temperature, and the resultant offspring sex ratio of populations across a climatic gradient, to demonstrate how geographic variation in behavior and physiology translates into sex ratios among populations of a widely-distributed species. We found that populations across the species’ geographic range match incubation conditions with local climatic conditions through population-specific adjustment of maternal nest-site choice. Incubation temperatures during the thermosensitive period were cooler and clutches were more male-biased in the south, with populations farther north having warmer incubation temperatures and more female-biased sex ratios, yet adult sex ratios were not strongly biased in any population. Most components of maternal nest-site choice varied latitudinally among populations, suggesting that the species may have a considerable repertoire for responding to climate change through adjustment of nest-site choice.