Environmental sex reversal,Trojan sex genes,and sex ratio adjustment: conditions and population consequences

The great diversity of sex determination mechanisms in animals and plants ranges from genetic sex determination (GSD, e.g. mammals, birds, and most dioecious plants) to environmental sex determination (ESD, e.g. many reptiles) and includes a mixture of both, for example when an individual’s genetically determined sex is environmentally reversed during ontogeny (ESR, environmental sex reversal, e.g. many fish and amphibia). ESD and ESR can lead to widely varying and unstable population sex ratios. Populations exposed to conditions such as endocrine‐active substances or temperature shifts may decline over time due to skewed sex ratios, a scenario that may become increasingly relevant with greater anthropogenic interference on watercourses. Continuous exposure of populations to factors causing ESR could lead to the extinction of genetic sex factors and may render a population dependent on the environmental factors that induce the sex change. However, ESR also presents opportunities for population management, especially if the Y or W chromosome is not, or not severely, degenerated. This seems to be the case in many amphibians and fish. Population growth or decline in such species can potentially be controlled through the introduction of so‐called Trojan sex genes carriers, individuals that possess sex chromosomes or genes opposite from what their phenotype predicts. Here, we review the conditions for ESR, its prevalence in natural populations, the resulting physiological and reproductive consequences, and how these may become instrumental for population management.     

Persistence of an extreme male-biased adult sex ratio in a natural population of polyandrous bird

In a number of insects, fishes and birds, the conventional sex roles are reversed: males are the main care provider, whereas females focus on matings. The reversal of typical sex roles is an evolutionary puzzle, because it challenges the foundations of sex roles, sexual selection and parental investment theory. Recent theoretical models predict that biased parental care may be a response to biased adult sex ratios (ASRs). However, estimating ASR is challenging in natural populations, because males and females often have different detectabilities. Here, we use demographic modelling with field data from 2101 individuals, including 579 molecularly sexed offspring, to provide evidence that ASR is strongly male biased in a polyandrous bird with male-biased care. The model predicts 6.1 times more adult males than females (ASR=0.860, proportion of males) in the Kentish plover Charadrius alexandrinus. The extreme male bias is consistent between years and concordant with experimental results showing strongly biased mating opportunity towards females. Based on these results, we conjecture that parental sex-role reversal may occur in populations that exhibit extreme male-biased ASR.     

蜜蜂性别决定与性比调控机理研究

叙述了 4个主要蜜蜂性别决定机理的假说 :即性位点假说、基因平衡假说、蜜蜂性别决定综合假说和性基因数量决定假说。然后就蜜蜂性比由蜂王操纵 ,或是由工蜂操纵进行了论述 ,并对蜜蜂性比调控机理研究提出了一些建议     

Heritable variation of sex ratio in a polychaete worm

Ophryotrocha labronica is a gonochoristic polychaete worm whose sex determining mechanism and sex ratio control are supposed to be polygenic. From a lab population, whose sex ratio (i.e., proportion of males) was 0.5, the estimate of sex ratio heritability by offspring-father regression was 0.54 ± 0.15 and by offspring-mother regression was not significantly different from 0. Estimate of sex ratio repeatability between successive broods of a pair was 0.64 ± 0.33. Since female parents do not contribute in any way to the variability of sex ratio, sex ratio variation seems to be largely a paternal character. On the basis of these estimates we advance the hypothesis that in this species sex is determined by a multilocus genetic system, allowing the combined effects of a female major sex gene (which could give rise to a form of female heterogamety) and masculinizing modifiers. The hypothesis that the male sex has the least canalised sexual differentiation is supported by the observation that some old males developed oocytes.     

Population differences in female resource abundance, adult sex ratio, and male mating success in Dendrobates pumilio

In this study I examined the relationship among abundance ofreproductive resources, population density, and adult sex ratioin the strawberry dart-poison frog, Dendrobates pumilio, andhow these variables in turn influence the mating system, malereproductive success, and sexual selection. I studied the matingbehavior in two populations of D. pumilio living in a primaryand secondary rainforest on the Caribbean slope of Costa Rica.The abundance of tadpole-rearing sites (reproductive resourcesfor females) was approximately 10-fold higher in the secondary forest. Accordingly, the population density was higher and theadult sex ratio was strongly female biased in the secondaryforest, whereas the adult sex ratio was even in the primaryforest. The female-biased sex ratio was associated with a higherlevel of polygyny and higher male mating and reproductive successin the secondary forest. In contrast, the level of polyandrydid not differ between habitats. As expected, the opportunityfor sexual selection on male mating success was lower in thesecondary forest, the habitat with high female density. Inconclusion, my results suggest that ecological variables suchas resource availability have a great impact on the matingsystem and sexual selection through their effect on population structure. Moreover, the results of this study give furtherevidence that the opportunity for sexual selection is influencedby the adult sex ratio and hence by the operational sex ratioin a population.     

Sex ratio selection and multi-factorial sex determination in the housefly: a dynamic model

Sex determining (SD) mechanisms are highly variable between different taxonomic groups and appear to change relatively quickly during evolution. Sex ratio selection could be a dominant force causing such changes. We investigate theoretically the effect of sex ratio selection on the dynamics of a multi-factorial SD system. The system considered resembles the naturally occurring three-locus system of the housefly, which allows for male heterogamety, female heterogamety and a variety of other mechanisms. Sex ratio selection is modelled by assuming cost differences in the production of sons and daughters, a scenario leading to a strong sex ratio bias in the absence of constraints imposed by the mechanism of sex determination. We show that, despite of the presumed flexibility of the SD system considered, equilibrium sex ratios never deviate strongly from 1 : 1. Even if daughters are very costly, a male-biased sex ratio can never evolve. If sons are more costly, sex ratio can be slightly female biased but even in case of large cost differences the bias is very small (<10% from 1 : 1). Sex ratio selection can lead to a shift in the SD mechanism, but cannot be the sole cause of complete switches from one SD system to another. In fact, more than one locus remains polymorphic at equilibrium. We discuss our results in the context of evolution of the variable SD mechanism found in natural housefly populations.     

Superparasitism and sex ratio in the solitary parasitoidEpidinocarsis lopezi

Highly variable sex ratios are found in the solitary parasitoidEpidinocarsis lopezi, both in the field and in a mass-rearing situation. Superparasitism is one of a number of factors which can influence sex ratios in parasitoid Hymenoptera. We show that superparasitism inE. lopezi is common in the field. Sex allocation decisions when parasitizing unparasitized hosts are not different from those with parasitized hosts; neither does differential mortality occur between the sexes in superparasitized hosts. Therefore superparasitism does not contribute to the variable sex ratio ofE. lopezi. Both the occurrence of superparasitism and the sex produced when ovipositing are shown to be functional forE. lopezi.     

Primary sex ratio adjustment to experimentally reduced male UV attractiveness in blue tits

The study of primary sex ratio adjustment in birds is notoriousfor inconsistency of results among studies. To develop our understandingof avian sex ratio variation, experiments that test a prioripredictions and the replication of previous studies are essential.We tested if female blue tits Parus caeruleus adjust the sexratio of their offspring to the sexual attractiveness of theirmates, as was suggested by a previous benchmark study on thesame species. In 2 years, we reduced the ultraviolet (UV) reflectanceof the crown feathers of males in the period before egg layingto decrease their attractiveness. In contrast to the simpleprediction from sex allocation theory, we found that the overallproportion of male offspring did not differ between broods ofUV-reduced and control-treated males. However, in 1 year, theUV treatment influenced offspring sex ratio depending on thenatural crown UV reflectance of males before the treatment.The last result confirms the pattern found in the previous bluetit study, which suggests that these complex patterns of primarysex ratio variation are repeatable in this bird species, warrantingfurther research into the adaptive value of blue tit sex ratioadjustment to male UV coloration.     

The operational sex ratio influences choosiness in a pipefish

If more females than males are available for mating in the breedingpopulation (i.e., the operational sex ratio, OSR, is femalebiased), males can afford to be choosy. In the pipefish (Syngnathustyphle) females compete for males, who are choosy. In natureOSRs are typically female biased, but may occasionally be malebiased. In a series of experiments, males were allowed to choosebetween a large and a small female under a perceived excessof either males or females. Under female bias, males preferredthe large female: they spent more time close to her than tothe small female; they courted the large female sooner thanthe small; and they tended to copulate sooner and more oftenwith the large female. Under male bias all these differencesvanished and males mated at random with respect to female size.Males reproduced at a faster rate under male than under femalebias because they received more eggs in their brood pouches.Thus, males switched from maximizing mate quality (i.e., beingchoosy) to minimizing the risk of not reproducing (i.e., beingquick) as the OSR became male biased.     

Sex ratio and male sexual characters in a population of blue tits, Parus caeruleus

Sex allocation theory proposes that parents should bias thesex ratio of their offspring if the reproductive value of onesex is greater than that of the other. In the monogamous bluetit (Parus caeruleus), males have a greater variance in reproductivesuccess than females, and high-quality males have higher reproductivesuccess than high-quality females due to extrapair paternity.Consequently, females mating with attractive males are expectedto produce broods biased toward sons, as sons benefit more thandaughters from inheriting their father's characteristics. Songand plumage color in birds are secondary sexual characters indicatingmale quality and involved in female choice. We used these malesexual traits in blue tits to investigate adaptive sex ratiomanipulation by females. We did not find any relationship betweenmale color ornamentation and brood sex ratio, contrary to previousstudies. On the other hand, the length of the strophe bout (i.e.,the mean number of strophes per strophe bout) of fathers waspositively related with the proportion of sons in their broods.The length of the strophe bout is supposed to reflect male qualityin terms of neuromuscular performance. We further showed thatsons produced in experimentally enlarged broods had shorterstrophe bouts than sons raised in reduced broods. These resultsare consistent with the hypothesis that females adjust the sexratio of their broods in response to the phenotype of theirmate.     

Seasonal sex ratio and unbalanced investment sex ratio in the Banksia bee Hylaeus alcyoneus

Abstract 1. Hylaeus alcyoneus is an endemic solitary bee common on coastal heaths of Western Australia. The bee is unusual in that males are larger than females. This size dimorphism presents an opportunity to test the theory of resource-dependent sex allocation, in which theory predicts that when resources are low the sex ratio should be biased towards the smaller sex. In most bees, females are larger than males and, in line with theoretical prediction, sex ratios are male biased when resources are scarce.
2. The emerging sex ratio and brood mass from a natural population of H. alcyoneus using trap nests was studied over two seasons (1999, 2000). A switch from a male- to a female-biased sex ratio through the season was found, which was related to a reduced floral resource.
3. Fisherian sex ratio theory predicts that total investment in each sex throughout a season should be equal and that the sex ratio should be biased towards the smaller sex. By measuring the mass of the emerging progeny, the total investment was found to favour males. Possible explanations for this bias in investment are discussed.     

Constraints on adaptation: explaining deviation from optimal sex ratio using artificial neural networks

Determining processes constraining adaptation is a major challenge facing evolutionary biology, and sex allocation has proved a useful model system for exploring different constraints. We investigate the evolution of suboptimal sex allocation in a solitary parasitoid wasp system by modelling information acquisition and processing using artificial neural networks (ANNs) evolving according to a genetic algorithm. Theory predicts an instantaneous switch from the production of male to female offspring with increasing host size, whereas data show gradual changes. We found that simple ANNs evolved towards producing sharp switches in sex ratio, but additional biologically reasonable assumptions of costs of synapse maintenance, and simplification of the ANNs, led to more gradual adjustment. Switch sharpness was robust to uncertainty in fitness consequences of host size, challenging interpretations of previous empirical findings. Our results also question some intuitive hypotheses concerning the evolution of threshold traits and confirm how neural processing may constrain adaptive behaviour.     

Effects of sexual differences of age at maturity and survival on population sex ratio

Summary Five demographical factors influencing the sex ratio of a population are classically considered. The influence of two of them is dependent on the longevity of individuals in the population. The effect of differential age at maturity between males and females is higher for animals with low annual survival, whereas the effect of differential annual survival between males and females is higher for animals with high annual survival. Such a conclusion applied to turtles, which are long life-span animals, allows us to retain differential survival between sexes as a major factor influencing the population sex ratio.     

Female egg dumping and the effect of sex ratio on male egg carrying in a coreid bug

Phyllomorpha laciniata Vill (Heteroptera, Coreidae) is uniqueamong terrestrial insects in that females glue eggs on the backsof other conspecifics. Egg carrying byP. laciniatamales haspreviously been considered as paternal care. We explored femaleoviposition with respect to previous mating experience of femalesand tested whether sex ratio affects male egg-carrying. Thehypothesis that male egg-carrying is a form of paternal carepredicts that a male should always accept eggs after matingwith a female. However, if male egg-carrying is a form of postcopulatorymate guarding rather than paternal care, egg carrying shouldincrease in the presence of other males. When two couples wereplaced together, females laid eggs on the backs of all individualsenclosed, including the backs of other females. However, whena female was accompanied by 2 males, 22 out of 26 females ovipositedon their mating partner. Thus, sexual competition rather thanpaternity alone, affects a male's eagerness to carry eggs. However,even if males sometimes carry their own eggs, females lay eggson the backs of all conspecifics they can easily acquire. Thus,egg carrying in P. laciniata is partially voluntary and partiallythe result of female egg dumping     

Brood sex ratio variation in a cooperatively breeding bird

In cooperatively breeding species, the fitness consequences of producing sons or daughters depend upon the fitness impacts of positive (repayment hypothesis) and negative (local competition hypothesis) social interactions among relatives. In this study, we examine brood sex allocation in relation to the predictions of both the repayment and the local competition hypotheses in the cooperatively breeding long-tailed tit Aegithalos caudatus. At the population level, we found that annual brood sex ratio was negatively related to the number of male survivors across years, as predicted by the local competition hypothesis. At an individual level, in contrast to predictions of the repayment hypothesis, there was no evidence for facultative control of brood sex ratio. However, immigrant females produced a greater proportion of sons than resident females, a result consistent with both hypotheses. We conclude that female long-tailed tits make adaptive decisions about brood sex allocation.     

Litter size and fetal sex ratio adjustment in a highly polytocous species: the wild boar

For species in which reproductive success is more variable inone sex than the other, the Trivers and Willard model (TWM)predicts that females are able to adjust their offspring sexratio. High-quality mothers should provide greater investmentto one sex than the other. Previous tests of the TWM have beeninconsistent, and whether the TWM applies to species with severaloffspring per litter is unclear due to possible trade-offs betweensize, number, and sex of the offspring. Williams' model (WM)accounts for confounding effects of these trade-offs on sexratio variation. Lastly, the "extrinsic modification hypothesis"predicts changes in offspring sex ratio in relation to climaticconditions and population density. Using wild boar as a model,we tested 1) whether the WM fitted observed sex ratio variationand 2) whether sex ratio variations were related to maternalattributes (test of the TWM) and/or to resource availability(test of the extrinsic modification hypothesis). Females adjustedtheir litter size rather than their litter composition, so thatthe WM was not supported. Likewise, changes in resource availabilitydid not influence the fetal sex ratio, so that the extrinsicmodification hypothesis was not supported. The fetal sex ratiowas negatively related to increasing litter size, providingsome support for the TWM. Sex ratio was male biased for littersizes up to 6 and then became female biased in larger litters.Our results provide the first case study showing marked changesin sex ratio in relation to litter size in a large mammal.