Unbiased Sex Ratio Research Articles

Multi-year evidence of unbiased sex ratios in hatchery and wild-reared age-0 lake sturgeon (Acipenser fulvescens)

Assessment of population sex ratios allows managers to forecast recruitment dynamics and loss of genetic diversity in natural populations and is important when the focal population is in low abundance and subject to demographic stochasticity. If levels of natural or artificial selection differ for males and females and levels of mortality likewise vary, lower levels of population recruitment, loss of genetic diversity, and genetic drift can occur. Lake sturgeon (Acipenser fulvescens) are a species of conservation concern, where restoration efforts increasingly rely on hatchery supplementation. Raising larvae to the juvenile stage can increase survival during important early life stages; however, knowledge is lacking concerning effects of artificial rearing environments on differential sex-specific survival before release. We genetically determined the sex of 1459 age-0 lake sturgeon from three cohorts (2016 through 2018) using PCR assays of the ALLWSex2 acipenserid sexing marker. Sexed individuals represented three groups: (1) wild-captured dispersing larvae that died during hatchery rearing, (2) wild-captured dispersing larvae that survived hatchery rearing to release, and (3) wild-captured, wild-raised age-0 individuals. Sex ratios of wild-captured larvae (dead + live) were nearly 50:50 in all years surveyed. We observed slight, but non-significant, directionality in sex ratios in the live and dead hatchery-reared larvae and in wild-captured age-0 individuals. Genetic sexing methods allow for analyses during prolonged pre-reproductive periods and associated variable environmental and demographic circumstances, in situations where physical determination of sex is not possible.

Capture-Recapture Reveals Heterogeneity in Habitat-Specific Mongoose Densities and Spatiotemporal Variability in Trapping Success in St. Kitts, West Indies

The small Indian mongoose (Urva auropunctata) is a non-native invasive species across the Caribbean and a rabies reservoir on at least four islands in the region. Although previous studies reported mongoose density estimates in their non-native range, the variability in trapping designs, study seasonality, and analytical methods among studies precludes direct comparisons. This study is the first to report mongoose densities for the island of St. Kitts, West Indies. Our objective was to quantify mongoose densities across four habitats characteristic for the island. High capture and recapture rates in this study resulted in detailed estimates of spatial heterogeneity in mongoose densities, ranging from 0.53 (CI95: 0.46–0.61) mongooses/ha in suburban habitat to 5.85 (CI95: 4.42–7.76) mongooses/ha in nearby dry forest. Estimates were robust to the estimation method used (correlation among methods, r > 0.9). Female-biased sex ratios estimated from fall season versus mostly unbiased sex ratios estimated from summer season suggests seasonality in capture success resulting from differences in sex-specific activity patterns of mongooses. We found no effect of habitat characteristics, at the scale of trap placements, associated with mongoose capture success.

Male-biased sex ratios of Tripneustes gratilla around Taiwan

In a preliminary study of the sea urchin, Tripneustes gratilla at Hobihu, south Taiwan, biased sex ratios were found in 2010. Three hypotheses were proposed to explain the mechanism and tested in a wider region around Taiwan. The Sampling Bias Hypothesis was not supported since external morphology, including “masking” percentages, i.e., percentages of debris cover on top of urchin tests, and the height:diameter ratios of urchin tests were not different between the sexes. The Innate Hypothesis was not supported since an island-wide investigation revealed unbiased sex ratios in six out of seven surveys carried out in March/April when the urchins started to appear on the surface of the substrate, but the sex ratios were male-biased in all 11 surveys, later in the year. Moreover, artificially propagated sea urchins raised in seawater ponds had unbiased sex ratios, whereas the wild population in the same region and season had significantly male-biased sex ratios. With the progress of season, the sex-ratios became more and more biased with increasing urchin sizes, in two field cases. These phenomena falsified the Innate Hypothesis. The Differential Mortality Hypothesis was the only one that could not be falsified. Females obviously suffer higher mortality rates than males in the field, presumably due to predators. It is suggested that females attracted predators during repeated spawning when they released eggs. The additional mortality rates of females than males were estimated to be no less than 20% per month based on the change of sex ratios through seasons.

Population characteristics of the house rat (Rattus rattus) in rural areas of Pothwar, Pakistan

The house rat (Rattus rattus) is the major commensal rodent species present in rural habitats of Pakistan. Little is known about the biology of this species in the country. Hence, proper control plans for its management could not be developed. The objective of the present study was to determine the population biology of the house rat in rural commensal habitats of Pothwar, Pakistan. A two-year study was conducted in four villages during four seasons. A total of 217 house rats were captured with snap traps. The species had an unbiased sex ratio. Individuals from different age groups were present in the population, and the adults outnumbered sub-adults and juveniles. Reproductive activity was observed throughout the year, and reproductively active individuals outnumbered the inactive ones. These results show that rural commensal habitats were providing suitable environment for the house rats throughout the year. The findings of the present study will be useful for the planning of control strategies in the commensal habitats of rural Pothwar.

Demography of the endangered butterfly Euphydryas aurinia (Lepidoptera: Nymphalidae): A case study of populations in sub-Mediterranean dry calcareous grasslands

We studied a population of the regionally endangered marsh fritillary butterfly Euphydryas aurinia inhabiting a system of loosely connected dry calcareous grasslands in sub-Mediterranean Slovenia. Our goal was to set the basis for a long-term monitoring of this butterfly in four meadows using mark-release-recapture (MRR). We determined its demographic parameters, dispersal, behaviour and utilization of nectar plants in different quality patches. Total population size was estimated to be approximately 347 males (95% confidence interval: 262-432) and 326 females (95% confidence interval: 250-402), with an unbiased sex ratio. The average lifespans were 6.3 and 8.6 days, respectively. Daily population sizes followed a parabola with marked protandry. Both sexes were relatively highly mobile with both occasionally moving over half a kilometre. The spatial distribution of animals seemed to be associated with patch size, host plant densities and nectar sources, resulting in much higher population densities in the largest patch. Adult behaviour differed between the sexes, with females resting more and flying less than males. Behaviour also changed during daytime and with the progression of the season. Adults were confirmed to be opportunistic feeders, since as many as ten nectar sources were detected. We conclude that demographic parameters differ greatly among regions and habitats, thus conservation aims should be planned accordingly. Although the population studied is apparently in good condition, there are threats that may hamper the long-term persistence of the species in this area: succession, intensification of mowing and overgrazing.

Asexual queen succession mediates an accelerated colony life cycle in the termite Silvestritermes minutus.

Mixed modes of reproduction, combining sexual processes with thelytokous parthenogenesis, occur in all major clades of social insects. In several species of termites, queens maximize their genetic input into nondispersing replacement queens through parthenogenesis, while maintaining genetically diverse sterile offspring and dispersing reproductives via sexual reproduction. This so-called asexual queen succession (AQS) has multiple independent origins and its presumed advantages are diverse as well, ranging from multiplication of colony reproductive potential to extension of its lifespan beyond that of the foundress. However, how AQS shapes colony life cycles under natural conditions remains poorly known. The neotropical termite Silvestritermes minutus inhabits small but conspicuous nests, offering a unique opportunity to investigate the impact of AQS on life history. We report on its breeding system, life cycle and sex allocation using social structure census in 137 nests and genotyping of 12 colonies at 12 microsatellite loci. We show that colonies are established by an outbred pair of primary reproductives. In less than 2years, the foundress is replaced by multiple neotenic queens, arising mostly through automixis with central fusion. Sterile castes, male and most (93%) female dispersers are produced sexually. Colony reproduction is usually restricted to a single dispersal of alates with unbiased sex ratio, taking place after 3years. We conclude that S.minutus benefits from AQS to maximize colony growth rate and alate production within a very short life cycle rather than to extend colony lifespan. This highlights the versatile role of AQS in different cases of its polyphyletic origin.

Spatial variation in adult sex ratio across multiple scales in the invasive golden apple snail, Pomacea canaliculata.

Adult sex ratio (ASR) has critical effects on behavior and life history and has implications for population demography, including the invasiveness of introduced species. ASR exhibits immense variation in nature, yet the scale dependence of this variation is rarely analyzed. In this study, using the generalized multilevel models, we investigated the variation in ASR across multiple nested spatial scales and analyzed the underlying causes for an invasive species, the golden apple snail Pomacea canaliculata. We partitioned the variance in ASR to describe the variations at different scales and then included the explanatory variables at the individual and group levels to analyze the potential causes driving the variation in ASR. We firstly determined there is a significant female‐biased ASR for this species when accounting for the spatial and temporal autocorrelations of sampling. We found that, counter to nearly equal distributed variation at plot, habitat and region levels, ASR showed little variation at the town level. Temperature and precipitation at the region level were significantly positively associated with ASR, whereas the individual weight, the density characteristic, and sampling time were not significant factors influencing ASR. Our study suggests that offspring sex ratio of this species may shape the general pattern of ASR in the population level while the environmental variables at the region level translate the unbiased offspring sex ratio to the female‐biased ASR. Future research should consider the implications of climate warming on the female‐biased ASR of this invasive species and thus on invasion pattern.

Non-Invasive Genetic Mark-Recapture as a Means to Study Population Sizes and Marking Behaviour of the Elusive Eurasian Otter (Lutra lutra).

Quantifying population status is a key objective in many ecological studies, but is often difficult to achieve for cryptic or elusive species. Here, non-invasive genetic capture-mark-recapture (CMR) methods have become a very important tool to estimate population parameters, such as population size and sex ratio. The Eurasian otter (Lutra lutra) is such an elusive species of management concern and is increasingly studied using faecal-based genetic sampling. For unbiased sex ratios or population size estimates, the marking behaviour of otters has to be taken into account. Using 2132 otter faeces of a wild otter population in Upper Lusatia (Saxony, Germany) collected over six years (2006–2012), we studied the marking behaviour and applied closed population CMR models accounting for genetic misidentification to estimate population sizes and sex ratios. We detected a sex difference in the marking behaviour of otters with jelly samples being more often defecated by males and placed actively exposed on frequently used marking sites. Since jelly samples are of higher DNA quality, it is important to not only concentrate on this kind of samples or marking sites and to invest in sufficiently high numbers of repetitions of non-jelly samples to ensure an unbiased sex ratio. Furthermore, otters seemed to increase marking intensity due to the handling of their spraints, hence accounting for this behavioural response could be important. We provided the first precise population size estimate with confidence intervals for Upper Lusatia (for 2012: = 20 ± 2.1, 95% CI = 16–25) and showed that spraint densities are not a reliable index for abundances. We further demonstrated that when minks live in sympatry with otters and have comparably high densities, a non-negligible number of supposed otter samples are actually of mink origin. This could severely bias results of otter monitoring if samples are not genetically identified.

The human sex ratio from conception to birth

We describe the trajectory of the human sex ratio from conception to birth by analyzing data from (i) 3- to 6-d-old embryos, (ii) induced abortions, (iii) chorionic villus sampling, (iv) amniocentesis, and (v) fetal deaths and live births. Our dataset is the most comprehensive and largest ever assembled to estimate the sex ratio at conception and the sex ratio trajectory and is the first, to our knowledge, to include all of these types of data. Our estimate of the sex ratio at conception is 0.5 (proportion male), which contradicts the common claim that the sex ratio at conception is male-biased. The sex ratio among abnormal embryos is male-biased, and the sex ratio among normal embryos is female-biased. These biases are associated with the abnormal/normal state of the sex chromosomes and of chromosomes 15 and 17. The sex ratio may decrease in the first week or so after conception (due to excess male mortality); it then increases for at least 10-15 wk (due to excess female mortality), levels off after ∼20 wk, and declines slowly from 28 to 35 wk (due to excess male mortality). Total female mortality during pregnancy exceeds total male mortality. The unbiased sex ratio at conception, the increase in the sex ratio during the first trimester, and total mortality during pregnancy being greater for females are fundamental insights into early human development.

Small-scale variation in sexual size dimorphism and sex ratio in the aquatic moth Acentria ephemerella Denis and Schiffermüller, 1775 (Lepidoptera: Crambidae)

The aquatic herbivorous and capital-breeding moth Acentria ephemerella Denis and Schiffermüller, 1775 feeds on submerged pondweeds, Potamogeton spp., and is highly preyed upon by fish in the littoral zone. We studied the spatiotemporal within-lake variability of length, sexual size dimorphism (SSD) and sex ratio of A. ephemerella pupae and of larval population densities. Population densities at three sampling sites strongly increased from July to August and were significantly higher at the Reichenau site in July. Acentria ephemerella sex ratio was male-biased at the Güttingen and Hagnau sites, but showed unbiased or slightly biased sex ratios at Reichenau. The SSD was strongly female-biased. Female size and SSD declined during summer, possibly due to reduced food quantity/quality. The SSD was highest at Reichenau, with little to no differences between Hagnau and Güttingen. At Reichenau, the high population size in July coincided with an unbiased sex ratio, and large SSD/female size due to multiple, possibly interacting factors, including fish predation.

Female-Biased Sex Ratio in Moulting Black-Necked GrebesPodiceps nigricollisin Southern Spain

We tested if Black-necked Grebe, a species in which both sexes undertake moult-migration, have an unbiased sex ratio at a moulting site in Europe, as previously found in North America and as was expected for a species with biparental care. For this we used a unique long-term dataset of 5821 grebes captured for ringing throughout the moulting seasons of 2006–2012 in the Odiel salt-marshes (SW Spain). The grebes were sexed and classified as adults (74%) or juveniles (26%). Birds ringed at Odiel were recovered over a wide area up to central Russia and south to the Canary Islands and Morocco. We report on a unique case of a strongly biased sex ratio in a moult-migrating bird species with biparental care, in which adult females were significantly more abundant than adult males in all 7 years (1.6–4.2 females per male). Biased sex ratios were not found among juveniles. Differences between North America and Europe in the sex ratios of adult Black-necked Grebes at moulting sites may be explained by the much large...

Observations on the ecology and behaviour of the New Zealand giraffe weevil (Lasiorhynchus barbicornis)

The New Zealand giraffe weevil (Lasiorhynchus barbicornis) is an endemic, wood-boring insect (Coleoptera: Brentidae). Despite being a large and charismatic species, very little is known about its life history. We conducted observations of L. barbicornis behaviour and ecology in a wild population west of Auckland and developed a marking system in preparation for a future large-scale observational experiment. We found that giraffe weevils were easily located and observable in the field, and therefore provide a useful model species for behavioural ecology. Adults were found to aggregate, copulate and oviposit on 17 host tree species from 16 families, extending the current host plant association records for this species. A breeding experiment determined that the length of the larval stage is a minimum of 2 years and that the population at emergence has an unbiased sex ratio.

A chalcid wasp acts chiefly as a hyperparasitoid by mostly using small uncommon hosts

AbstractAlthough ovipositing insects may predominantly use resources that lead to high offspring quality, exceptions to this rule have considerably aided understanding of oviposition decisions. We report the frequency of host species use by a solitary facultative hyperparasitoid, Brachymeria subrugosa Blanchard (Hymenoptera: Chalcididae). In our samples, the wasp attacks the large pupae of the moth Gonioterma indecora Zeller (Lepidoptera: Elachistidae), as well as the considerably smaller, and rarer, pupae of two of its other parasitoids. Consistent with conditional sex allocation models, the wasp produced mainly female offspring on the largest (moth) host, an unbiased sex ratio on the middle‐sized (parasitoid) host, and only males on the smallest (parasitoid) host. Adult offspring size was correlated with the size of the host attacked. These features strongly suggest that the two smaller, primary parasitoid, hosts produce lower‐quality offspring. Despite being more common, the proportion of hosts from which parasitoids emerged was lowest (14%) on the largest host species, and highest on the rarer middle‐sized (34%) and smallest (30%) hosts. This suggests that costs or constraints on attacking high‐quality primary hosts may be a selective force favouring the evolution of hyperparasitism.

Development and pre-validation of a testosterone enzyme immunoassay (EIA) for predicting the sex ratio of immature loggerhead sea turtles (Caretta caretta) recovered along the western coast of the central Adriatic Sea

Plasma testosterone levels were evaluated, by validating and using a commercially available testosterone enzyme immunoassay (EIA) as an indicator of the sex of immature loggerhead turtles (Caretta caretta) recovered along the western coast of the central Adriatic Sea between November 2011 and February 2012. Testosterone levels were measured in blood samples collected from 28 immature turtles kept in short-term maintenance at the Fondazione Cetacea Rescue Centre (Italy). Overall, plasma testosterone ranged between 229.3 and 2628.6 pg ml−1, suggesting that the EIA procedure is effective for determining androgen titers in immature loggerhead sea turtles. Analysis of the obtained data indicates an unbiased sex ratio supporting previous studies of juvenile loggerhead turtle sex ratios in the Mediterranean Sea. The present work can be considered a starting point for augmenting knowledge on the dynamics of juvenile loggerhead aggregations increasingly found in the northern-central Adriatic Sea and for promoting local management for conservation actions.

Mothers adjust offspring sex to match the quality of the rearing environment

Theory predicts that mothers should adjust offspring sex ratios when the expected fitness gains or rearing costs differ between sons and daughters. Recent empirical work has linked biased offspring sex ratios to environmental quality via changes in relative maternal condition. It is unclear, however, whether females can manipulate offspring sex ratios in response to environmental quality alone (i.e. independent of maternal condition). We used a balanced within-female experimental design (i.e. females bred on both low- and high-quality diets) to show that female parrot finches (Erythrura trichroa) manipulate primary offspring sex ratios to the quality of the rearing environment, and not to their own body condition and health. Individual females produced an unbiased sex ratio on high-quality diets, but over-produced sons in poor dietary conditions, even though they maintained similar condition between diet treatments. Despite the lack of sexual size dimorphism, such sex ratio adjustment is in line with predictions from sex allocation theory because nutritionally stressed foster sons were healthier, grew faster and were more likely to survive than daughters. These findings suggest that mothers may adaptively adjust offspring sex ratios to optimally match their offspring to the expected quality of the rearing environment.

Bateman gradients in a promiscuous mating system

The Bateman gradient is increasingly used to measure sexual selection and characterize mating systems. In a landmark paper, Arnold and Duvall (Am Nat 143:317–348, 1994) formulated predictions about the relationships between sex-specific Bateman gradients and the major types of mating system. In promiscuous species, gradients are expected to be strong and similar in both sexes. Current support for this prediction however remains equivocal as reported male gradients are almost constantly steeper than female gradients. Here, we estimated Bateman gradients in a wild population of Eastern chipmunks (Tamias striatus) over two reproductive seasons characterized by extreme levels of promiscuity and unbiased operational sex ratios. We found significant and positive Bateman gradients for both sexes. The gradients were not different among sexes suggesting that the strength of sexual selection was similar for males and females. The opportunity for selection was also particularly strong for a promiscuous species and not different among sexes. Our results thus support the predicted Bateman gradients for a promiscuous mating system.

Spiders do not escape reproductive manipulations by Wolbachia

BackgroundMaternally inherited bacteria that reside obligatorily or facultatively in arthropods can increase their prevalence in the population by altering their hosts' reproduction. Such reproductive manipulations have been reported from the major arthropod groups such as insects (in particular hymenopterans, butterflies, dipterans and beetles), crustaceans (isopods) and mites. Despite the observation that endosymbiont bacteria are frequently encountered in spiders and that the sex ratio of particular spider species is strongly female biased, a direct relationship between bacterial infection and sex ratio variation has not yet been demonstrated for this arthropod order.ResultsFemales of the dwarf spider Oedothorax gibbosus exhibit considerable variation in the sex ratio of their clutches and were infected with at least three different endosymbiont bacteria capable of altering host reproduction i.e. Wolbachia, Rickettsia and Cardinium. Breeding experiments show that sex ratio variation in this species is primarily maternally inherited and that removal of the bacteria by antibiotics restores an unbiased sex ratio. Moreover, clutches of females infected with Wolbachia were significantly female biased while uninfected females showed an even sex ratio. As female biased clutches were of significantly smaller size compared to non-distorted clutches, killing of male embryos appears to be the most likely manipulative effect.ConclusionsThis represents to our knowledge the first direct evidence that endosymbiont bacteria, and in particular Wolbachia, might induce sex ratio variation in spiders. These findings are pivotal to further understand the diversity of reproductive phenotypes observed in this arthropod order.

The interplay of sex ratio, male success and density-independent mortality affects population dynamics

Environmental constraints can limit a population to a certain size, which is usually called the carrying capacity of a habitat. Besides to this ‘external’ factor, which is mainly determined by the limitation of resources, we investigate here another set of population-intrinsic factors that can limit a population size significantly below the maximum sustainable size. Firstly, density-independent mortality is a prominent factor in all organisms that show age-related and/or accidental death. Secondly, in sexually reproducing organisms the sex ratio and the success of pairing is important for finding reproductive partners. Using a simple model, we demonstrate how sex ratio, mating success and gender-specific mortality can strongly affect the speed of population growth and the maximum population size. In addition, we demonstrate that density-independent mortality, which is often neglected in population models, adds a very important feature to the system: it strongly enhances the negative influence of unbiased sex ratios and inefficient pairing to the maximum sustainable population size. A decrease of the maximum population size significantly affects a population's survival chance in inter-specific competition. Thus, we conclude that the inclusion of density-independent mortality is crucial, especially for models of species that reproduce sexually. We show that density-independent mortality, together with biased sex ratios, can significantly lower the abilities of a population to survive in conditions of strong inter-specific competition and due to the Allee effect. We emphasize that population models should incorporate the sex ratio, male success and density-independent mortality to make plausible predictions of the population dynamics in a gender-structured population. We show that the population size is limited by these intrinsic factors. This is of high ecological significance, because it means that there will always be resources available in any habitat that allows other species (e.g., invaders) to use these resources and settle successfully, if they are sufficiently adapted.

Diet and reproduction in the white-spotted eagle ray Aetobatus narinari from Queensland, Australia and the Penghu Islands, Taiwan

Aetobatus narinari, a circumglobal batoid, is subjected to increasing fishing pressures, especially throughout South-east Asia. However, its management and protection is complicated by the lack of relevant life history information. It appears to be a late-maturing, long-lived stingray with a size-at-maturity of ∼130 and >150 cm in ventral disc width for males and females respectively. Like other myliobatids, A. narinari is a matrotrophic viviparous species exhibiting lipid histotrophy as indicated by trophonemata. Only the left ovary and uterus are functional. The presence of mature sperm in the testes, collecting ducts, epididymis and ductus deferens coincided with the estimated time of parturition and mating. Catches indicated an unbiased sex ratio. Aetobatus narinari is a hard-prey specialist that feeds mainly on gastropods, molluscs and hermit crabs (Diogenidae). Molluscs comprised numerically and gravimetrically the most important prey group (Index of Relative Importance (IRI): 85.9% in Australia, 99.9% in Taiwan) and were observed in 83.3% and 100% of stomachs containing food from Australia and Taiwan respectively. Minor dietary shifts from a gastropod–crustacean to a more gastropod–bivalve based diet occurred as body size increased. This study provides vital biological data for the effective management and conservation of A. narinari.

Success of mutant Drosophila at different sex ratios

Relative courtship success of mutant Drosophila melanogaster males was found to vary with sex ratio. Males with one of three recessive mutants: White, vermilion, or vestigial, competed with wild type males for females. Female-biased sex ratios were associated with increased success of all three different mutant phenotypes relative to wild-type as compared to an unbiased sex ratio. There was no difference in the success of mutant males in the first or second half of the observation periods, which spanned one hour.