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).     

Treatment with an aromatase inhibitor suppresses high-temperature feminization of genetic male (YY) Nile tilapia

High temperature (36° C) treatment during sexual differentiation caused significant changes in sex ratio in YY male Nile tilapia Oreochromis niloticus fry (64.5% males compared to 100.0% males at 28° C), while dietary treatment with a chemical aromatase inhibitor (AI: Fadrozole™ CGS16949A) during this period suppressed the high temperature feminization (98.9% males). This implies that cytochrome P450 aromatase is mechanistically associated with temperature-dependent sex determination (TSD) in this species. XY male fry did not show significant sex reversal at 36° C. In XX female fry, high temperature treatment resulted in significant masculinization (62.5% males compared with 21.9% males at 28° C), while treatment with AI at either temperature resulted in very high proportions of males (100.0% males at 36° C; 99.0% males at 28° C). These results confirm the importance of aromatase in sexual differentiation in the Nile tilapia below the TSD threshold and suggest that it also plays a role in TSD, at least in the YY genotype.     

Sex change in the subdioecious shrub Eurya japonica (Pentaphylacaceae)

Sex change affects the sex ratios of plant populations and may play an essential role in the evolutionary shift of sexual systems. Sex change can be a strategy for increasing fitness over the lifetime of a plant, and plant size, environmental factors, and growth rate may affect sex change. We described frequent, repeated sex changes following various patterns in a subdioecious Eurya japonica population over five successive years. Of the individuals, 27.5% changed their sex at least once, and these changes were unidirectional or bidirectional. The sex ratio (females/males/all hermaphrodite types) did not fluctuate over the 5 years. In our study plots, although the current sex ratio among the sexes appears to be stable, the change in sex ratio may be slowly progressing toward increasing females and decreasing males. Sex was more likely to change with higher growth rates and more exposure to light throughout the year. Among individuals that changed sex, those that were less exposed to light in the leafy season and had less diameter growth tended to shift from hermaphrodite to a single sex. Therefore, sex change in E. japonica seemed to be explained by a response to the internal physiological condition of an individual mediated by intrinsic and abiotic environmental factors.     

The importance of cytoplasmic male killing elements in natural populations of the two spot ladybird, Adalia bipunctata (Linnaeus) (Goleoptera: Goccinellidae)

Adalia bipunctata , the two spot ladybird, is polymorphic for a cytoplasmically inherited element which produces female-biased sex ratios by effecting the death of male offspring during embryogenesis. The levels of this element were assessed in Cambridge populations. Six out of 82 females tested showed both a female-biased sex ratio and low egg hatch rates consistent with the presence of this element. Population sex ratios were assessed by collecting pupae from the Cambridge area. The population sex ratio was found to be 1.15: 1, female biased, significantly different from 1:1, and consistent with predictions based on a model incorporating the observed level of the sex ratio element in the population.     

REPLICATED ORIGIN OF FEMALE‐BIASED ADULT SEX RATIO IN INTRODUCED POPULATIONS OF THE TRINIDADIAN GUPPY (POECILIA RETICULATA)

There are many theoretical and empirical studies explaining variation in offspring sex ratio but relatively few that explain variation in adult sex ratio. Adult sex ratios are important because biased sex ratios can be a driver of sexual selection and will reduce effective population size, affecting population persistence and shapes how populations respond to natural selection. Previous work on guppies (Poecilia reticulata) gives mixed results, usually showing a female‐biased adult sex ratio. However, a detailed analysis showed that this bias varied dramatically throughout a year and with no consistent sex bias. We used a mark‐recapture approach to examine the origin and consistency of female‐biased sex ratio in four replicated introductions. We show that female‐biased sex ratio arises predictably and is a consequence of higher male mortality and longer female life spans with little effect of offspring sex ratio. Inconsistencies with previous studies are likely due to sampling methods and sampling design, which should be less of an issue with mark‐recapture techniques. Together with other long‐term mark‐recapture studies, our study suggests that bias in offspring sex ratio rarely contributes to adult sex ratio in vertebrates. Rather, sex differences in adult survival rates and longevity determine vertebrate adult sex ratio.     

Female common lizards (Lacerta vivipara) do not adjust their sex-biased investment in relation to the adult sex ratio

Sex allocation theory predicts that facultative maternal investment in the rare sex should be favoured by natural selection when breeders experience predictable variation in adult sex ratios (ASRs). We found significant spatial and predictable interannual changes in local ASRs within a natural population of the common lizard where the mean ASR is female-biased, thus validating the key assumptions of adaptive sex ratio models. We tested for facultative maternal investment in the rare sex during and after an experimental perturbation of the ASR by creating populations with female-biased or male-biased ASR. Mothers did not adjust their clutch sex ratio during or after the ASR perturbation, but produced sons with a higher body condition in male-biased populations. However, this differential sex allocation did not result in growth or survival differences in offspring. Our results thus contradict the predictions of adaptive models and challenge the idea that facultative investment in the rare sex might be a mechanism regulating the population sex ratio.     

Do operational sex ratios influence sex allocation in viviparous lizards with temperature‐dependent sex determination?

Under certain environmental situations, selection may favour the ability of females to adjust the sex ratio of their offspring. Two recent studies have suggested that viviparous scincid lizards can modify the sex ratio of the offspring they produce in response to the operational sex ratio (OSR). Both of the species in question belong to genera that have also recently been shown to exhibit temperature-dependent sex determination (TSD). Here we test whether pregnant montane water skinks (Eulamprus tympanum) utilise TSD to select offspring sex in response to population wide imbalances in the OSR, by means of active thermoregulation. We use a combination of laboratory and field-based experiments, and conduct the first field-based test of this hypothesis by maintaining females in outdoor enclosures of varying OSR treatments throughout pregnancy. Although maternal body temperature during pregnancy was influenced by OSR, the variation in temperature was not great enough to affect litter sex ratios or any other phenotypic traits of the offspring.     

Life-history and sex allocation in Trypoxylon (syn. Trypargilum) lactitarse (Hymenoptera; Crabronidae)

Hymenopterans have become a model for the study of factors that govern sex allocation. In 1983, Seger proposed a model to study Sphecidae wasps with a strong prediction that sex ratio for univoltine wasps should be 1 : 1 (female : male), and for partially bivoltine species it should be male-biased. The present study investigates if Trypoxylon lactitarse (Saussure, 1867) is a univoltine or a bivoltine species and if Seger's model prediction fits the pattern of sex ratio found in this species. The study was carried out at Parque Municipal das Araucárias, in the municipality of Guarapuava, state of Paraná, southern Brazil, from December 2001 to December 2004. Nests of T. lactitarse were obtained using trap-nests drilled longitudinally to a depth to 80 mm with 7.0, 10.0 and 13.0 mm opening diameter. They were placed in a very heterogeneous site filled with araucaria forests, swamps and grasslands. Trypoxylon lactitarse showed two alternative life histories: either they pupated immediately and emerged as adults later in the same season (direct development), or they entered diapause, overwintering and pupating the following spring (delayed development). Its annual sex ratios were not significantly different from 1 : 1, and both sex ratio of overwintering and sex ratio of direct-developing wasps were also not significantly different from 1 : 1, in all years of this study. By examining these results, it was possible to conclude that although T. lactitarse is a multivoltine species, with four generations per year and two alternative life histories, its sex ratio did not support Seger's model.     

Effect of Aedes aegypti (Diptera:Culicidae) Age on Sex Ratios in Romanomermis culicivorax (Nematoda:Mermithidae)

First, second, third, early and late fourth-instar larvae, and pupae of Aedes aegypti were infected with Romanomerrais culicivorax and reared at 20, 25, and 30 C. An increase in the ratio of male to female nematodes was observed with increase in host age at the time of infection at each temperature. The number of pupal and late fourth-instar infections was low, but R. culicivorax continued to develop in adult A. aegypti. Since male nematodes were recovered from both male and female hosts infected as late fourth instars or pupae, the sex of the host did not influence the sex of the nematode.     

Heritability of sex tendency in a harpacticoid copepod,Tigriopus californicus

Abstract.— Systems with genetic variation for the primary sex ratio are important for testing sex-ratio theory and for understanding how this variation is maintained. Evidence is presented for heritable variation of the primary sex ratio in the harpacticoid copepod Tigriopus californicus. Variation in the primary sex ratio among families cannot be accounted for by Mendelian segregation of sex chromosomes. The covariance in sex phenotype between full-sibling clutches and between mothers and offspring suggests that this variation has a polygenic basis. Averaged over four replicates, the full-sibling heritability of sex tendency is 0.13 ± 0.040; and the mother-offspring heritability of sex tendency is 0.31 ± 0.216. Genetic correlations in the sex phenotype across two temperature treatments indicate large genotype-by-temperature interactions. Future experiments need to distinguish between zygotic, parental, or cytoplasmic mechanisms of sex determination in T. californicus.     

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.     

Sex ratio variation as a function of host size in Pseudacteon flies (Diptera: Phoridae), parasitoids of Solenopsis fire ants (Hymenoptera: Formicidae)

Some Pseudacteon (Diptera: Phoridae) flies are parasitoids of Solenopsis (Hymenoptera: Formicidae) ant workers in North and South America. Laboratory studies of sex allocation revealed a pattern of sex ratio variation as a function of host size, with more females arising from larger hosts. Environmental sex determination is a possible mechanism for the observed pattern, and examination of Pseudacteon life history reveals several traits assumed to be important in models predicting conditions under which environmental sex determination is favoured. Sex allocation patterns of Pseudacteon are compared with theoretical predictions and empirical data from better-studied hymenoptcran parasitoids that have haplodiploid sex determination. The pattern of sex ratio variation observed has important implications for biocontrol efforts of imported Solenopsis fire ants by the introduction of Pseudacteon parasitoids.     

Thermolabile Sex Determination in honmoroko

In six pairings (one female × three males and vice versa) of honmoroko Gnathopogon caerulescens , although in one pairing the sex ratio of the offspring did not deviate significantly from 1:1, in four pairings the proportion of females decreased significantly with an increase in temperature. Heavy mortality due to disease was observed in the remaining pair. There were highly significant differences in sex ratios among the broods produced by different mothers with the same father and vice versa, and the response of sex ratio to temperature treatments differed considerably within pairings. The progeny of five out of 20 males produced at 34°C were almost all females, two were male-biased, and the remaining had balanced (1:1) sex ratios. These results suggest that the sex determination system in honmoroko is close to female homogamety but is influenced by temperature, genetic factors and genotype-temperature interactions.     

Lowered female reproductive effort as an indicator for increased male production and sexuality in Daphnia (Crustacea: Cladocera)

Summary

The relationship between environmental factors, sex ratio, mode of reproduction, and female reproductive effort was examined in the cyclically parthenogenetic Daphnia magna. Female reproductive effort was found to decline before a significant production of males and sexual eggs takes place. Unlike factors such as crowding, poor nourishment, low (sometimes high) temperature and short or long day length, lowered reproductive effort is not a cue but rather an indicator of the selective advantage that would accrue from a changed sex ratio and mode of reproduction. The mechanism of the complex system of environmental sex determination in Daphnia is reviewed, and the adaptivity of ESD is discussed.     

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.     

Laboratory and field studies on the reproductive ecology of Parocneria orienta (Lepidoptera: Lymantriidae) in China

To lay a foundation for the monitoring, prevention and control of Parocneria orienta, a pest moth in China, we investigated the reproductive ecology of P. orienta, including the environmental factors affecting reproduction and the effects of pheromones in field traps. The results showed that the mating duration is shorter when the temperature is higher, with the optimal temperature range for P. orienta reproduction being 22–27°C. The sex ratio had an effect on the male mating capacity, which significantly increased when the sex ratio was ♀:♂ ≥ 3:1. The average number of matings was 2.44 for males, while female P. orienta mated only once in a lifetime. Males were more attracted to virgin females than to mated females, and the temperature and light period had an effect on the release of sex pheromones by females. Field trap tests using virgin females supported the results obtained in the laboratory, showing that the release of sex pheromones by P. orienta follows a distinct circadian rhythm.     

Facultative sex allocation in snow skink lizards (Niveoscincus microlepidotus)

Mathematical models suggest that reproducing females may benefit by facultatively adjusting their relative investment into sons vs. daughters, in response to population‐wide shifts in operational sex ratio (OSR). Our field studies on viviparous alpine skinks (Niveoscincus microlepidotus) document such a case, whereby among‐ and within‐year shifts in OSR were followed by shifts in sex allocation. When adult males were relatively scarce, females produced male‐biased litters and larger sons than daughters. The reverse was true when adult males were relatively more common. That is, females that were courted and mated by few males produced mainly sons (and these were larger than daughters), whereas females that were courted and mated by many males produced mainly daughters (and these were larger than sons). Maternal body size and condition also covaried with sex allocation, and the shifting pattern of sexual size dimorphism at birth may reflect these correlated effects rather than a discrete component of an evolved sex‐allocation strategy.     

SEX RATIO VARIATION IN A PARASITIC WASP I. REACTION NORMS

To understand genetic and phenotypic constraints on the sex ratio in a parasitic wasp that attacks fly pupae, I carried out a laboratory study of sex ratio variability in five strains of Muscidifurax raptor (Hymenoptera: Pteromalidae). I manipulated the environment through combinations of temperature and day length, and the numbers of females that attack a group of hosts. The change of phenotype in each strain over the range of environmental conditions describes the norm of each reaction for that strain, and measures how a strain responds to environmental variation to create phenotypic variability. Sex ratio in parasitic wasps is a complex trait that has several components—the numbers of eggs laid by an ovipositing wasp and the fraction of eggs that are fertilized (female). Further, sex ratio may be influenced by a female's reaction to other females exploiting the same hosts (superparasitism). I found no strain-environment interactions in either sex ratio or fecundity when I varied environmental conditions. Although strains differed in sex ratio and fecundity, all strains produced a more female-biased sex ratio and had higher fecundity when temperature and day length increased. Sex ratio and fecundity were phenotypically correlated, and strains with greater fecundity also produced a more female-biased sex ratio. All strains facultatively shifted sex ratio toward a higher fraction of males with increasing female density, despite apparent differences in superparasitism among strains. Males and females survived equally during development, so that mortality differences among strains and across environments could not account for sex ratio variability. This study indicates that sex ratio variability among strains is constrained by the correlation between sex ratio and fecundity, and that strains display similar facultative shifts in sex ratio as female density increases because sex ratio shifts are insensitive to differing levels of superparasitism.     

SEX RATIO SELECTION AND THE EVOLUTION OF ENVIRONMENTAL SEX DETERMINATION IN LABORATORY POPULATIONS OF MENIDIA MENIDIA

What happens when a population with environmental sex determination (ESD) experiences a change to an extreme environment that causes a highly unbalanced sex ratio? Theory predicts that frequency-dependent selection would increase the proportion of the minority sex and decrease the level of ESD in subsequent generations. We empirically modeled this process by maintaining five laboratory populations of a fish with temperature-dependent sex determination (the Atlantic silverside, Menidia menidia) in extreme constant temperature environments that caused highly skewed sex ratios to occur initially. Increases in the minority sex consistently occurred from one generation to the next across all five populations, first establishing and then maintaining a balanced sex ratio until termination of the experiment at 8 to 10 generations. The extent to which the level of ESD changed as balanced sex ratios evolved, however, was not consistent. Two populations that experienced high temperatures each generation displayed a loss of ESD, and in one of these ESD was virtually eliminated. This suggests that temperature-insensitive, sex-determining genes were being selected. In populations maintained in low temperature environments, however, the level of ESD did not decline. Instead, the response of sex ratio to temperature was adjusted upward or downward, perhaps by selection of sex-determining genes sensitive to higher (or lower) temperatures. The two different outcomes at low versus high temperatures occurred independent of the geographic origin of the founding population. Our results demonstrate that ESD is capable of evolving in response to selection.     

Variable Female Mating Positions and Offspring Sex Ratio in the Spider Pityohyphantes phrygianus (Araneae: Linyphiidae)

Chromosomal sex determination and male heterogamety have been thought to seriously impede direct sex ratio control. However, in Pityohyphantes phrygianus, a solitary sheetweb spider with a skewed sex ratio, earlier experimental studies suggested that there are options for female control of offspring sex ratio, if females change their position during the normal mating sequence. Here we show that under natural conditions there is considerable between-female variation in positions, especially after termination of mating. Computer simulations of the orientation of female inner genitalia suggest that sperm are placed in different storage sites depending on the positions adopted. This means that a specific position after mating might potentially influence offspring sex ratio. The variance in offspring sex ratio among females in earlier experiments was binomially distributed, which leads us to conclude that females control the mean sex ratio but do not exercise direct control of the sex of individual offspring.