Biased Sex Ratios Research Articles

Effects of global warming on species with temperature-dependent sex determination: Bridging the gap between empirical research and management.

Global warming could threaten over 400 species with temperature‐dependent sex determination (TSD) worldwide, including all species of sea turtle. During embryonic development, rising temperatures might lead to the overproduction of one sex and, in turn, could bias populations’ sex ratios to an extent that threatens their persistence. If climate change predictions are correct, and biased sex ratios reduce population viability, species with TSD may go rapidly extinct unless adaptive mechanisms, whether behavioural, physiological or molecular, exist to buffer these temperature‐driven effects. Here, we summarize the discovery of the TSD phenomenon and its still elusive evolutionary significance. We then review the molecular pathways underpinning TSD in model species, along with the hormonal mechanisms that interact with temperatures to determine an individual's sex. To illustrate evolutionary mechanisms that can affect sex determination, we focus on sea turtle biology, discussing both the adaptive potential of this threatened TSD taxon, and the risks associated with conservation mismanagement.

Home range use in the West Australian seahorse Hippocampus subelongatus is influenced by sex and partner\u2019s home range but not by body size or paired status

Genetic monogamy is the rule for many species of seahorse, including the West Australian seahorse Hippocampus subelongatus. In this paper, we revisit mark-recapture and genetic data of H. subelongatus, allowing a detailed characterization of movement distances, home range sizes and home range overlaps for each individual of known sex, paired status (paired or unpaired) and body size. As predicted, we find that females have larger home ranges and move greater distances compared to males. We also confirm our prediction that the home ranges of pair-bonded individuals (members of a pair known to reproduce together) overlap more on average than home ranges of randomly chosen individuals of the opposite or same sex. Both sexes, regardless of paired status, had home ranges that overlapped with, on average, 6–10 opposite-sex individuals. The average overlap area among female home ranges was significantly larger than the overlap among male home ranges, probably reflecting females having larger home ranges combined with a female biased adult sex ratio. Despite a prediction that unpaired individuals would need to move around to find a mate, we find no evidence that unpaired members of either sex moved more than paired individuals of the same sex. We also find no effect of body size on home range size, distance moved or number of other individuals with which a home range overlapped. These patterns of movement and overlap in home ranges among individuals of both sexes suggest that low mate availability is not a likely explanation for the maintenance of monogamy in the West Australian seahorse.

Male-biased effective sex ratio across populations of the threatened Zamia boliviana (Zamiaceae)

Populations of dioecious plants commonly exhibit dissimilarities to the equilibrium expectation of a 1:1 sex ratio. Differential expenditure for reproduction between genders is cited as the primary mechanism responsible for a male-biased sex ratio, with increased effects on long-living species, but these mechanisms are still poorly understood. We explore the sex ratio in the endemic gymnosperm Zamia boliviana (Zamiaceae) populations from the Brazilian savanna (the Cerrado). We aim to investigate what the Z. boliviana sex ratio is, and whether population density and ecological correlates lead to variation in the sex proportion among Cerrado habitats. The study was conducted on ten in situ populations of Z. boliviana at sexual maturity (tertiary sex ratio). We estimated the populations’ sex ratio and performed a redundancy analysis to assess the relationship between biotic traits, such as sex ratio, and associated environmental features. Soil texture classes were used to classify the cycad habitats and were expressed in a ternary phase diagram. The results show a significant male-biased sex ratio in seven of the ten populations surveyed. Environmental factors did not explain the redundancy in the reproductive characteristics. However, the cycad occurs in different habitats in their endemic zone. Our study provides new biological data for Z. boliviana, suggesting that the differential reproductive expenditure of sexes in reproduction is governing the mechanisms of sex ratio variation, compared to local environmental factors in this cycad. The pattern of effective sex ratio found here improves our understanding of mechanisms causing biased sex ratios in cycads and other dioecious species from tropical ecosystems.

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.

Sex Ratios in a Warming World: Thermal Effects on Sex-Biased Survival, Sex Determination, and Sex Reversal.

Rising global temperatures threaten to disrupt population sex ratios, which can in turn cause mate shortages, reduce population growth and adaptive potential, and increase extinction risk, particularly when ratios are male biased. Sex ratio distortion can then have cascading effects across other species and even ecosystems. Our understanding of the problem is limited by how often studies measure temperature effects in both sexes. To address this, the current review surveyed 194 published studies of heat tolerance, finding that the majority did not even mention the sex of the individuals used, with <10% reporting results for males and females separately. Although the data are incomplete, this review assessed phylogenetic patterns of thermally induced sex ratio bias for 3 different mechanisms: sex-biased heat tolerance, temperature-dependent sex determination (TSD), and temperature-induced sex reversal. For sex-biased heat tolerance, documented examples span a large taxonomic range including arthropods, chordates, protists, and plants. Here, superior heat tolerance is more common in females than males, but the direction of tolerance appears to be phylogenetically fluid, perhaps due to the large number of contributing factors. For TSD, well-documented examples are limited to reptiles, where high temperature usually favors females, and fishes, where high temperature consistently favors males. For temperature-induced sex reversal, unambiguous cases are again limited to vertebrates, and high temperature usually favors males in fishes and amphibians, with mixed effects in reptiles. There is urgent need for further work on the full taxonomic extent of temperature-induced sex ratio distortion, including joint effects of the multiple contributing mechanisms.

Effects of environmental factors on changing sex structure of cultivated mussels (Mytilus galloprovincialis, Lamarck, 1819) in the coastal zone of the Black Sea

AbstractAnthropogenically‐induced stressors such as eutrophication and pollution cause fundamental changes of environmental factors in many coastal ecosystems worldwide and may subsequently alter the sex structure of bivalve populations. Such a change of sex structure was observed in the mussel Mytilus galloprovincialis at the Black Sea coast of Crimea, where the sex ratio shifted toward male mussels. This pattern may be caused by the sex inversion in females, higher female mortality, and their falling off to the bottom. Experiments with cultivated mussels M. galloprovincialis were conducted in natural and laboratory conditions to identify the reasons for this phenomenon. The inversion of the mussel sex proceeds in one direction: from females to males. The change of sex occurs under the influence of environmental factors during the post‐spawning restructuring of gonads. Such factors can be adverse hydrological and hydrochemical conditions; environmental pollution; food availability; age and size of mollusks. The sex inversion of mussels in the polluted water area was 20% higher than in the relatively clean water of the mussel farm. The higher mortality of mussel females (69%) in the polluted area as compared to the clean one (19%) was also observed. In a laboratory experiment, the mortality level of females was 34% higher than that of males. The sex ratio on the farm, 1:2.9 (♀:♂), and on the bottom under the farm, 2.6:1 (♀:♂), was found, and the predominance of females at the bottom under the farm was noted. A bias in the sex structure in one direction—from females to males—can have economic implications in aquaculture as well as ecological significance. The increasing anthropogenic impacts on natural mussel populations can cause abnormal bias of sex ratio.

Parental relatedness and parasitoid sex ratios under local mate competition

AbstractSex ratio theory predicts that, under local mate competition, a more female‐biased offspring sex ratio will be produced by females when their relatedness to their mates is closer. We assess how the sexual composition of broods responds to mother–mate relatedness using Goniozus legneri Gordh (Hymenoptera: Bethylidae), a parasitoid wasp that has biased sex ratios due to local mate competition. Relatedness was varied by providing virgin females with a mate that was either a sibling, a non‐sibling from the same strain, from a strain with geographically similar origin or from a strain with geographically distant origin. The sex ratios among broods produced by mothers that had mated with a sibling or a same‐strain male were similar and were more biased than broods produced by females mated with males from a different strain. Brood sex variances were higher after mating with different‐strain males. Previous evaluations of parasitoid sex ratio responses to mate relatedness have not found the patterns predicted, possibly because the species investigated can control progeny sex ratio but cannot discriminate kin. In contrast, female G. legneri appear to possess both these abilities and appears to respond to mate relatedness in qualitative agreement with theoretical predictions.

Silence of the killers: discovery of male-killing suppression in a rearing strain of the small brown planthopper, Laodelphax striatellus.

According to evolutionary theory, sex ratio distortions caused by reproductive parasites such as Wolbachia and Spiroplasma are predicted to be rapidly normalized by the emergence of host nuclear suppressors. However, such processes in the evolutionary arms race are difficult to observe because sex ratio biases will be promptly hidden and become superficially unrecognizable. The evolution of genetic suppressors has been reported in just two insect species so far. In the small brown planthopper, Laodelphax striatellus, female-biases caused by Spiroplasma, which is a 'late' male-killer, have been found in some populations. During the continuous rearing of L. striatellus, we noted that a rearing strain had a 1 : 1 sex ratio even though it harboured Spiroplasma. Through introgression crossing experiments with a strain lacking suppressors, we revealed that the L. striatellus strain had the zygotic male-killing suppressor acting as a dominant trait. The male-killing phenotype was hidden by the suppressor even though Spiroplasma retained its male-killing ability. This is the first study to demonstrate the existence of a late male-killing suppressor and its mode of inheritance. Our results, together with those of previous studies, suggest that the inheritance modes of male-killing suppressors are similar regardless of insect order or early or late male killing.

Regal Fritillary (Speyeria idalia) Sex Ratio in Tallgrass Prairie: Effects of Survey Timing and Management Regime

The regal fritillary, Speyeria idalia (Drury), was once a common inhabitant of North American grassland communities. Regal fritillary populations are commonly reported to have a male biased adult sex ratio (ASR) throughout their range. We assessed the observed ASR of regal fritillary throughout an annual flight period, investigated how the overall density of both sexes changed, and tested effects of prescribed fire, grazing and haying management treatments on male and female density. We found that regal fritillary exhibited an observed 2:1 male biased ASR across the entire emergence period. Our analysis also revealed that male density peaked earlier than female density in the flight period. Point estimates of density indicated sites that received prescribed burning at the moderate fire-return interval supported ≥1.3 times greater density of males and ≥5.6 times greater density of females versus sites burned with short and long fire-return intervals. Additionally, this effect was enhanced when combined with grazing which showed males were ≥1.9 times and females had ≥1.2 times greater point estimates of density in sites that were grazed and burned at a moderate fire-return interval versus other sites. The relatively stable status of regal fritillary within our study region suggests that a 2:1 male to female ASR may be considered the model composition of populations throughout their range. Likewise, the dynamic nature of the ASR throughout the flight period highlights the importance of conducting surveys across the flight period. Finally, these results corroborate an increasing number of research results that reveal common prairie management practices, such as prescribed fire can be applied within sites that contain regal fritillary and continue to support stable populations.

Osugoroshi virus, a male-killer virus

In insects, sex ratio bias is sometimes introduced by feminization, parthenogenesis, cytoplasmic incompatibility, or male-killing. Some intracellular bacteria such as Wolbachia or Spiroplasma has been known as male-killing agents. Here I introduce an example of non-bacterial male-killing agent, Osugoroshi virus found in oriental tea tortrix.

Biased sex-ratio in woodland grouse population of the Tatra National Park, suggested by molecular sexing of non-invasive samples

Sex ratio (ratio between the number of male and female individuals in a population) is an important factor contributing to the survival rates of the population in wild. Imbalanced sex ratio is often the cause of diminished survival rates of endangered species. The analysis of DNA collected through noninvasive methodologies effectively allows to monitor populations of rare species or species that are difficult to observe in the wild. Such method was used to determine the sex ratio in populations of the capercaillie (Tetrao urogallus) and black grouse (Lyrurus tetrix) in the Tatra National Park. We collected over 250 samples (mostly excrement) in the area of the Tatra National Park and identified species via microsatellite genotyping and determined the sex using fragments of the CHD gene. We found that the majority of the samples belonged to male specimens irrespective of the species suggesting a large deviation from an equal sex ratio in wild populations of capercaillie and black grouse in the Tatra National Park. Our results point out the fundamental contribution of genetic assessment of sex ration to monitor the viability of both species in the Tatra National Park.

A simple model for the evolution of temperature-dependent sex determination explains the temperature sensitivity of embryonic mortality in imperiled reptiles.

A common reptile conservation strategy involves artificial incubation of embryos and release of hatchlings or juveniles into wild populations. Temperature-dependent sex determination (TSD) occurs in most chelonians, permitting conservation managers to bias sex ratios towards females by incubating embryos at high temperatures, ultimately allowing the introduction of more egg-bearing individuals into populations. Here, we revisit classic sex allocation theory and hypothesize that TSD evolved in some reptile groups (specifically, chelonians and crocodilians) because male fitness is more sensitive to condition (general health, vigor) than female fitness. It follows that males benefit more than females from incubation environments that confer high-quality phenotypes, and hence high-condition individuals. We predict that female-producing temperatures, which comprise relatively high incubation temperatures in chelonians and crocodilians, are relatively stressful for embryos and subsequent life stages. We synthesize data from 28 studies to investigate how constant temperature incubation affects embryonic mortality in chelonians with TSD. We find several lines of evidence suggesting that warm, female-producing temperatures are more stressful than cool, male-producing temperatures. Further, we find some evidence that pivotal temperatures (TPiv, the temperature that produces a 1:1 sex ratio) may exhibit a correlated evolution with embryonic thermal tolerance. If patterns of temperature-sensitive embryonic mortality are also indicative of chronic thermal stress that occurs post-hatching, then conservation programs may benefit from incubating eggs close to species-specific TPivs, thus avoiding high-temperature incubation. Indeed, our models predict that, on average, a sex ratio of >75% females can generally be achieved by incubating eggs only 1°C above TPiv. Of equal importance, we provide insight into the enigmatic evolution of TSD in chelonians, by providing support to the hypothesis that TSD evolution is related to the quality of the phenotype conferred by incubation temperature, with males produced in high-quality incubation environments.

Sex ratio and life history traits at reaching sexual maturity in the dioecious shrub Fuchsia parviflora: field and common garden experiments

AbstractFuchsia parviflora is a dioecious shrub that depends on biotic pollination for reproduction. Previous studies suggest that the male plants produce more flowers, and male-biased sex ratios have been found in some natural populations. To assess whether the biased sex ratios found between genders in natural populations are present at the point at which plants reach sexual maturity, and to identify possible trade-offs between growth and reproduction, we performed a common garden experiment. Finally, to complement the information of the common garden experiment, we estimated the reproductive biomass allocation between genders in one natural population. Sex ratios at reaching sexual maturity in F. parviflora did not differ from 0.5, except in one population, which was the smallest seedling population. We found no differences between genders in terms of the probability of germination or flowering. When flowering began, female plants were taller than males and the tallest plants of both genders required more time to reach sexual maturity. Males produced significantly more flowers than females, and the number of flowers increased with plant height in both genders. Finally, in the natural population studied, the investment in reproductive biomass was seven-fold greater in female plants than in male plants. Our results showed no evidence of possible trade-offs between growth and reproduction. Despite the fact that female plants invest more in reproductive biomass, they were taller than the males after flowering, possibly at the expense of herbivory defence.

Life cycle of the dung beetle Onthophagus cervus (Fabricius, 1798) (Coleoptera: Scarabaeidae: Scarabaeinae) in moist belts of south India

Biology, nesting behaviour, and the factors favouring the high abundance of prominent dung beetle species, Onthophagus cervus (Fabricius, 1798) in an open agricultural field in North Kerala were studied. Short life cycle with high fecundity, low egg mortality, shorter larval duration, shorter developmental period, short generation time, female-biased sex ratio, and longer survivability of females were recorded. Female-biased sex ratio in O. cervus indicates that mating competition takes place between male offsprings and the high cost of producing males led to their reduction. Broad categorization of Onthophagus species is provided based on the comparison of data of brood mass production, fecundity, duration of egg, larval, pupal, adult stages, adult mortality and life span of various Onthophagus species. Higher abundance of O. cervus in the region is attributed to traits that are characterize of r-selection such as high fecundity, small body size, low egg mortality, shorter larval duration, early onset of maturity, and shorter developmental period. Short generation time which enables attaining maturity earlier together with female biased sex ratio, longer duration of females favouring high egg production and shallow tunnels which enable easy and fast tunnelling process and development in thin soil top soil layer are the other factors that contributed to the higher abundance of O. cervus. Present study showed that geographic region wise knowledge on the life history traits of prominent dung beetles are necessary for interpretation of the exact mechanism behind their seasonality and abundance in specific regions and the generated data will be useful for the conservation of species in natural habitats.

On Sahastata (Araneae: Filistatidae): complementary description of the generotype and two new species from Oman and Morocco

The Filistatinae genus Sahastata Benoit, 1968 is distributed in arid and semi-arid areas, from westernmost Sahara to India, and includes seven known species. Four of these are only known from one sex, including Sahastata nigra (Simon, 1897), the type species. Here we present the first description of a male of this species collected near the type locality in Muscat, Oman. Additionally, two new species are described: S. wunderlichi sp. nov. (♂♀, Morocco) and S. wesolowskae sp. nov. (♂♀, Oman). Sahastata infuscata (Kulczyński, 1901) is newly recorded from Kenya and Yemen and S. nigra is newly recorded from the United Arab Emirates. DNA barcodes are given for S. nigra and the two new species. We observed some details of the life cycle of three Sahastata species, including clutch size, time to maturation, and a biased sex ratio for individuals raised from egg sacs, indicating that only 20–25% of specimens reaching adulthood are males. We provide SEM images of spiders of this genus, some observations on the morphology of spinnerets and male palps, and a distribution map of the species included in the genus.

X-linked meiotic drive can boost population size and persistence.

X-linked meiotic drivers cause X-bearing sperm to be produced in excess by male carriers, leading to female-biased sex ratios. Here, we find general conditions for the spread and fixation of X-linked alleles. Our conditions show that the spread of X-linked alleles depends on sex-specific selection and transmission rather than the time spent in each sex. Applying this logic to meiotic drive, we show that polymorphism is heavily dependent on sperm competition induced both by female and male mating behavior and the degree of compensation to gamete loss in the ejaculate size of drive males. We extend these evolutionary models to investigate the demographic consequences of biased sex ratios. Our results suggest driving X-alleles that invade and reach polymorphism (or fix and do not bias segregation excessively) will boost population size and persistence time by increasing population productivity, demonstrating the potential for selfish genetic elements to move sex ratios closer to the population-level optimum. However, when the spread of drive causes strong sex-ratio bias, it can lead to populations with so few males that females remain unmated, cannot produce offspring, and go extinct. This outcome is exacerbated when the male mating rate is low. We suggest that researchers should consider the potential for ecologically beneficial side effects of selfish genetic elements, especially in light of proposals to use meiotic drive for biological control.

Sex Bias in Sample Collections From Bats, the Culprit of SARS Coronavirus, SARS-Coronavirus-2, and Other Emerging Viruses.

Sex Bias in Sample Collections From Bats, the Culprit of SARS Coronavirus, SARS-Coronavirus-2, and Other Emerging Viruses.

The evolution of reversed sex roles and classical polyandry: Insights from coucals and other animals

AbstractIn most animals, competition for mating opportunities is higher among males, whereas females are more likely to provide parental care. In few species, though, these "conventional" sex roles are reversed such that females compete more strongly for matings and males provide most or all parental care. This "reversal" in sex roles is often combined with classical polyandry—a mating system in which a female forms a harem with several males. Here, we review the major hypotheses relating such role reversals to evolutionary and behavioural traits (anisogamy, phylogenetic history, sexy males, parental care, genetic paternity, trade‐off between mating and parenting, adult sex ratio) and to ecological factors (food supply, offspring predation). We evaluate each hypothesis in relation to coucals (Centropodinae), a group of nesting cuckoos of great interest for mating system and parental care theory. The black coucal (Centropus grillii) is the only known bird combining classical polyandry with altricial development of young, a costly trait with regard to parental care. Our long‐term study offers a unique possibility to compare the strongly polyandrous black coucal with a monogamous close relative breeding in the same area and habitat, the white‐browed coucal (C. superciliosus). We show that the evolution of sex roles in coucals and other animals has many different facets. Whereas phylogenetic constraints are important, confidence in genetic paternity is not. In combination with facilitating ecological conditions, adult sex ratios are key to understanding sex roles in coucals, shorebirds, and most likely also other animals. We plead for more studies including experimental tests to understand how biased adult sex ratios emerge and whether they drive sexual selection or vice versa. How do sex ratios and sexual selection interact and feedback on each other? Answers to these questions will be fundamental for understanding the evolution of sex roles in mating and parenting in coucals and other species.

Host fitness of different aphid species for Diaeretiella rapae (M’Intosh): a life table approach

Diaeretiella rapae [M’Intosh (Hymenoptera: Braconidae)] is a koinobiont, cosmopolitan, solitary and polyphagous endo-parasitoid of various species of aphids especially attacking on cruciferous plants. Present study intended to assess the quality of three aphid species i.e. Myzus persicae (Sulzer), Lipaphis erysimi (Kaltenbach), and Brevicoryne brassicae (Linn.) (Hemiptera: Aphididae) as host influencing the survival rate, demography, population growth, longevity and sex ratio of D. rapae. Diaeretiella rapae exhibited considerably highest life expectancy on M. persicae followed by L. erysimi and B. brassicae. However, mortality survival ratio and indispensable mortality was highest at pupal stage when D. rapae was reared on M. persicae. Moreover, natality rate (mx), potential fecundity (pf), net reproductive rate (R0) and intrinsic rate of increase (rm) was significantly (P < 0.05) highest on M. persicae followed by L. erysimi and B. brassicae. Similarly, adult longevity was prolonged on M. persicae with female biased sex ratio. Based on the present study it can be concluded that M. persicae proved to be the best host for D. rapae, however, L. erysimi and B. brassicae proved to be the moderate or less suitable host for the multiplication of this parasitoid species. Moreover, it may be difficult to find whether the use of a particular food for nutrition by a host of parasitoid will have a positive or negative impact on biological performance of parasitoid, therefore, there is an urge to determine these facts experimentally using biochemical analysis.

Birth sex ratio in the offspring of professional male soccer players: influence of exercise training load.

Can the exercise training load of elite male athletes influence the sex ratio of their offspring? This is the first study assessing the influence of exercise training load on the offspring sex ratio of children from male professional athletes, observing a bias toward more females being born as a result of both high-intensity and high-volume loads, with intensity having the greatest effect. There is a relatively constant population sex ratio of males to females among various species; however, certain events and circumstances may alter this population sex ratio favoring one sex over the other. Observational, descriptive cross-sectional study with a duration of 3 months. Seventy-five male professional soccer players from First Division soccer teams. Offspring variables were sex of the offspring, number of children and order of birth. Exercise training variables were volume and intensity. Total offspring was 122 children (52 males (42.6%), 70 females (57.4%)). Analysis revealed that increase in either the volume (P < 0.001) or intensity (P < 0.001) of training by the players shifted the birth offspring ratio more toward females. Within the sample of females born, more births (i.e. number) were observed as a consequence of training at the highest intensity (45 out of 70; P < 0.001), no such pattern occurred within males (P > 0.05). When female versus male births were compared within each intensity, only the high-intensity comparison was significant (45 (75%) females vs 15 (25%) males, P < 0.001). While this is the first study assessing differences in the sex ratio of the offspring of male athletes (i.e. soccer players), we acknowledge there are limitations and confounders within our approach; e.g. small sample size, ethnic background and variations in the timing of intercourse relative to ovulation as well as in sex hormone levels. As such, we propose that future research is needed to confirm or refute our findings. It is recommended that such work expand on the measurements obtained and conduct direct assessment of sperm characteristics. The findings of the study support the fact that different stressors on the body may alter the sex of the offspring. While in the present study the stressor is the excessive training load of soccer players, other events may lead to similar results. The bias in offspring sex ratio may have important implications for demography and population dynamics, as well as genetic trait inheritance. There is no funding nor competing interests. N/A.