Paternal inheritance of the primary sex ratio in a copepod

Uniparentally inherited genetic elements are under strong selection to manipulate sex determination in their host and shift the host sex ratio towards the transmitting sex. For any sex-ratio trait, lineage analysis and quantitative genetics are important tools for characterizing the mode of inheritance (biparental vs. maternal vs. paternal) thereby narrowing the field of possible sex-determining mechanisms (e.g. polygenic, sex chromosomes with meiotic drive, cytoplasmic microorganisms). The primary sex ratio of the harpacticoid copepod, Tigriopus californicus is often male-biased and is highly variable among full sib families. We found that this extra-binomial variation for the primary sex ratio is paternally but not maternally transmitted in T. californicus. Paternal transmission of the primary sex ratio has been well documented in the haplo-diploid hymenoptera but is relatively rare in diplo-diploid organisms. If the sex-ratio trait is paternally transmitted in other closely related harpacticoid copepods it would explain why male biased primary sex ratios are so common in this group.     

Environmental sex determination in a splash pool copepod

The sex-determining mechanism has important demographic and genetic consequences by virtue of its effect on the population sex ratio. Here we investigate the effect of temperature dependent sex determination (TSD) on the primary sex ratio of the harpacticoid copepod, Tigriopus californicus . At the two experimental temperatures (15° and 22°C) used in this study, the primary sex ratio is almost always biased in favour of males. Higher temperatures induce masculinization and the change in sex ratio is not caused by differential mortality of the sexes. The mean level of TSD in the population is small (proportion of males increases by ~5% between 15° and 22°C) because only one-third of the families actually exhibit a significant sex-ratio response while the rest of the population is insensitive to temperature. A comparison of the primary sex ratio and the level of TSD between two locations reveals few differences among populations. Finally, individuals still exhibited TSD after having been maintained under constant temperature conditions in the lab for several generations. In addition the proportion of temperature-sensitive individuals remained unchanged. This suggests that the observed level of TSD is not an artefact of testing field-captured individuals in a novel laboratory environment. At this point the adaptive significance of temperature-dependent sex determination in T. californicus remains unknown.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76 , 511–520.     

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.     

Genetic variation of sex allocation in the parasitoid wasp Heterospilus prosopidis

The genetic variation of sex ratio and sex allocation were examined in a series of half-sib analyses on the sex ratio of braconid parasitoid wasp Heterospilus prosopidis populations collected in Hawaii and Arizona. The mean threshold value and the range of the threshold for change in the sex of offspring in response to resource quality (host size) were determined. Estimates of the narrow-sense heritability (h2) of sex ratio at a specific host size ranged from 0.185 to 0.315, and those of the sex changing point (threshold value) ranged from 0.220 to 0.342. The coefficient of variation (CV(A)) of sex ratio was significantly larger than CV(A) of body weight. We discuss factors that maintained the significant additive genetic variation of sex ratio.     

Multigenerational response to artificial selection for biased clutch sex ratios in Tigriopus californicus populations

Polygenic sex determination (PSD) is relatively rare and theoretically evolutionary unstable, yet has been reported across a range of taxa. Evidence for multilocus PSD is provided by (i) large between‐family variance in sex ratio, (ii) paternal and maternal effects on family sex ratio and (iii) response to selection for family sex ratio. This study tests the polygenic hypothesis of sex determination in the harpacticoid copepod Tigriopus californicus using the criterion of response to selection. We report the first multigenerational quantitative evidence that clutch sex ratio responds to artificial selection in both directions (selection for male‐ and female‐biased families) and in multiple populations of T. californicus. In the five of six lines that showed a response to selection, realized heritability estimated by multigenerational analysis ranged from 0.24 to 0.58. Divergence of clutch sex ratio between selection lines is rapid, with response to selection detectable within the first four generations of selection.     

Segregating variation for temperature-dependent sex determination in a lizard

Temperature-dependent sex determination (TSD) was first reported in 1966 in an African lizard. It has since been shown that TSD occurs in some fish, several lizards, tuataras, numerous turtles and all crocodilians. Extreme temperatures can also cause sex reversal in several amphibians and lizards with genotypic sex determination. Research in TSD species indicates that estrogen signaling is important for ovary development and that orthologs of mammalian genes have a function in gonad differentiation. Nevertheless, the mechanism that actually transduces temperature into a biological signal for ovary versus testis development is not known in any species. Classical genetics could be used to identify the loci underlying TSD, but only if there is segregating variation for TSD. Here, we use the ‘animal model'' to analyze inheritance of sexual phenotype in a 13-generation pedigree of captive leopard geckos, Eublepharis macularius, a TSD reptile. We directly show genetic variance and genotype-by-temperature interactions for sex determination. Additive genetic variation was significant at a temperature that produces a female-biased sex ratio (30 °C), but not at a temperature that produces a male-biased sex ratio (32.5 °C). Conversely, dominance variance was significant at the male-biased temperature (32.5 °C), but not at the female-biased temperature (30 °C). Non-genetic maternal effects on sex determination were negligible in comparison with additive genetic variance, dominance variance and the primary effect of temperature. These data show for the first time that there is segregating variation for TSD in a reptile and consequently that a quantitative trait locus analysis would be practicable for identifying the genes underlying TSD.     

Sex reversal and primary sex ratios in the common frog (Rana temporaria)

Sex reversal has been suggested to have profound implications for the evolution of sex chromosomes and population dynamics in ectotherms. Occasional sex reversal of genetic males has been hypothesized to prevent the evolutionary decay of nonrecombining Y chromosomes caused by the accumulation of deleterious mutations. At the same time, sex reversals can have a negative effect on population growth rate. Here, we studied phenotypic and genotypic sex in the common frog (Rana temporaria) in a subarctic environment, where strongly female‐biased sex ratios have raised the possibility of frequent sex reversals. We developed two novel sex‐linked microsatellite markers for the species and used them with a third, existing marker and a Bayesian modelling approach to study the occurrence of sex reversal and to determine primary sex ratios in egg clutches. Our results show that a significant proportion (0.09, 95% credible interval: 0.04–0.18) of adults that were genetically female expressed the male phenotype, but there was no evidence of sex reversal of genetic males that is required for counteracting the degeneration of Y chromosome. The primary sex ratios were mostly equal, but three clutches consisted only of genetic females and three others had a significant female bias. Reproduction of the sex‐reversed genetic females appears to create all‐female clutches potentially skewing the population level adult sex‐ratio consistent with field observations. However, based on a simulation model, such a bias is expected to be small and transient and thus does not fully explain the observed female‐bias in the field.     

Precision in sex allocation is influenced by mate choice in Drosophila melanogaster

Theory predicts that a 1 : 1 sex ratio is favoured in the absence of countervailing selection pressures. In an experiment with Drosophila melanogaster, we found significantly greater variation in the offspring sex ratios of freely mated flies than would be expected by the binomial distribution. In a surprise result, control flies given no mate choice exhibited significant under-dispersal in their sex ratio variation, possibly from sperm limitation. Both treatments, however, produced populations with a 1 : 1 sex ratio. This supports the hypothesis that sexually antagonistic selection for reproductive success in sons, and fecundity in daughters, may overcome selection for an equal sex ratio. Such precision in sex allocation may allow for the maintenance of genetic variation underlying trade-offs between male and female reproductive success.     

Biased sex ratios in the dioecious annual Croton texensis (Euphorbiaceae) are not due to environmental sex determination

At Arapaho Prairie, in the sandhills of western Nebraska, the dioecious annual Croton texensis (Euphorbiaceae) exhibits biased sex ratios. Moreover, the direction of bias changes from year to year: in 1994 the study population was significantly female biased, in 1995 and 1996 it was significantly male biased, and in 1997 and 1998 the sex ratio did not differ from 1 : 1. Such variation in the observed sex ratio in plants is frequently attributed to environmental sex determination (ESD), which is favored by natural selection if the rate of fitness gain across an environmental gradient is greater for one sex than the other. We performed experiments to determine: (1) whether variation in the sex ratio is correlated with environmental conditions, as would be expected if ESD is operating, and (2) whether ESD, if present, would be favored by natural selection. In a common garden experiment in which water and fertilizer were manipulated the sex ratio was marginally male biased in treatments in which water was added, but not different from 1 : 1 in other treatments. In field plots into which seeds were planted none of several soil characteristics, nor overall plot quality for C. texensis (measured as average plant biomass) were correlated with plot sex ratio. However, plots in which a large number of planted seeds emerged tended to be female biased. These results provide very weak evidence for sex ratio bias across an environmental gradient, and thus provide little evidence for ESD. Moreover, sex-by-environment interactions for fitness, which are required for the evolution of ESD, were absent for all measured variables. Thus, ESD does not appear to be favored by natural selection in this population. Instead, these biases may have been caused by differences between the sexes in germination and/or early mortality.     

Effective heritability of targets of sex-ratio selection under environmental sex determination

Selection is expected to maintain primary sex ratios at an evolutionary equilibrium. In organisms with temperature-dependent sex determination (TSD), targets of sex-ratio selection include the thermal sensitivity of the sex-determining pathway (hereafter, sex determination threshold) and nest-site choice. However, offspring sex may be canalized for nests located in thermally extreme environments; thus, genetic variance for the sex determination threshold is not expressed and is invisible to direct selection. The concept of 'effective heritability' accounts for this dependence and provides a more realistic prediction of the expected evolutionary response to selection in the wild. Past estimates of effective heritability of the sex determination threshold, which were derived from laboratory data, suggested that the potential for the sex determination threshold to evolve in the wild was extremely low. We re-evaluated original estimates of this parameter by analysing field-collected measures of nest temperatures, vegetation cover and clutch sex ratios from nests in a population of painted turtles (Chrysemys picta). We coupled these data with measurements of broad-sense heritability of the sex determination threshold in C. picta, using an experiment that splits clutches of eggs between a constant temperature (i.e. typical laboratory incubation) and a daily fluctuating temperature (i.e. similar to natural nests) with the same mean. We found that (i) the effective heritability of the sex determination threshold appears to have been historically underestimated and the effective heritability of nest-site choice has been overestimated and (ii) significant family-by-incubation treatment interaction exists for sex for C. picta between constant- and fluctuating-temperature regimes. Our results suggest that the thermal sensitivity of the sex-determining pathway may play a larger, more complex role in the microevolution of TSD than traditionally thought.     

Maintenance of polygenic sex determination in a fluctuating environment: an individual‐based model

R. A. Fisher predicted that individuals should invest equally in offspring of both sexes, and that the proportion of males and females produced (the primary sex ratio) should evolve towards 1:1 when unconstrained. For many species, sex determination is dependent on sex chromosomes, creating a strong tendency for balanced sex ratios, but in other cases, multiple autosomal genes interact to determine sex. In such cases, the maintenance of multiple sex‐determining alleles at multiple loci and the consequent among‐family variability in sex ratios presents a puzzle, as theory predicts that such systems should be unstable. Theory also predicts that environmental influences on sex can complicate outcomes of genetic sex determination, and that population structure may play a role. Tigriopus californicus, a copepod that lives in splash‐pool metapopulations and exhibits polygenic and environment‐dependent sex determination, presents a test case for relevant theory. We use this species as a model for parameterizing an individual‐based simulation to investigate conditions that could maintain polygenic sex determination. We find that metapopulation structure can delay the degradation of polygenic sex determination and that periods of alternating frequency‐dependent selection, imposed by seasonal fluctuations in environmental conditions, can maintain polygenic sex determination indefinitely.     

Humans at tropical latitudes produce more females

Skews in the human sex ratio at birth have captivated scientists for over a century. The accepted average human natal sex ratio is slightly male biased, at 106 males per 100 females or 51.5 per cent males. Studies conducted on a localized scale show that sex ratios deviate from this average in response to a staggering number of social, economical and physiological variables. However, these patterns often prove inconsistent when expanded to other human populations, perhaps because the nature of the influences themselves exhibit substantial cultural variation. Here, data collected from 202 countries over a decade show that latitude is a primary factor influencing the ratio of males and females produced at birth; countries at tropical latitudes produced significantly fewer boys (51.1% males) annually than those at temperate and subarctic latitudes (51.3%). This pattern remained strong despite enormous continental variation in lifestyle and socio-economic status, suggesting that latitudinal variables may act as overarching cues on which sex ratio variation in humans is based.     

Trends in Population Sex Ratios May be Explained by Changes in the Frequencies of Polymorphic Alleles of a Sex Ratio Gene

A test for heritability of the sex ratio in human genealogical data is reported here, with the finding that there is significant heritability of the parental sex ratio by male, but not female offspring. A population genetic model was used to examine the hypothesis that this is the result of an autosomal gene with polymorphic alleles, which affects the sex ratio of offspring through the male reproductive system. The model simulations show that an equilibrium sex ratio may be maintained by frequency dependent selection acting on the heritable variation provided by the gene. It is also shown that increased mortality of pre-reproductive males causes an increase in male births in following generations, which explains why increases in the sex ratio have been seen after wars, also why higher infant and juvenile mortality of males may be the cause of the male-bias typically seen in the human primary sex ratio. It is concluded that various trends seen in population sex ratios are the result of changes in the relative frequencies of the polymorphic alleles of the proposed gene. It is argued that this occurs by common inheritance and that parental resource expenditure per sex of offspring is not a factor in the heritability of sex ratio variation.     

Weakened purifying selection leads to elevated mutation load under environmental sex determination

In many gonochoristic taxa, sex is influenced by developmental environment, a system that can lead to temporal fluctuations in offspring sex ratio. Demographic models suggest that only short‐lived species with environmental sex determination (ESD) are negatively impacted by sex‐ratio fluctuations, yet these models fail to account for the potential mutation load associated with reductions in genetically effective population sizes. In this study, we developed a series of individual‐based simulation models that explore the fixation rates of mildly deleterious alleles under different sex‐determining systems and examine the impacts of variation in lifespan and offspring sex ratio. Populations with ESD exhibited increases in fixation rates in both short‐ and long‐lived populations, but substantial increases were limited to populations characterized by a combination of high sex‐ratio variation and short lifespan. Fixation rates were negatively associated with effective population size, indicating that purifying selection operates less efficiently under ESD relative to genotypic sex determination. Reductions in effective population size could be attributed to both intragenerational forces (unequal sex ratio) and intergenerational forces (variable census population sizes). Levels of temporal sex‐ratio variation calculated from wild populations of ESD species were capable of yielding large increases in fixation rates, although this relationship was strongly mediated by lifespan. Our results may help to explain the limited phylogenetic distribution of ESD in short‐lived taxa.     

Sex without sex chromosomes: genetic architecture of multiple loci independently segregating to determine sex ratios in the copepod Tigriopus californicus

Sex‐determining systems are remarkably diverse and may evolve rapidly. Polygenic sex‐determination systems are predicted to be transient and evolutionarily unstable, yet examples have been reported across a range of taxa. Here, we provide the first direct evidence of polygenic sex determination in Tigriopus californicus, a harpacticoid copepod with no heteromorphic sex chromosomes. Using genetically distinct inbred lines selected for male‐ and female‐biased clutches, we generated a genetic map with 39 SNPs across 12 chromosomes. Quantitative trait locus mapping of sex ratio phenotype (the proportion of male offspring produced by an F2 female) in four F2 families revealed six independently segregating quantitative trait loci on five separate chromosomes, explaining 19% of the variation in sex ratios. The sex ratio phenotype varied among loci across chromosomes in both direction and magnitude, with the strongest phenotypic effects on chromosome 10 moderated to some degree by loci on four other chromosomes. For a given locus, sex ratio phenotype varied in magnitude for individuals derived from different dam lines. These data, together with the environmental factors known to contribute to sex determination, characterize the underlying complexity and potential lability of sex determination, and confirm the polygenic architecture of sex determination in T. californicus.     

Direct, maternal, and sibsocial genetic effects on individual and colony traits in an ant

When social interactions occur, the phenotype of an individual is influenced directly by its own genes (direct genetic effects) but also indirectly by genes expressed in social partners (indirect genetic effects). Social insect colonies are characterized by extensive behavioral interactions among workers, brood, and queens so that indirect genetic effects are particularly relevant. I used a series of experimental manipulations to disentangle the contribution of direct effects, maternal (queen) effects, and sibsocial (worker) effects to variation for worker, gyne, and male mass; caste ratio; and sex ratio in the ant Temnothorax curvispinosus. The results indicate genetic variance for direct, maternal, and sibsocial effects for all traits, except for male mass there was no significant maternal variance, and for sex ratio the variance for direct effects was not separable from maternal variance for the primary sex ratio. Estimates of genetic correlations between direct, maternal, and sibsocial effects were generally negative, indicating that these effects may not evolve independently. These results have broad implications for social insect evolution. For example, the genetic architecture underlying social insect traits may constrain the realization of evolutionary conflicts between social partners.     

Inheritance of progeny sex ratio in Urtica dioica

Seed samples collected from female Urtica dioica plants in the field showed considerable inter-family variation in the sex ratio (faction of males). To investigate the inheritance pattern of the sex ratio trait, crosses were performed between individual male and female plants from different sex ratio families. Our results suggest, at least for the families studied here, that maternal parents strongly contribute to the variation in the primary sex ratio. Furthermore, progeny sex ratios from reciprocal crosses were significantly different and resembled the sex ratios produced by their maternal parents. We discuss the possible mechanisms underlying maternal control.     

SEX RATIO VARIATION IN THE LESSONIA NIGRESCENS COMPLEX (LAMINARIALES,PHAEOPHYCEAE): EFFECT OF LATITUDE,TEMPERATURE, AND MARGINALITY1

Little is known about variation of sex ratio, the proportion of males to females, in natural populations of seaweed, though it is a major determinant of the mating system. The observation of sexual chromosomes in kelps suggested that sex is partly genetically determined. However, it is probably not purely genetic since the sex ratio can be modified by environmental factors such as salinity or temperature. In this paper, sex ratio variation was studied in the kelp Lessonia nigrescens Bory complex, recently identified as two cryptic species occurring along the Chilean coast: one located north and the other south of the biogeographic boundary at latitude 29°–30° S. The life cycle of L. nigrescens is characterized by an alternation of microscopic haploid gametophytic individuals and large macroscopic fronds of diploid sporophytes. The sex ratio was recorded in progenies from 241 sporophytic individuals collected from 13 populations distributed along the Chilean coast in order (i) to examine the effect of an environmental gradient coupled with latitude, and (ii) to compare marginal populations to central populations of the two species. In addition, we tested the hypothesis that the sex ratios of the two cryptic species would be affected differently by temperature. First, our results demonstrate that sex ratio seems to be mainly genetically determined and temperature can significantly modify it. Populations of the northern species showed a lower frequency of males at 14°C than at 10°C, whereas populations of the southern species showed the opposite pattern. Second, both species displayed an increased variation in sex ratio at the range limits. This greater variation at the margins could be due either to differential mortality between sexes or to geographic parthenogenesis (asexual reproduction).     

Individual variation in body color in the field cricket Teleogryllus occipitalis (Orthoptera: Gryllidae)

Body color of animals may affect individual fitness through direct effects on various processes, such as predatory avoidance, thermoregulation, UV resistance, and mating behavior. Body color variation of the field cricket Teleogryllus occipitalis (Audinet‐Serville) (Orthoptera: Gryllidae) is often observed. We quantified the individual variation in body color of this species by measuring the luminance of hind leg femur. Thereafter, we examined whether the body color was a heritable trait or not using parent–offspring analysis. In addition, the effect of body color of both parents on body size, sex ratio, and survival rate of progeny was investigated. The results showed that maternal body color was not heritable, whereas paternal body color was correlated with the body color of the progeny. Body size and sex ratio were not correlated with body color of parents. Although paternal body color did not affect the survival rate of the progeny beyond the stage of final instar nymph, progeny survival rate significantly increased with darkness of maternal body.     

High‐throughput behavioral phenotyping in the expanded panel of BXD recombinant inbred strains

Genetic reference populations, particularly the BXD recombinant inbred (BXD RI) strains derived from C57BL/6J and DBA/2J mice, are a valuable resource for the discovery of the bio‐molecular substrates and genetic drivers responsible for trait variation and covariation. This approach can be profitably applied in the analysis of susceptibility and mechanisms of drug and alcohol use disorders for which many predisposing behaviors may predict the occurrence and manifestation of increased preference for these substances. Many of these traits are modeled by common mouse behavioral assays, facilitating the detection of patterns and sources of genetic coregulation of predisposing phenotypes and substance consumption. Members of the Tennessee Mouse Genome Consortium (TMGC) have obtained phenotype data from over 250 measures related to multiple behavioral assays across several batteries: response to, and withdrawal from cocaine, 3,4‐methylenedioxymethamphetamine; “ecstasy” (MDMA), morphine and alcohol; novelty seeking; behavioral despair and related neurological phenomena; pain sensitivity; stress sensitivity; anxiety; hyperactivity and sleep/wake cycles. All traits have been measured in both sexes in approximately 70 strains of the recently expanded panel of BXD RI strains. Sex differences and heritability estimates were obtained for each trait, and a comparison of early (N = 32) and recent (N = 37) BXD RI lines was performed. Primary data are publicly available for heritability, sex difference and genetic analyses using the MouseTrack database, and are also available in GeneNetwork.org for quantitative trait locus (QTL) detection and genetic analysis of gene expression. Together with the results of related studies, these data form a public resource for integrative systems genetic analysis of neurobehavioral traits.