Male life history and the unusual adult sex ratios of redfronted lemur, Eulemur fulvus rufus, groups

In group-living species, theoretical considerations indicate the existence of a fundamental conflict of interest between the sexes over the adult sex ratio within groups. Females may derive certain benefits from living with many males. Males, in contrast, should generally try to monopolize access to a group of females. Which sex ultimately controls adult group sex ratio is poorly known. We examined this conflict between the sexes in redfronted lemurs, Malagasy primates characterized by an unusual lack of female-biased adult sex ratios. Using various demographic and behavioural data from several groups collected over 6 years, we examined (1) the proximate determinants of this unusual sex ratio, (2) the temporal distribution of female fertile phases within groups as a determinant of male monopolization potential, (3) sources of between-group variation in the adult sex ratio, and (4) possible social benefits of the relatively high number of males for both sexes. Birth and mortality rates were not sex biased and males migrated considerably more frequently than females, providing no proximate explanation for the unusual sex ratio. However, certain life history traits (fast maturation, short interbirth intervals) may ultimately play a role because they act to facilitate joint group transfers of male coalitions. Despite a relatively small female group size and an associated high monopolization potential, female oestrous synchrony may prevent the formation of single-male groups. Reduced male group size seems to be the main predictor of take-over rate, and, thus, infanticide risk, suggesting that both sexes may benefit from the high number of coresident males, thereby considerably defusing the conflict of interest between the sexes.     

Male work and sex ratio in social crab spiders

Summary: Biased sex ratios may alter the contribution that individuals of either sex make to group living. Such a possibility has not been examined in social spiders, in part as adult male spider anatomy and behaviour are focussed on mating. Subadult male behaviour was examined in two congener social crab spiders that have similar ecological niches, Diaea ergandros with an equal sex ratio and D. socialis with a female-biased sex ratio. A laboratory experiment that varied sex ratios of groups of subadults of the two species found that nest construction in D. ergandros did not vary with sex ratio, but that of D. socialis did as males did not contribute to nest construction. This may suggest that among social species, biased sex ratios might influence the appearance of drone-like behaviour.     

Novel genetic sex markers reveal high frequency of sex reversal in wild populations of the agile frog (Rana dalmatina) associated with anthropogenic land use

Populations of ectothermic vertebrates are vulnerable to environmental pollution and climate change because certain chemicals and extreme temperatures can cause sex reversal during early ontogeny (i.e. genetically female individuals develop male phenotype or vice versa), which may distort population sex ratios. However, we have troublingly little information on sex reversals in natural populations, due to unavailability of genetic sex markers. Here, we developed a genetic sexing method based on sex‐linked single nucleotide polymorphism loci to study the prevalence and fitness consequences of sex reversal in agile frogs (Rana dalmatina). Out of 125 juveniles raised in laboratory without exposure to sex‐reversing stimuli, 6 showed male phenotype but female genotype according to our markers. These individuals exhibited several signs of poor physiological condition, suggesting stress‐induced sex reversal and inferior fitness prospects. Among 162 adults from 11 wild populations in North‐Central Hungary, 20% of phenotypic males had female genotype according to our markers. These individuals occurred more frequently in areas of anthropogenic land use; this association was attributable to agriculture and less strongly to urban land use. Female‐to‐male sex‐reversed adults had similar body mass as normal males. We recorded no events of male‐to‐female sex reversal either in the laboratory or in the wild. These results support recent suspicions that sex reversal is widespread in nature, and suggest that human‐induced environmental changes may contribute to its pervasiveness. Furthermore, our findings indicate that sex reversal is associated with stress and poor health in early life, but sex‐reversed individuals surviving to adulthood may participate in breeding.     

Reproductive success in reindeer males in a herd with varying sex ratio

In polygynous species, male reproductive success is often correlated with dominance status of individual males and sex ratio in the population. Reindeer, Rangifer tarandus, is a polygynous species, and here we compared the variation in male reproductive success and dominance status during two successive years in a herd with a male:female sex ratio of 1:7 and 1:3. Copulations were recorded, together with data on male dominance hierarchy and size of mating groups. Male reproductive success was estimated by paternity analysis of calves using microsatellite DNA markers. The distribution of reproductive success among the males was highly skewed for both years with the most dominant male also being the most successful. The largest mating group was established in the herd with the least skew in sex ratio. In this herd some of the adult males present were less reproductively successful than some of the more subordinate younger males. Estimates of the mating group size of males, correcting for dominance status when more than one male is present in the groups, gave good prediction of individual males' reproductive success.     

Sexual dimorphism and intraspecific aggression,and their relationship to sex ratios in Caprella gorgonia Laubitz & Lewbel (Crustacea: Amphipoda: Caprellidae)

The amphipod Caprella gorgonia Laubitz & Lewbel is an obligate commensal on gorgonian octocorals. Its primary host is Lophogorgia chilensis (Verrill), found below 20 m.C. gorgonia breeds throughout the year, with wide fluctuations in abundance. Mating and oviposition follow molting. Sex reversal does not occur; two distinct sexes are present from the first instar after emergence from the brood pouch.Young males and females grow at approximately the same rate, but males are larger by a relatively constant increment. Males continue to grow at their original rate to a maximum size (about twice that of females). The growth rate of females is not limited by the onset of reproduction and brooding, but rather by an approach to maximum size when the rate is greatly reduced. Fecundity of females is not affected by size.The population sex ratio is about 1:3 (males:females), and about 1:4 among adults. The secondary sex ratio is 1:1. The post-emergence sex ratio bias is a result of heavier mortality among males. Sex ratios drop from 50% at emergence to 25% as females approach maximum size, then rise to 100% in larger size classes.Differential predation on males did not appear to be a source of any sex ratio bias. Adult males possess a “poison spine”, a puncturing weapon on the large second gnathopod, which functions in mating-related intraspecific combat with other males. Intraspecific male aggression during mating is a major cause of sex ratio bias. In the laboratory, increased density in breeding groups may affect mortality due to male aggression. In nature, adult sex ratios are negatively correlated with population density. The reproductive capacity of the population is not limited by a shortage of adult males, despite the low adult sex ratio.     

The influence of females on the initiation of female-to-male sex change in a coral reef fish

In the protogynous coral reef fish Anthias squamipinnis (Peters), all males are sex-reversed females. A sexually mature female can be induced to change sex by removing a male from her social group. The influence of non-sex-changing females on the initiation of sex change was evaluated in 109 social groups in the Gulf of Eilat. When the male and largest female were removed from each of 12 single-male groups, the second-largest female changed sex in 9 groups. This result distinguished between two behavioral hypotheses suggested by previous work and made it tenable that a particular behavioral measure, the profile of behavior-received, that depends on adult females, is critical to the initiation of sex change. This species forms all-female groups as well as bisexual groups. All-female groups can be expected to have some mechanism for the production of a male. The removal of the largest female from each of 8 all-female groups failed to induce sex change in any group. The dominant female in these groups thus does not function in the same way as does the male in bisexual groups, at least in terms of the initiation of sex change. Following the removal of the male from each of 8 bisexual groups containing five or fewer adult females, a female changed sex in only 4 groups. This 50% incidence of sex reversal was lower than the 77–80% incidence in control groups containing more than five adult females. Data suggest that a minimum of four adult females is probably required for the probability of sex change after male removal to equal 75%.     

The influence of increased line-fishing mortality on the sex ratio and age of sex reversal of the venus tusk fish

The age of sex reversal of the venus tusk fish Choerodon venustus , caught by line fishing at various locations on the southern Great Barrier Reef, indicated that C. venustus is capable of modifying its life cycle in response to increased mortality. The evidence suggests Masthead Reef fish, which experience the highest mortality, underwent sex reversal at a smaller size and younger age than at the other sites. The largest female fish, sexually transitional fish and males were smaller at Masthead Reef than at the Swains Reefs or One Tree Reef at Masthead Reef. There was also considerable overlap in the size of males and females within the exploited populations indicating that sex reversal is not initiated at a particular length but may have a social cause. The sex ratio of fish was essentially the same for fish fully susceptible to line fishing in the Swains and Masthead samples. Circumstantial evidence suggested that the absence of large males in a population may initiate sex reversal, indicating the maintenance of a constant sex ratio may have a social basis.     

Crowd control: sex ratio affects sexually selected cuticular hydrocarbons in male Drosophila serrata

Although it is advantageous for males to express costly sexually selected signals when females are present, they may also benefit from suppressing these signals to avoid costly interactions with rival males. Cuticular chemical profiles frequently function as insect sexual signals; however, few studies have asked whether males alter these signals in response to their social environment. In Drosophila serrata, an Australian fly, there is sexual selection for a multivariate combination of male cuticular hydrocarbons (CHCs). Here, we show that the ratio of females to males that an adult male experiences has a strong effect on his CHC expression, with female‐biased adult sex ratios eliciting greater expression of CHC profiles associated with higher male mating success. Classical models predict that male reproductive investment should be highest when there is a small but nonzero number of rivals, but we found that males expressed the most attractive combination of CHCs when there were no rivals. We found that male CHCs were highly sensitive to adult sex ratio, with males expressing higher values of CHC profiles associated with greater mating success as the ratio of females to males increased. Moreover, sex ratio has a stronger effect on male CHC expression than adult density. Finally, we explore whether sex ratio affects the variance among a group of males in their CHC expression, as might be expected if individuals respond differently to a given social environment, but find little effect. Our results reveal that subtle differences in social environment can induce plasticity in male chemical signal expression.     

Complex sex allocation in the laughing kookaburra

In groups of the cooperatively breeding laughing kookaburra(Dacelo novaeguineae), offspring sex varied with the type ofsocial group and with hatch rank. Groups with female helpers,especially if all helpers were female, had male-biased clutchand fledging sex ratios. Groups without female helpers (unassistedpairs or male-only helpers) had female-biased clutch and fledgingsex ratios. Breeding females responded facultatively to increasesin the number of female helpers in their group by producingmore male eggs. These biases may occur if breeding femalestry to limit the number of daughters recruited into their groupbecause unlike male helpers, female helpers depress the breedingsuccess of their parents. Across all nests, two-thirds of first-hatchedyoung were male, two-thirds of second-hatched young were female, and the sex ratio of third-hatched young was even. Hatch ranksex ratios also varied dramatically between different typesof social groups, from 16.7% for second-hatched nestlings ofunassisted pairs to 100% for first-hatched nestlings of groupswith only female helpers. A corollary of the relationship betweenhatch rank and sex was that hatching sex sequences were distributed nonrandomly: all groups avoided hatching a daughter first followedby a son (FM). Sibling competition is aggressive and sometimesfatal. Since females grow to be 15% larger than males the hatchingsequence of sexes could affect nestling growth and mortality.However, an exhaustive analysis found little evidence thatgrowth or survival of males was compromised if hatched aftera sister. The small number of FM sequences may only have occurredin nests that were able to ameliorate any negative consequences.Alternatively, when clutch size is small and fledging successunpredictable because of brood reduction, the preferred broodsex ratio may be contingent on the number of fledged young,making it advantageous to order the sexes in the brood.     

A model for environmental sex reversal in fish

A mathematical model is presented which combines genetic XX-female/XY-male sex determination with environmental pressure for phenotypic sex reversal. This may occur when fishes are exposed to endocrine disrupters, specifically masculinization by exposure to androgens and feminization by exposure to estrogens. A generic model is derived for the sex ratio in successive generations and three special cases, with chronic and constant pressure to sex reverse, are discussed in detail. These show that, with extreme environmental pressure to masculinize, the male genotype is at risk of dying out but with less extreme pressure, masculinization will not be detectable since the proportion of phenotypic males becomes one-half. With feminization at any pressure to sex reverse, the male and female genotypes will be maintained in a stable sex ratio in which the proportion of genotypic males exceeds one-half and is close to one-half if YY offspring (eggs) are not viable. In converse, the model is also applicable to the genetic ZZ-male/ZW-female system of sex determination in fish. At present suitable data are not available with which to validate the model, but proposals are made for relevant experimental studies.     

Distinguishing behavioral interactions from visual cues as causes of adult sex change in a coral reef fish

Two experiments tested the hypothesis that adult female-to-male sex reversal in protogynous fish is induced by the loss of close-contact behavioral interactions between males and females, and not by the loss of simple visual cues from the male. Twenty-six laboratory groups of Anthias squamipinnis were manipulated so that females within each group (1) retained chemical and acoustic access to a male, (2) were denied behavioral access to a male, and (3) were either allowed or denied visual access to a male alone or to a male interacting with another female. At least one female subsequently changed sex in each of 22 groups. While acoustic and chemical cues were not completely eliminated as possible causes, sex change is apparently induced by loss of male-female behavioral interaction in combination with continued interaction between females.     

Induced sex change in black sea bass

Experiments were conducted to identify factors involved in sex change in the protogynous black sea bass Centropristis striata . Black sea bass maintained in the ratio of 8 females (F):0 males (M) for 9 months reversed sex while those kept at the ratios of 6F:2M or 4F:4M did not. Female black sea bass implanted with 1·0 mg 11-ketotestosterone (11-KT) or 10 mg fadrozole (FAD) changed sex and began spermiating while those implanted with 0·1 mg 11-KT or 1·0 mg FAD underwent incomplete sex reversal. One fish implanted with 1·0 mg FAD initiated sex change but was not spermiating at the end of the study. One fish in the control group, the largest fish in the study, initiated sex change. These results suggest that the presence of males may restrict sex reversal in black sea bass and that high 17β-oestradiol:11-KT is required for maintaining ovarian function.     

An analysis of birth sex ratio bias in captive prosimian species

The extent to which sex ratio bias is a common reproductive characteristic of prosimians has not been well established. The present study analyzed reproduction in 13 breeding groups of captive prosimians for evidence of birth sex ratio bias. A substantial male bias was demonstrated in nongregarious, but not gregarious, breeding groups. Analyses of birth sex ratios of individual mothers suggested that the observed bias did not result from the tendency of a few mothers to overproduce males, but rather from a small but reliable excess of male births in general. An examination of infant mortality revealed that male Otolemur garnettii and Microcebus murinus infants were more vulnerable to preweaning mortality, whereas female Eulemur fulvus albifrons infants were more vulnerable. An analysis of birth order by sex found that mothers of one group (O. garnettii) tended to produce males initially and females later. Additionally, a distinct pattern of birth seasonality was noted among Malagasy prosimians that was absent in the African prosimians. Greater length of period of sexual receptivity for nongregarious females as compared to gregarious females is proposed as a possible mechanism of male birth sex ratio bias. © 1996 Wiley-Liss, Inc.     

The primary sex ratio under environmental sex determination

The ESS primary sex ratio (male/female) under environmental sex determination (ESD) is shown to be equal to the ratio of the average fertility of a female to the average fertility of a male. Thus, depending upon how male and female fertility change over the environmental variable causing ESD, the primary sex ratio may be either male or female biased, or neither. The primary sex ratio thus contains information as to how male and female fertilities change with the environment.     

The proximate determinants of sex ratio in C. elegans populations

The soil nematode Caenorhabditis elegans is an example of a species in which self-fertilizing hermaphrodites predominate, but functional males continue to persist--allowing outcrossing to persevere at low levels. Hermaphrodites can produce male progeny as a consequence of sex chromosome non-disjunction or via outcrossing with males. Consequently, the genetics of sex determination coupled with the efficiency by which males find, inseminate and obtain fertilizations with hermaphrodites will influence the frequency at which males and outcrossing occurs in such populations. Behavioural and physiological traits with a heritable basis, as well as ecological characters, may influence male reproductive success and therefore sex ratio. Because sex ratio is tied to male reproductive success, sex ratio greatly affects outcrossing rates, patterns of genetic variation, and the ability of natural selection to act within populations. In this paper we explore the determinants of male frequency in C. elegans with a mathematical model and experimental data. We address the role of the genetic machinery of sex determination via sex chromosome non-disjunction on sex ratio and the influence of physiological components of C. elegans' life history that contribute to variation in sex ratio by way of male reproductive success. Finally, we discuss the short-term and long-term factors that are likely to affect sex ratio and breeding system evolution in species like C. elegans.     

The effect of size and sex ratio experiences on reproductive competition in Nicrophorus vespilloides burying beetles in the wild

Male parents face a choice: should they invest more in caring for offspring or in attempting to mate with other females? The most profitable course depends on the intensity of competition for mates, which is likely to vary with the population sex ratio. However, the balance of pay‐offs may vary among individual males depending on their competitive prowess or attractiveness. We tested the prediction that sex ratio and size of the resource holding male provide cues regarding the level of mating competition prior to breeding and therefore influence the duration of a male's biparental caring in association with a female. Male burying beetles, Nicrophorus vespilloides were reared, post‐eclosion, in groups that differed in sex ratio. Experimental males were subsequently translocated to the wild, provided with a breeding resource (carcass) and filmed. We found no evidence that sex ratio cues prior to breeding affected future parental care behaviour but males that experienced male‐biased sex ratios took longer to attract wild mating partners. Smaller males attracted a higher proportion of females than did larger males, securing significantly more monogamous breeding associations as a result. Smaller males thus avoided competitive male–male encounters more often than larger males. This has potential benefits for their female partners who avoid both intrasexual competition and direct costs of higher mating frequency associated with competing males.     

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.