Biased Sex Ratios Research Articles

Evidence for Strategic Sex Allocation in the Guppy (Poecilia reticulata): Brood Sex Ratio and Size Predict Subsequent Adult Male Mating Success

Sex allocation theory predicts that females should produce more sons when the reproductive success of sons is expected to be high, whereas they should produce more daughters, not daughters when the reproductive success of sons is expected to be low. The guppy (Poecilia reticulata) is a live-bearing fish, and female guppies are known to produce broods with biased sex ratios. In this study, we examined the relationship between brood sex ratio and reproductive success of sons and daughters, to determine whether female guppies benefit from producing broods with biased sex ratios. We found that sons in male-biased broods had greater mating success at maturity than sons in female-biased broods when brood sizes were larger. On the other hand, the reproductive output of daughters was not significantly affected by brood sizes and sex ratios. Our results suggest that female guppies benefit from producing large, male-biased brood when the reproductive success of sons is expected to be high.

Sex allocation and sex‐specific parental investment in an endangered seabird

Biased offspring sex ratio is relatively rare in birds and sex allocation can vary with environmental conditions, with the larger and more costly sex, which can be either the male or female depending on species, favoured during high food availability. Sex‐specific parental investment may lead to biased mortality and, coupled with unequal production of one sex, may result in biased adult sex ratio, with potential grave consequences on population stability. The African Penguin Spheniscus demersus, endemic to southern Africa, is an endangered monogamous seabird with bi‐parental care. Female adult African Penguins are smaller, have a higher foraging effort when breeding and higher mortality compared with adult males. In 2015, a year in which environmental conditions were favourable for breeding, African Penguin chick production on Bird Island, Algoa Bay, South Africa, was skewed towards males (1.5 males to 1 female). Males also had higher growth rates and fledging mass than females, with potentially higher post‐fledging survival. Female, but not male, parents had higher foraging effort and lower body condition with increasing number of male chicks in their brood, thereby revealing flexibility in their parental strategy, but also the costs of their investment in their current brood. The combination of male‐biased chick production and higher female mortality, possibly at the juvenile stage as a result of lower parental investment in female chicks, and/or at the adult stage as a result of higher parental investment, may contribute to a biased adult sex ratio (ASR) in this species. While further research during years of contrasting food availability is needed to confirm this trend, populations with male‐skewed ASRs have higher extinction risks and conservation strategies aiming to benefit female African Penguin might need to be developed.

Dioecy in Amborella trichopoda: evidence for genetically based sex determination and its consequences for inferences of the breeding system in early angiosperms.

This work aimed to gain insight into the breeding system at the base of living angiosperms through both character state reconstructions and the study of sex ratios and phenotypes in the likely sister to all other living angiosperms, Amborella trichopoda . Sex phenotypes were mapped onto a phylogeny of basally diverging angiosperms using maximum parsimony. In parallel, sex ratios and phenotypes were studied over two consecutive flowering seasons in an ex situ population of A. trichopoda , while the sex ratio of an in situ population was also assessed. Parsimony analyses failed to resolve the breeding system present at the base of living angiosperms, but indicated the importance of A. trichopoda for the future elucidation of this question. The ex situ A. trichopoda population studied showed a primary sex ratio close to 1:1, though sex ratio bias was found in the in situ population studied. Instances of sexual instability were quantified in both populations. Sex ratio data support the presence of genetic sex determination in A. trichopoda , whose further elucidation may guide inferences on the breeding system at the base of living angiosperms. Sexual instability in A. trichopoda suggests the operation of epigenetic mechanisms, and the evolution of dioecy via a gynodioecious intermediate.

Linking loggerhead locations: using multiple methods to determine the origin of sea turtles in feeding grounds

Many marine megavertebrate taxa, including sea turtles, disperse widely from their hatching or birthing locations but display natal homing as adults. We used flipper tagging, satellite tracking and genetics to identify the origin of loggerhead turtles living in Amvrakikos Gulf, Greece. This location has been identified as hosting regionally important numbers of large-juvenile to adult sized turtles that display long-term residency and/or association to the area, and also presents a male biased sex ratio for adults. A total of 20 individuals were linked to nesting areas in Greece through flipper tagging and satellite telemetry, with the majority (16) associated with Zakynthos Island. One additional female was tracked from Amvrakikos Gulf to Turkey where she likely nested. Mitochondrial DNA mixed stock analyses of turtles captured in Amvrakikos Gulf (n = 95) indicated 82% of individuals originated from Greek nesting stocks, mainly from Zakynthos Island (63%), with lesser contributions from central Turkey, Cyprus and Libya. These results suggest that the male-biased sex ratio found in Amvrakikos Gulf may be driven by the fact that males breed twice as frequently on Zakynthos, resulting in their using foraging grounds of greater proximity to the breeding site. Conservation measures in localised foraging habitats for the protection of marine vertebrates, such as sea turtles, may have positive impacts on several disparate breeding stocks and the use of multiple methods to determine source populations can indicate the relative effectiveness of these measures.

Can the meiotic sex ratio explain the sex ratio bias in adult populations in the dioicous moss Drepanocladus lycopodioides?

Sex ratio variation is commonly observed in natural populations of many organisms with separate sexes and genetic sex determination, including bryophytes. Most bryophyte populations exhibit female-skewed expressed adult sex ratios, generally inferred from counts of sexually mature plants. For the rarely sexually reproducing perennial dioicous moss Drepanocladus lycopodioides, we showed that a female bias also exists in the genetic adult sex ratio, using a specifically designed molecular sex-associated marker. Here, we investigated whether the meiotic spore sex ratio contributes to the observed bias in genetic adult sex ratio in natural populations. Earlier attempts to study meiotic sex ratios have involved commonly cultivated ruderals that rapidly express sex in the laboratory. We established single-spore cultures from field-collected sporophytes from these populations and used the marker to assess the sex of individual sporelings. Spore germinability was (near) complete, and mortality among sporelings was virtually absent. The true meiotic sex ratio did not differ from equality, but strongly differed both from the observed genetic sex ratios in the natural adult populations, and from the European scale genetic sex ratio. We conclude that the biased population sex ratios in this species arise at life cycle stages after spore germination. Sexual dimorphism may selectively favour female proliferation during some phase of gametophyte development. Based on methodological progress, we successfully used a perennial study species with rare sexual reproduction, which significantly broadens the life history spectrum investigated in bryophyte sex ratio studies.

Utility of a Collaborative At‐Sea Sampling Program (CASP) for the California Spiny Lobster Commercial Fishery: Catch Characteristics and Implications for Management

AbstractFisheries management, including the development of fishery management plans (FMPs), requires the best available scientific information. To address this need, we piloted a collaborative at‐sea sampling program (CASP) among California commercial lobster fishermen, scientists, and fishery managers to develop scientifically rigorous protocols and collect, analyze, and interpret essential fisheries information (EFI). Significant differences in catch characteristics among three regions (South, North Coast, and Northwest Islands) were documented. Legal CPUE was generally similar among regions, whereas sublegal CPUE was consistently highest in the South, followed by the North Coast and Northwest Islands. Evaluation of size structure revealed that legal lobsters were significantly smaller, just larger than legal size, in the South than in the other two regions, suggesting a higher exploitation rate there. Despite this, the South had significantly more prerecruits than the northern regions, a fact not considered in present fishery models. We also found a female bias in the legal sex ratios in the north regions and in the sublegal sex ratios in all regions that could affect model parameters for trap vulnerability and reproductive capacity. A discrepancy in the average weight of legal lobster for the Northwest Islands was identified which has implications for the spawning potential ratio, a reference point that elicits management action. The regional variations in catch characteristics suggest that the California lobster fishery would benefit from using more sophisticated models that incorporate area‐based EFI to better inform the harvest control rules. This finding supports the recommendations of the lobster FMP scientific review panel and the interests of resource managers, with the CASP data illustrating the value of the additional EFI and a mechanism for obtaining it. The demonstrated utility of the CASP for both cross‐checking and providing additional data supports its ongoing use to inform management of the lobster fishery and as a model for other fisheries.

Altitudinal variation in somatic condition and reproductive investment of male Yunnan pond frogs (Dianrana pleuraden)

Comparisons between populations that differ in resource availability and in environmental variables affecting the intensity of male–male competition allow insights into the mechanisms shaping reproductive allocation. Here, we studied inter-population variation in male investments in testis size and sperm length across four populations of the Yunnan pond frog (Dianrana pleuraden) along an altitudinal gradient in western China. Male body condition, relative testis size and sperm length did not increase with altitude despite an increasing male bias in the operational sex ratio (OSR) in high altitude was recorded. Our results were inconsistent with previous prediction that increasing latitude and/or altitude should lead to a declining male reproductive investment in anurans due to shortening breeding seasons and declining resource availability. We found a positive correlation between body condition and testes mass along the altitudinal gradient, which was indicative of a condition-dependent expression of testis size. By contrast, we recorded a non-significant correlation between testes mass and OSR, suggesting that male–male competition did not result in increasing levels of sperm competition. A non-significant correlation between sperm length and testis mass suggested that the intensity of sperm competition can account for the variation in sperm length.

Reproductive Biology of Albacore Tuna (Thunnus alalunga) in the Western Indian Ocean.

The reproductive biology of albacore tuna, Thunnus alalunga, in the western Indian Ocean was examined through analysis of the sex ratio, spawning season, length-at-maturity (L50), spawning frequency and fecundity. From 2013 to 2015, a total of 923 female and 867 male albacore were sampled. A bias in sex ratio was found in favor of females with fork length (LF) < 100 cm. Using histological analyses and gonadosomatic index, spawning was found to occur between 10°S and 30°S, mainly to the east of Madagascar from October to January. Large females contributed more to reproduction through their longer spawning period compared to small individuals. The L50 (mean ± standard error) of female albacore was estimated at 85.3 ± 0.7 cm LF. Albacore spawn on average every 2.2 days within the spawning region and spawning months, from November to January. Batch fecundity ranged between 0.26 and 2.09 million oocytes and the relative batch fecundity (mean ± standard deviation) was estimated at 53.4 ± 23.2 oocytes g-1 of somatic-gutted weight. The study provides new information on the reproductive development and classification of albacore in the western Indian Ocean. The reproductive parameters will reduce uncertainty in current stock assessment models which will eventually assist the fishery to be sustainable for future generations.

Dmrt1 is necessary for male sexual development in zebrafish

The dmrt1 (doublesex and mab-3 related transcription factor 1) gene is a key regulator of sex determination and/or gonadal sex differentiation across metazoan animals. This is unusual given that sex determination genes are typically not well conserved. The mechanisms by which zebrafish sex is determined have remained elusive due to the lack of sex chromosomes and the complex polygenic nature of sex determination in domesticated strains. To investigate the role of dmrt1 in zebrafish sex determination and gonad development, we isolated mutations disrupting this gene. We found that the majority of dmrt1 mutant fish develop as fertile females suggesting a complete male-to-female sex reversal in mutant animals that would have otherwise developed as males. A small percentage of mutant animals became males, but were sterile and displayed testicular dysgenesis. Therefore zebrafish dmrt1 functions in male sex determination and testis development. Mutant males had aberrant gonadal development at the onset of gonadal sex-differentiation, displaying reduced oocyte apoptosis followed by development of intersex gonads and failed testis morphogenesis and spermatogenesis. By contrast, female ovaries developed normally. We found that Dmrt1 is necessary for normal transcriptional regulation of the amh (anti-Müllerian hormone) and foxl2 (forkhead box L2) genes, which are thought to be important for male or female sexual development respectively. Interestingly, we identified one dmrt1 mutant allele that co-operates with a linked segregation distorter locus to generate an apparent XY sex determination mechanism. We conclude that dmrt1 is dispensable for ovary development but necessary for testis development in zebrafish, and that dmrt1 promotes male development by transcriptionally regulating male and female genes as has been described in other animals. Furthermore, the strong sex-ratio bias caused by dmrt1 reduction-of-function points to potential mechanisms through which sex chromosomes may evolve.

Virility does not imply immensity: Testis size, accessory gland size and ejaculate depletion pattern do not evolve in response to experimental manipulation of sex ratio in Drosophila melanogaster

Sperm competition theory predicts that with increase in sperm competition, males either invest more in reproductive organ(s) and/or improve ejaculate investment. We test this idea using experimental evolution in Drosophila melanogaster. We maintained replicate populations of Drosophila melanogaster under male (M) and female (F) biased sex ratio regimes for more than a hundred generations with the result that males from the M regime evolved higher sperm competitive abilities relative to males from the F regime. In the present study, we measured the testes and the accessory gland size of virgin and singly mated males from the M and F regimes. The M and F males do not differ in either testis or accessory gland size. Additionally, ejaculate investment is not different in the M and F males, as measured by reduction in testis and accessory gland sizes. Thus, contrary to theoretical prediction and evidence from other species, we found that evolved differences in sperm competitive ability are not necessarily due to evolution of testis/accessory gland size or strategic ejaculate investment in these populations.

Developmental sexual dimorphism and the evolution of mechanisms for adjustment of sex ratios in mammals.

Sex allocation theory predicts biased offspring sex ratios in relation to local conditions if they would maximize parental lifetime reproductive return. In mammals, the extent of the birth sex bias is often unpredictable and inconsistent, leading some to question its evolutionary significance. For facultative adjustment of sex ratios to occur, males and females would need to be detectably different from an early developmental stage, but classic sexual dimorphism arises from hormonal influences after gonadal development. Recent advances in our understanding of early, pregonadal sexual dimorphism, however, indicate high levels of dimorphism in gene expression, caused by chromosomal rather than hormonal differences. Here, we discuss how such dimorphism would interact with and link previously hypothesized mechanisms for sex-ratio adjustment. These differences between males and females are sufficient for offspring sex both to be detectable to parents and to provide selectable cues for biasing sex ratios from the earliest stages. We suggest ways in which future research could use the advances in our understanding of sexually dimorphic developmental physiology to test the evolutionary significance of sex allocation in mammals. Such an approach would advance our understanding of sex allocation and could be applied to other taxa.

The colour of paternity: extra-pair paternity in the wild Gouldian finch does not appear to be driven by genetic incompatibility between morphs.

In socially monogamous species, individuals can use extra-pair paternity and offspring sex allocation as adaptive strategies to ameliorate costs of genetic incompatibility with their partner. Previous studies on domesticated Gouldian finches (Erythrura gouldiae) demonstrated a genetic incompatibility between head colour morphs, the effects of which are more severe in female offspring. Domesticated females use differential sex allocation, and extra-pair paternity with males of compatible head colour, to reduce fitness costs associated with incompatibility in mixed-morph pairings. However, laboratory studies are an oversimplification of the complex ecological factors experienced in the wild and may only reflect the biology of a domesticated species. This study aimed to examine the patterns of parentage and sex ratio bias with respect to colour pairing combinations in a wild population of the Gouldian finch. We utilized a novel PCR assay that allowed us to genotype the morph of offspring before the morph phenotype develops and to explore bias in morph paternity and selection at the nest. Contrary to previous findings in the laboratory, we found no effect of pairing combinations on patterns of extra-pair paternity, offspring sex ratio or selection on morphs in nestlings. In the wild, the effect of morph incompatibility is likely much smaller, or absent, than was observed in the domesticated birds. Furthermore, the previously studied domesticated population is genetically differentiated from the wild population, consistent with the effects of domestication. It is possible that the domestication process fostered the emergence (or enhancement) of incompatibility between colour morphs previously demonstrated in the laboratory.

Maternal corticosterone exposure has transgenerational effects on grand-offspring.

The hormone fluctuations that an animal experiences during ovulation can have lifelong effects on developing offspring. These hormones may act as an adaptive mechanism, allowing offspring to be 'pre-programmed' to survive in an unstable environment. Here, we used a transgenerational approach to examine the effects of elevated maternal corticosterone (CORT) on the future reproductive success of female offspring. We show that female zebra finches (Taeniopygia guttata) exposed to embryonic CORT produce daughters that have equal reproductive success (clutch sizes, fertility, hatching success) compared with the daughters produced from untreated mothers, but their offspring had accelerated post-hatching growth rates and were significantly heavier by nutritional independence. Although there was no significant effect on primary offspring sex ratio, females from CORT-treated mothers produced significantly female-biased clutches by nutritional independence. To the best of our knowledge, this is the first record of a transgenerational sex ratio bias in response to elevated maternal CORT in any avian species.

Sex ratio evolution when fitness and dispersal vary

In a heterogeneous environment, when the fitness of males and females are differently influenced by habitat quality, habitat-dependent sex ratios may evolve to favor the production of the sex that benefits more (or loses less) from the local habitat. Similarly, sex-biased dispersal favors the evolution of habitat-dependent sex ratios. The present study documents the convergence stable sex ratios expected in the presence of sex-specific fitness gains when dispersal is partial, sex-biased or costly, using a simple model with patches of two qualities. Results show that partial dispersal reduces the sex ratio bias expected with sex-specific fitness gains. The direction of the sex ratio bias can be reversed by sex-biased dispersal or the existence of sex-specific dispersal costs, provided that fitness gains for the two sexes are not too different. The reversal of the sex ratio bias is more readily observed when sex-specific dispersal rates are opposite and extreme. Both dispersal and fitness gains, especially when they are sex-specific, should thus be considered when making predictions about sex ratio evolution in a heterogeneous environment.

Genetic markers provide insight on origins of immature green turtles Chelonia mydas with biased sex ratios at foraging grounds in Sabah, Malaysia

An understanding of population dynamics is needed to assess the viability of migra- tory species. Monitoring of marine turtles at foraging grounds may detect changes in population trends that would take decades to be seen at nesting beaches. Mixed Stock Analysis using molec- ular markers provides a tool for estimating the origin of turtles sampled at foraging grounds. Here, we analysed mitochondrial DNA sequences of 90 immature green turtles at 2 foraging grounds in northwestern Sabah, Malaysia. We used data from 30 Indo-Pacific green turtle rookeries as the baseline for tracing the origin of turtles at the 2 foraging grounds. The inferred origins of turtles at the 2 locations were not different and indicated that the majority originated from 3 major popula- tions in Southeast Asia, the Turtle Islands of Sarawak in northwestern Borneo (29%), the Turtle Islands Heritage Protected Area (TIHPA) (28%) and Peninsular Malaysia (25%). Previous analy- ses indicated a 1:4 female-biased sex ratio at the foraging grounds, and based on our results, this largely reflects the use of unshaded beach hatcheries at some of the source rookeries for decades, which resulted in mostly female hatchlings. This result is supported by differences in the origins of male and female turtles. The result suggests a greater proportion of males originating from Peninsular Malaysia and fewer males originating from Sarawak and possibly the TIHPA com- pared to females. We discuss the implications of hatchery practices that influence sex ratios of hatchlings and recommend future research to improve the management of marine turtles in the region.

Recognition and management of ecological refugees: A case study of the Cape mountain zebra

Anthropogenic activities have led to long-term range contraction in many species, creating isolated populations in ecologically marginal and suboptimal habitats. ‘Refugee’ species have a current distribution completely restricted to suboptimal habitat. However, it is likely that many species are partial refugees, where one or more populations are managed in ecologically unsuitable habitat. Here, we develop a framework to assess potential refugee populations in marginal habitats using a model species: the Cape mountain zebra. We assessed habitat quality by the abundance and palatability of grass and diet quality using proximate nutrient and element analysis. High grass abundance was associated with higher population growth rates and zebra density and less skewed adult sex ratios. Furthermore, faecal nutrient and dietary element quality was also positively associated with grass abundance. Our results show that poorly performing populations were characterised by suboptimal habitat, supporting the hypothesis that the Cape mountain zebra has refugee populations. In addition, we found more variance in sex ratio and population growth rates in smaller populations suggesting they may be more at risk for random stochastic effects, such as a biased sex ratio, compounding poor performance. We show how the ‘refugee’ concept can be applied more generally when managing species with fragmented populations occurring across marginal habitats. More broadly, the results presented herein highlight the importance of recognizing the range of habitats historically occupied by a species when assessing ecological suitability. Identifying and mitigating against refugee, relict and gap populations is especially critical in the face of on-going environmental change.

Social behavior and cooperative breeding in a precocial species: The Kalij Pheasant (Lophura leucomelanos) in Hawaii

We examined social behavior and documented cooperative breeding in Kalij Pheasants (Lophura leucomelanos) in an introduced population in Hawaii, only the third reported instance of cooperative breeding in Phasianidae. Birds in 31 distinct social groups occupied overlapping home ranges, and group composition remained relatively constant over the 3-yr study period. Each social group contained 1 breeding female and 1 to 6 males. One male was socially dominant in each multiple-male group. Age was the only factor found to determine within-group dominance, suggesting that subordinate males may gain dominance and breeding status by staying in the group. All adults exhibited cooperative behavior, including caring for chicks, agonistic behaviors against conspecific intruders, and vigilance against predators. Average population density was high (3.21 residents per ha), which may lead to habitat saturation in this population. The adult sex ratio was male-biased, with an average M:F ratio of 2.1:1.0. Genetic sex identification of egg samples revealed unbiased primary and secondary sex ratios, which suggests that the bias in adult sex ratio may be caused by differential survival and/or dispersal. Paternity analysis of 13 broods revealed that ~68% of offspring were fathered by the dominant male of the social group, while ~17% were fathered by subordinate males in the group, suggesting that helpers gained some direct benefit by sharing reproduction. We suggest that cooperative breeding may be more common in precocial species than conventionally recognized.

Do mothers bias offspring sex ratios in carotenoid-rich environments?

If environmental or maternal factors favour the fitness of one sex over the other, theory predicts that mothers should produce more offspring of the sex most likely to benefit from prevailing conditions. For species where males depend on carotenoid-based colourful ornaments to secure territory or attract mates, carotenoid availability in the environment could be one such component: mothers experiencing high availability of carotenoids should produce more sons. Here, we test this hypothesis by providing carotenoids to a wild population of a sexually dimorphic passerine, the hihi (stitchbird: Notiomystis cincta). Access to carotenoids during early life influences the colour of male hihi plumage, which improves territory acquisition as adults. Therefore, carotenoid availability when young may influence male fitness. However, we found no evidence of sex ratio bias in treated or untreated groups, either before or after hatching. First-laid eggs, where carotenoid concentrations are usually highest, were also unbiased. For hihi, access to carotenoids during egg-laying does not appear to encourage mothers to alter sex ratios of offspring. Alternatively, the fitness of daughters may also benefit from increased carotenoids during development. Disentangling these alternatives requires further work.

Frequency-dependent two-sex models: a new approach to sex ratio evolution with multiple maternal conditions.

Mothers that experience different individual or environmental conditions may produce different proportions of male to female offspring. The Trivers‐Willard hypothesis, for instance, suggests that mothers with different qualities (size, health, etc.) will use different sex ratios if maternal quality differentially affects sex‐specific reproductive success. Condition‐dependent, or facultative, sex ratio strategies like these allow multiple sex ratios to coexist within a population. They also create complex population structure due to the presence of multiple maternal conditions. As a result, modeling facultative sex ratio evolution requires not only sex ratio strategies with multiple components, but also two‐sex population models with explicit stage structure. To this end, we combine nonlinear, frequency‐dependent matrix models and multidimensional adaptive dynamics to create a new framework for studying sex ratio evolution. We illustrate the applications of this framework with two case studies where the sex ratios depend one of two possible maternal conditions (age or quality). In these cases, we identify evolutionarily singular sex ratio strategies, find instances where one maternal condition produces exclusively male or female offspring, and show that sex ratio biases depend on the relative reproductive value ratios for each sex.

Compensating for a stressful start: maternal corticosterone, offspring survival, and size at fledging in the Zebra Finch, Taeniopygia guttata

All organisms are exposed to a variety of physical, environmental and psychological challenges throughout their lives. We administered repeated oral doses of the stress hormone corticosterone (CORT) to ovulating Zebra Finches (Taeniopygia guttata) in order to mimic a disruptive environment, and investigated the effect on their reproductive output as well as outcomes for their offspring. Although females treated with CORT produced larger clutches than control females, hatching success was significantly reduced in the CORT-treated group, though there was no evidence of bias in offspring sex-ratio. Both treatment and sex had an effect on the size of chicks at hatching and their growth rate. Chicks from the experimental group were smaller at hatching than control chicks but grew faster. Similarly, male chicks were smaller than female chicks at hatching but grew faster than females. However, there was no significant difference in overall condition at nutritional independence, indicating that increased growth rates resulted from compensatory growth. These results have broad evolutionary implications, as maternal CORT is capable of affecting viability of eggs and offspring phenotype, even when maternal diet and body condition remain unchanged. As such, glucocorticoids may play a role in regulating population productivity and offspring phenotype, which provides a promising area for further research into the effects of maternal stress on adult offspring in successive generations.