Female-biased Offspring Sex Ratios Research Articles

Heatwaves are detrimental to fertility in the viviparous tsetse fly.

Heatwaves are increasing in frequency and intensity due to climate change, pushing animals beyond physiological limits. While most studies focus on survival limits, sublethal effects on fertility tend to occur below lethal thresholds, and consequently can be as important for population viability. Typically, male fertility is more heat-sensitive than female fertility, yet direct comparisons are limited. Here, we measured the effect of experimental heatwaves on tsetse flies, Glossina pallidipes, disease vectors and unusual live-bearing insects of sub-Saharan Africa. We exposed males or females to a 3-day heatwave peaking at 36, 38 or 40°C for 2 h, and a 25°C control, monitoring mortality and reproduction over six weeks. For a heatwave peaking at 40°C, mortality was 100%, while a 38°C peak resulted in only 8% acute mortality. Females exposed to the 38°C heatwave experienced a one-week delay in producing offspring, whereas no such delay occurred in males. Over six weeks, heatwaves resulted in equivalent fertility loss in both sexes. Combined with mortality, this lead to a 10% population decline over six weeks compared to the control. Furthermore, parental heatwave exposure gave rise to a female-biased offspring sex ratio. Ultimately, thermal limits of both survival and fertility should be considered when assessing climate change vulnerability.

No room for males in caves: Female-biased sex ratio in subterranean amphipods of the genus Niphargus.

Sex allocation theory predicts that the proportion of daughters to sons will evolve in response to ecological conditions that determine the costs and benefits of producing each sex. All else being equal, the adult sex ratio (ASR) should also vary with ecological conditions. Many studies of subterranean species reported female-biased ASR, but no systematic study has yet been conducted. We test the hypothesis that the ASR becomes more female-biased with increased isolation from the surface. We compiled a data set of ASRs of 35species in the subterranean amphipod Niphargus, each living in one of three distinct habitats (surface-subterranean boundary, cave streams, phreatic lakes) representing an environmental gradient of increased isolation underground. The ASR was female-biased in 27 of 35species; the bias was statistically significant in 12species. We found a significant difference in the ASR among habitats after correction for phylogeny. It is most weakly female-biased at the surface-subterranean boundary and most strongly female-biased in phreatic lakes. Additional modelling suggests that the ASR has evolved towards a single value for both surface-subterranean boundary and cave stream-dwelling species, and another value for 9 of 11 phreatic lake dwellers. We suggest that a history of inbreeding in subterranean populations might lower inbreeding depression such that kin selection favours mating with siblings. This could select for a female-biased offspring sex ratio due to local mate competition among brothers. The observed patterns in sex ratios in subterranean species make them a group worthy of more attention from those interested in sex allocation theory.

A solution to a sex ratio puzzle in Melittobia wasps

The puzzling sex ratio behavior of Melittobia wasps has long posed one of the greatest questions in the field of sex allocation. Laboratory experiments have found that, in contrast to the predictions of theory and the behavior of numerous other organisms, Melittobia females do not produce fewer female-biased offspring sex ratios when more females lay eggs on a patch. We solve this puzzle by showing that, in nature, females of Melittobia australica have a sophisticated sex ratio behavior, in which their strategy also depends on whether they have dispersed from the patch where they emerged. When females have not dispersed, they lay eggs with close relatives, which keeps local mate competition high even with multiple females, and therefore, they are selected to produce consistently female-biased sex ratios. Laboratory experiments mimic these conditions. In contrast, when females disperse, they interact with nonrelatives, and thus adjust their sex ratio depending on the number of females laying eggs. Consequently, females appear to use dispersal status as an indirect cue of relatedness and whether they should adjust their sex ratio in response to the number of females laying eggs on the patch.

Consequences of population structure for sex allocation and sexual conflict.

Both sex allocation and sexual conflict can be modulated by spatial structure. However, how the interplay between the type of dispersal and the scale of competition simultaneously affects these traits in sub-divided populations is rarely considered. We investigated sex allocation and sexual conflict evolution in meta-populations of the spider mite Tetranychus urticae evolving under budding (pairing females from the same patch) or random (pairing females from different patches) dispersal and either local (fixed sampling from each subpopulation) or global (sampling as a function of subpopulation productivity) competition. Females evolving under budding dispersal produced less female-biased offspring sex ratios than those from the random dispersal selection regimes, contradicting theoretical predictions. In contrast, the scale of competition did not strongly affect sex allocation. Offspring sex ratio and female fecundity were unaffected by the number of mates, but female fecundity was highest when their mates evolved under budding dispersal, suggesting these males inflict less harm than those evolving under random dispersal. This work highlights that population structure can impact the evolution of sex allocation and sexual conflict. Moreover, selection on either trait may reciprocally affect the evolution of the other, for example via effects on fecundity.

Effects of exposure time and ratio of irradiated larvae from three medfly strains on progeny yield in Diachasmimorpha longicaudata (Hymenoptera: Braconidae) mass rearing

ABSTRACTAn augmentative biological control strategy against Ceratitis capitata (= medfly) in fruit-producing irrigated-valleys of San Juan, central-western Argentina, has been recently implemented by the San Juan Fruit Fly Control and Eradication Program. The Asian-native parasitoid Diachasmimorpha longicaudata is currently reared at the San Juan Medfly and Parasitoids Mass Rearing Facility for this purpose. In this regard, the objective of this study was to evaluate adult emergence and offspring sex ratio to improve parasitoid production. Three medfly strains at different host larvae densities and exposure times to female parasitoids were assessed. Prevalence of superparasitism was also considered. Three parasitoid population lines were used in the trials: one reared on medfly larvae of the Vienna-8 temperature-sensitive lethal (tsl) genetic sexing strain without inversion, and the other two on larvae of biparental medfly strains native to San Juan (central-western Argentina) and Tucumán (northwestern Argentina). Gamma-irradiated 6 d-old larvae (early third-instars) of each medfly strain were exposed to parasitoids for 30, 60, 90, and 120 min at 3:1, 6:1, and 9:1 host/parasitoid ratios. The Vienna-8 C. capitata strain was as efficient in producing parasitoids as both biparental native strains. Medfly larvae exposed to 10 female parasitoids for a relatively long time (1.30 hrs) at a high ratio (6–9:1) of host to parasitoid were enough to achieve the highest mean adult emergence (50–60%) and a female-biased offspring sex ratio. Superparasitism positively influenced female parasitoid production. These findings may be used to develop a more cost-effective mass rearing method for D. longicaudata.

Combining predictions of sex ratio and mate choice models: pheromone-mediated mate choice by females in a parasitoid wasp

Abstract In haplodiploid species, daughter production, but not son production, is sexual, requiring paternal contributions. Females may use male signals to choose a mate with better daughter-production potential, if the choice facilitates her production of adaptive sex ratios, e.g., female-biased sex ratios in systems operating under local mate competition (LMC). In the parasitoid wasp Urolepis rufipes, females preferred pheromone markings from males that had mated once versus multiply, were young rather than old, and were uninfected rather than infected when infection was low, but not when infection was high. Mates of singly-mated males had more female-biased offspring sex ratios than those of multiply-mated males, whereas there was no difference for mates of young versus old males. Thus, female preference for singly-mated males appears to provide indirect fitness benefits. A preference for young males, was not beneficial in the laboratory, but in nature young males may have mated less.

Offspring sex ratio shifts of the solitary parasitoid wasp, Trichopria drosophilae (Hymenoptera: Diapriidae), under local mate competition

Localmate competition (LMC) models predict a female-biased offspring sex ratio when a single foundress oviposits alone in a patch and an increasing proportion of sons with increasing foundress number. We tested whether the solitary pupal parasitoid, Trichopria drosophilae (Hymenoptera: Diapriidae), adjusted offspring sex ratio with foundress number when parasitizing Drosophila melanogaster pupae. Mean number of female offspring was higher than that of males, with a male proportion of 26 ± 16% when only one foundress oviposited. However, male proportion reached 58 ± 26%, 48 ± 22%, and 51 ± 19% in three-, five and seven-foundress cohorts. That the male proportion of offspring increased with foundress number is consistent with LMC models.

Functional response of Diachasmimorpha longicaudata (Ashmead) over Ceratitis capitata (Wiedemann): Influence of temperature, fruit location and host density

To establish a successful Biological Control (BC) program, exotic parasitoids should be proven to be targeted species, capable of surviving in a new environment, inducing pest population reduction. Moreover, to achieve this aim, imported exotic parasitoids should usually adapt to a new host (the target pest), which usually results in practical improvements. The determination of the functional response of the imported parasitoid was recognized as a key requirement prior to its introduction. In this work, we determined the functional response of the parasitoids, Diachasmimorpha longicaudata, against the medfly, Ceratitis capitata, under two different scenarios, one in the laboratory and another in the greenhouse. In both scenarios, we determined D. longicaudata parasitism percentage, fertility, sex ratio, and induced host mortality, considering temperature, fruit location, and host density.In laboratory conditions, when the medfly host larvae were provided within an artificial diet, our results demonstrated that the two different temperature ranges (20–24 and 25–29 °C) were suitable for the activities and development of D. longicaudata. Parasitism, fertility, and medfly population reduction corresponded to a Type II functional response with a male-biased offspring sex-ratio (♀♀/♂♂+♀♀; 33–46%), while induced mortality decreased with an increase in host density. Similarly, when the hosts were provided inside fruits, parasitism and fertility also corresponded to a Type II functional response, and the offspring sex ratio was also male-biased (34–37%). However, in greenhouse conditions, our results showed no significant differences regarding fruit position. For host density, the only significant differences were found for fertility and a slightly female-biased offspring sex-ratio at higher ratios (38–58%) with the same Type II response, as in laboratory conditions.The information reported here about the key demographic parameters and the functional response of D. longicaudata using C. capitata as its host under various environments and situations will assist in the evaluation of its potential as a biological control agent against this pest. Our results show that this parasitoid can search efficiently for host individuals even at low host densities, irrespectively of their spatial location (infested fruits in the canopy or as ripened fruits fallen to the ground) or independently of the temperature of the environment.

Breeding sex ratio and population size of loggerhead turtles from Southwestern Florida.

Species that display temperature-dependent sex determination are at risk as a result of increasing global temperatures. For marine turtles, high incubation temperatures can skew sex ratios towards females. There are concerns that temperature increases may result in highly female-biased offspring sex ratios, which would drive a future sex ratio skew. Studying the sex ratios of adults in the ocean is logistically very difficult because individuals are widely distributed and males are inaccessible because they remain in the ocean. Breeding sex ratios (BSR) are sought as a functional alternative to study adult sex ratios. One way to examine BSR is to determine the number of males that contribute to nests. Our goal was to evaluate the BSR for loggerhead turtles (Caretta caretta) nesting along the eastern Gulf of Mexico in Florida, from 2013–2015, encompassing three nesting seasons. We genotyped 64 nesting females (approximately 28% of all turtles nesting at that time) and up to 20 hatchlings from their nests (n = 989) using 7 polymorphic microsatellite markers. We identified multiple paternal contributions in 70% of the nests analyzed and 126 individual males. The breeding sex ratio was approximately 1 female for every 2.5 males. We did not find repeat males in any of our nests. The sex ratio and lack of repeating males was surprising because of female-biased primary sex ratios. We hypothesize that females mate offshore of their nesting beaches as well as en route. We recommend further comparisons of subsequent nesting events and of other beaches as it is imperative to establish baseline breeding sex ratios to understand how growing populations behave before extreme environmental effects are evident.

When invasive ants meet: effects of outbreeding on queen performance in the tramp ant Cardiocondyla itsukii.

Most disturbed habitats in the tropics and subtropics harbor numerous species of invasive ants, and occasionally the same species has been introduced repeatedly from multiple geographical sources. We examined how experimental crossbreeding between sexuals from different populations affects the fitness of queens of the tramp ant Cardiocondyla itsukii, which is widely distributed in Asia and the Pacific Islands. Eggs laid by queens that mated with nestmate males had a higher hatching rate than eggs laid by queens mated to males from neighboring (Hawaii × Kauai) or distant introduced populations (Hawaii/Kauai × Okinawa). Furthermore, inbreeding queens had a longer lifespan and produced a less female-biased offspring sex ratio than queens from allopatric mating. This suggests that the genetic divergence between different source populations may already be so large that in case of multiple invasions eventual crossbreeding might negatively affect the fitness of tramp ants.

Interspecific interference in the closely related predatory mites Neoseiulus womersleyi and Neoseiulus longispinosus (Acari: Phytoseiidae)

ABSTRACTReproductive interference is known to occur in the morphologically similar species Neoseiulus womersleyi and Neoseiulus longispinosus: crosses between N. longispinosus females and N. womersleyi males produce (a few) female offspring, reciprocal crosses produce only male offspring. Details of the interspecific reproduction process remain largely unknown. In this article, we investigated intraspecific and interspecific crosses, spermathecal vesicles and spermatophores in females, and molecular identification of F1 hybrids based on the internal transcribed spacer (ITS) region of nuclear ribosomal RNA (rRNA). The copulation times of interspecific crosses were similar to those of intraspecific crosses, yet interspecific crosses between N. womersleyi females and N. longispinosus males exhibited extremely low fecundity with no female offspring. On the other hand, 1 out of 35 reciprocal crosses produced viable, but sterile female offspring (F1). Intraspecific crosses of N. womersleyi and N. longispinosus showed female-biased offspring sex ratios. Most N. womersleyi females (12 out of 15 females tested) that mated with N. longispinosus males had inflated vesicle(s) and were inseminated. Of the crosses between N. longispinosus females and N. womersleyi males, 14 pairs had neither inflated spermathecal vesicles nor were inseminated, and in only one pair, vesicles were inflated and insemination occurred that enabled the production of female offspring. Polymerase chain reaction products of the ITS region of rRNA gene digested with ClaI exhibited two fragments (361 and 278 bp) for the N. womersleyi and only a single fragment (642 bp) for the N. longispinosus, whereas three fragments for the F1 hybrids (642, 361, and 278 bp), confirming the identification. Our results confirmed the asymmetric reproductive interference between N. womersleyi and N. longispinosus and demonstrated that the F1 female offspring produced were (sterile) hybrids.

Population viability at extreme sex-ratio skews produced by temperature-dependent sex determination.

For species with temperature-dependent sex determination (TSD) there is the fear that rising temperatures may lead to single-sex populations and population extinction. We show that for sea turtles, a major group exhibiting TSD, these concerns are currently unfounded but may become important under extreme climate warming scenarios. We show how highly female-biased sex ratios in developing eggs translate into much more balanced operational sex ratios so that adult male numbers in populations around the world are unlikely to be limiting. Rather than reducing population viability, female-biased offspring sex ratios may, to some extent, help population growth by increasing the number of breeding females and hence egg production. For rookeries across the world (n = 75 sites for seven species), we show that extreme female-biased hatchling sex ratios do not compromise population size and are the norm, with a tendency for populations to maximize the number of female hatchlings. Only at extremely high incubation temperature does high mortality within developing clutches threaten sea turtles. Our work shows how TSD itself is a robust strategy up to a point, but eventually high mortality and female-only hatchling production will cause extinction if incubation conditions warm considerably in the future.

The Maternal Legacy: Female Identity Predicts Offspring Sex Ratio in the Loggerhead Sea Turtle.

In organisms with temperature-dependent sex determination, the incubation environment plays a key role in determining offspring sex ratios. Given that global temperatures have warmed approximately 0.6 °C in the last century, it is necessary to consider how organisms will adjust to climate change. To better understand the degree to which mothers influence the sex ratios of their offspring, we use 24 years of nesting data for individual female loggerhead sea turtles (Caretta caretta) observed on Bald Head Island, North Carolina. We find that maternal identity is the best predictor of nest sex ratio in univariate and multivariate predictive models. We find significant variability in estimated nest sex ratios among mothers, but a high degree of consistency within mothers, despite substantial spatial and temporal thermal variation. Our results suggest that individual differences in nesting preferences are the main driver behind divergences in nest sex ratios. As such, a female’s ability to plastically adjust her nest sex ratios in response to environmental conditions is constrained, potentially limiting how individuals behaviorally mitigate the effects of environmental change. Given that many loggerhead populations already show female-biased offspring sex ratios, understanding maternal behavioral responses is critical for predicting the future of long-lived species vulnerable to extinction.

A sex allocation cost to polyandry in a parasitoid wasp.

The costs and benefits of polyandry are central to understanding the near-ubiquity of female multiple mating. Here, we present evidence of a novel cost of polyandry: disrupted sex allocation. In Nasonia vitripennis, a species that is monandrous in the wild but engages in polyandry under laboratory culture conditions, sexual harassment during oviposition results in increased production of sons under conditions that favour female-biased sex ratios. In addition, females more likely to re-mate under harassment produce the least female-biased sex ratios, and these females are unable to mitigate this cost by increasing offspring production. Our results therefore argue that polyandry does not serve to mitigate the costs of harassment (convenience polyandry) in Nasonia. Furthermore, because males benefit from female-biased offspring sex ratios, harassment of ovipositing females also creates a novel cost of that harassment for males.

Fig wasps from the centre of figs have more chances to mate, more offspring and more female-biased offspring sex ratios

Pollinator fig wasps serve as useful empirical models for studies of sex ratio evolution because females adjust their offspring sex ratios in relation to the number of foundresses that share a fig. Placement of pollinator offspring within figs is not random and more centrally located flowers are more likely to support pollinator development. We compared components of fitness of female fig wasps developing in central and peripheral flowers and whether this influenced the sex ratios of their offspring. We used Ceratosolen solmsi marchali, a pollinator of the Asian dioecious fig tree, Ficus hispida. Mating frequency was determined from the number of mating holes in females' flowers. Most females mated once, but some had the opportunity to mate up to four times and multiple mating opportunities were more frequent among centrally located galls. Body size was not linked to flower location, although the females that mated most were significantly larger than others, and came from significantly larger galls. Females that had multiple mating opportunities produced more daughters but similar numbers of sons, resulting in more female-biased broods. These females are likely to have produced more offspring because of their larger size but may have also benefited from mating with more males. The results demonstrate that differences in the natal locations of foundresses can modify offspring sex ratios and obscure sex ratio adjustment in response to the number of foundresses sharing a fig.

Effect of Corticosterone and Hen Body Mass on Primary Sex Ratio in Laying Hen (Gallus gallus), Using Unincubated Eggs1

In various studies, chronic elevation of corticosterone levels in female birds under natural or experimental conditions resulted in female biased offspring sex ratios. In chicken, one study with injected corticosterone resulted in a male sex ratio bias. In the current study, we chronically elevated blood plasma corticosterone levels through corticosterone feeding (20 mg/kg feed) for 14 days using 30 chicken hens in each of treatment and control groups and studied the primary offspring sex ratio (here defined as the proportion of male fertile eggs determined in freshly laid eggs, i.e., without egg incubation). Mean plasma corticosterone concentrations were significantly higher in the treatment group but were not associated with sex ratio, laying rate, and fertility rate. Corticosterone treatment by itself did not affect egg sex but affected sex ratio as well as laying rate and fertility rate in interaction with hen body mass. Body mass had a negative association with sex ratio, laying rate, and fertility rate per hen in the corticosterone group, but a positive association with sex ratio in untreated hens. These interactions were already seen when taking the body mass at the beginning of the experiment, indicating intrinsic differences between light and heavy hens with regard to their reaction to corticosterone treatment. The effects on laying rate, fertility rate, and sex ratio suggest that some factor related to body mass act together with corticosterone to modulate ovarian functions. We propose that corticosterone treatment in conjunction with hen body mass can interfere with meiosis, which can lead to meiotic drive and to chromosomal aberrations resulting in postponed ovulation or infertile ova.

The Japanese ladybirds, Coccinula crotchi and Coccinula sinensis, are infected with very closely related strains of male‐killing Flavobacterium

Male-killing is 1 of 4 known strategies that inherited parasitic endosymbionts have evolved to manipulate their host's reproduction. In early male-killing, infected male offspring are killed early in embryogenesis. Within the Insecta, male-killing bacteria have been found in a wide range of hosts. The Coccinellidae families of beetles, better known as ladybirds, are particularly prone to male-killer invasion. In samples of the coccinellid, Coccinula crotchi, from Japan, a new male-killing bacterium was revealed by phenotypic assay. Molecular genetic analysis revealed the identity to be a tetracycline-sensitive Flavobacterium that causes female-biased offspring sex ratio. Furthermore, that Flavobacterium strain was found to be closely related to the Flavobacterium causing male-killing in the congeneric Japanese coccinellid, Coccinula sinensis, which was collected from the same region. However, we found slightly different Flavobacterium strains infecting C. sinensis from regions with different environmental conditions. This may be an indication of horizontal transmission of male-killing Flavobacterium between these 2 ladybird spices. Finally, environmental conditions may affect the spread of male-killing bacteria among their hosts.

Population size, not density, serves as a cue for sex ratio adjustments in polychaete worms

Local Mate Competition theory (LMC) predicts female-biased offspring sex ratios when mate competition occurs locally between siblings. The mating system of the marine polychaete worm Dinophilus gyrociliatus apparently fits LMC theory well. Females lay egg capsules with 3–6 large eggs (which produce females), and 1–2 small eggs (which produce males), resulting in female-biased sex ratios. However, mating occurs between larvae, inside egg capsules, and brothers fertilize sisters, possibly preventing any competition between unrelated males and obviating the need for sex ratio adjustments to local population size. Therefore, we tested whether mothers adjusted their offspring sex ratio to local population size, controlling for density. As predicted by LMC theory, sex ratios of single females were less male-biased than those of populations of multiple females, suggesting that males also compete with unrelated males. Sex ratio adjustments occurred irrespective of density, revealing sophisticated perception of the social environment in these worms.

Effects of female diet and age on offspring sex ratio of the solitary parasitoid Pachycrepoideus vindemmiae (Rondani) (Hymenoptera, Pteromalidae)

Effects of female diet and age on offspring sex ratio of the solitary parasitoid Pachycrepoideus vindemmiae (Rondani) (Hymenoptera, Pteromalidae). Theories predict that females of parasitoid wasps would adjust the offspring sex ratio to environmental conditions in the oviposition patch, but the diet and age of females would also affect the sex ratio adjustment. Our focus was to test the effects of female diet and age on offspring sex ratio of the solitary parasitoid wasp, Pachycrepoideus vindemmiae (Rondani, 1875). Our results showed that females fed with honey had significantly less female biased offspring sex ratio than those fed only with water. Offspring sex ratio (male percentage) decreased with female age or female longevity at the beginning of oviposition but increased at the end. There should be a sperm limitation in P. vindemmiae females at the end of oviposition, and a higher frequency of unfertilized eggs were laid then. Females also laid more unfertilized eggs at the beginning of oviposition, which would be necessary to insure the mating among offspring. Male offspring developed faster and emerged earlier, which would also reduce the risk of virginity in offspring with female-biased sex ratio.

Acute corticosterone treatment prior to ovulation biases offspring sex ratios towards males in zebra finches Taeniopygia guttata

Researchers have documented significant skews in the primary sex ratios of avian offspring in relation to a variety of environmental and social cues. Zebra finches Taeniopygia guttata, in particular, adjust offspring sex ratio according to both the quality and quantity of available food, as well as male attractiveness. The mechanisms behind such manipulation of offspring sex remain elusive. Recent studies suggest that females with chronically elevated corticosterone levels (both naturally and artificially) produce significantly female biased offspring sex ratios. We tested the effects of a pharmacological dose of corticosterone or progesterone administered at the time of sex chromosome segregation on the primary sex ratio of zebra finch offspring to determine whether one or both hormones act on offspring sex at this critical period. Females were injected with 20 mg of corticosterone or 20 mg of progesterone five hours prior to the predicted time of ovulation of the 3 rd or 4th ovulating follicle. A third group of females were unmanipulated. The corticosterone treated group produced 72% males while the control group produced 37.5% in the 3rd or 4th ovulation of the sequence. Progesterone injections disrupted ovulation and oviposition in 90% of females. Corticosterone administration did not adversely affect oviposition or ovulation. Females injected with corticosterone had significantly elevated levels of corticosterone 20 min, 1 h and 2.5 h post-injection and produced significantly more males compared to untreated females. Our results suggest that offspring sex ratios may be influenced at the time of meiotic division by acute exposure to corticosterone and provides evidence for the timing of this effect.