Operational sex ratio, sexual conflict and the intensity of sexual selection

Modern sexual selection theory indicates that reproductive costs rather than the operational sex ratio predict the intensity of sexual selection. We investigated sexual selection in the polygynandrous common lizard Lacerta vivipara . This species shows male aggression, causing high mating costs for females when adult sex ratios (ASR) are male-biased. We manipulated ASR in 12 experimental populations and quantified the intensity of sexual selection based on the relationship between reproductive success and body size. In sharp contrast to classical sexual selection theory predictions, positive directional sexual selection on male size was stronger and positive directional selection on female size weaker in female-biased populations than in male-biased populations. Thus, consistent with modern theory, directional sexual selection on male size was weaker in populations with higher female mating costs. This suggests that the costs of breeding, but not the operational sex ratio, correctly predicted the strength of sexual selection.     

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.     

Sex-biased survival predicts adult sex ratio variation in wild birds

Adult sex ratio (ASR) is a central concept in population demography and breeding system evolution, and has implications for population viability and biodiversity conservation. ASR exhibits immense interspecific variation in wild populations, although the causes of this variation have remained elusive. Using phylogenetic analyses of 187 avian species from 59 families, we show that neither hatching sex ratios nor fledging sex ratios correlate with ASR. However, sex-biased adult mortality is a significant predictor of ASR, and this relationship is robust to 100 alternative phylogenetic hypotheses, and potential ecological and life-history confounds. A significant component of adult mortality bias is sexual selection acting on males, whereas increased reproductive output predicts higher mortality in females. These results provide the most comprehensive insights into ASR variation to date, and suggest that ASR is an outcome of selective processes operating differentially on adult males and females. Therefore, revealing the causes of ASR variation in wild populations is essential for understanding breeding systems and population dynamics.     

Demographic parameters of sexes in an elusive insect: implications for monitoring methods

Estimating demographic parameters in rare species is challenging because of the low number of individuals and their cryptic behaviour. One way to address this challenge is to gather data from several regions or years through mark-release-recapture (MRR) and radio-tracking monitoring. However, the comparison of demographic estimates obtained using these methods has rarely been investigated. Using 5 years of intensive MRR and radio-tracking surveys of an elusive and endangered saproxylic insect, the hermit beetle (Osmoderma eremita), in two regions of France, we aimed to estimate population size at the adult stage for each sex separately and to assess differences in demographic parameter estimates between survey methods. We found that males were approximately three times more likely to be recaptured than females. Taking this into account, we determined that the sex ratio was male-biased in almost all populations, except in Malus trees, where it was female-biased. Temporal fluctuations of sex ratios were also detected in one region. The radio-tracking transmitter (450 mg) allowed only the largest individuals (>2 g) to be targeted. However, we found that, among non-equipped individuals, the larger males survived better than the smaller males. We also confirmed that transmitter-equipped individuals survived approximately 25 % better than non-equipped individuals. Extrapolating the estimates from radio-tracking surveys to the population scale may result in overly optimistic population projections. Our results revealed large temporal and spatial variations in population size and sex ratios. This knowledge is crucial for predicting the persistence of small populations in fragmented landscapes. This study also questioned the representativeness of radio-tracking surveys for insect species in estimating demographic parameters at the population scale.     

Male-biased sex ratios in mature damselfly populations: real or artefact?

1. There is ongoing controversy about whether biased sex ratios in diploid insect populations are real or an artefact caused by different behaviours and/or different catchability of the sexes. This was tested by monitoring two field and three semi-natural populations of the damselfly Lestes sponsa. 2. Capture–mark–recapture data showed that population size estimates were about twice as large for males as for females at both field sites. Independent estimates of the sex ratios based on total numbers of males and females captured supported the male bias. 3. Males had higher recapture probabilities than females due to longer times between successive visits in females. Because the same pattern was found in the semi-natural populations, the longer intervals in females are no artefact due to their lower detectability. 4. Theoretical models show that the strong temporary emigration of females tends, if anything, to overestimate female population sizes and that the heterogeneity of recapture probabilities observed in males tends to underestimate male population sizes. Hence, behavioural differences between the sexes do not cause an artificially male-biased sex ratio. 5. Spatial data show that operational sex ratios are male biased at the pond but become female biased in the plots further away from the shoreline; however because of the decrease in densities away from the shoreline, this does not result in a global even sex ratio. 6. Spatial data, temporary emigration patterns, and independent estimates suggest strongly that the male-biased sex ratios in mature damselfly populations are real.     

Relative abundance of males to females affects behaviour, condition and immune function in a captive population of dark-eyed juncos Junco hyemalis

Relative numbers of males and females in breeding groups may vary from expected values owing to a variety of factors. To determine how sex ratio might influence individual phenotypes in a captive population of dark-eyed juncos Junco hyemalis during the breeding season, we established three treatment groups: a male-biased (2:1), equal (1:1), and female-biased group (1:2). Within-group density (birds/m²) was constant across groups. We assessed the frequency of flight chases (a proxy for social instability), measured changes in body mass and pectoral muscle condition, assayed plasma levels of testosterone (T) and compared cell-mediated immunity of individuals. We found significantly more chases in the male-biased group than in the female-biased group. Birds in the male-biased group lost more mass and displayed poorer pectoral-muscle condition than birds in the equal group. Cell-mediated immune responses were reduced in individuals in the male-biased group in comparison to the female-biased group. Plasma T levels in both sexes did not vary with sex ratio. Collectively, these results suggest that during the breeding season, social instability is greater in male-biased populations, and instability may lead to decreased general health and vigour.     

Mating System Variation in Woodhouse's Toad (Bufo woodhousii)

Sexual selection and mating-system variation was studied in two disjunct populations of Woodhouse's toad (Bufo woodhousii) with dissimilar breeding-period durations. In spite of the differences in breeding-period duration, nightly operational sex ratios were roughly equivalent and strongly male biased in both populations, ranging from 0 to 0.5 in the population with a prolonged breeding period, and from 0 to 0.2 in the explosively breeding form. Although operational sex ratios were similar, some males mated with up to three females in the population with an extended breeding period, whereas none of the males mated polygynously in the population with a short breeding season. Two alternative reproductive tactics, satellite and active-searching behavior, were only exhibited by males under high densities in the population with a short breeding period. In the population with an extended breeding period, male mating success was positively related to call rate, but independent of size or number of nights of participation in chorus activity. Although operational sex ratios were equally low, mating was random by size, number of nights of participation in chorus activity, and call rate for males in the explosively breeding population.     

西藏极小种群野生植物密叶红豆杉种群的性比及雌雄空间格局

雌雄异株植物种群具有性比和雌雄个体空间分布格局, 这对个体成功繁殖、种群生存潜力、天然更新能力和遗传多样性的维持都是重要的, 对于珍稀濒危雌雄异株植物种群尤其如此。密叶红豆杉(Taxus fuana)为国家I级重点保护植物, 是首批列入《全国极小种群野生植物拯救保护工程规划》的120种极小种群野生植物之一, 具有重要的生态和经济价值。但目前关于密叶红豆杉种群生态学方面的研究, 尤其是性比结构与空间分布格局在国内外鲜有报道。本文对西藏吉隆地区的6个天然密叶红豆杉种群(吉普、多甫、朗久、吉隆、开热和唐蕃)进行了实地调查, 研究其性比结构及其空间分布格局。结果表明, 调查的6个种群中总计雄株1,651株, 雌株1,231株, 仅吉普(雄/雌 = 1.89)与吉隆(雄/雌 = 1.39)两个种群有显著的性别偏倚现象且显著偏雄性(P < 0.001)。6个种群雌雄植株间的空间相关性不强, 整体趋于相互独立。不同径级间, 吉隆和开热种群的性比格局相似, 均在小径级上性比显著偏雄性, 而吉普种群则在中等径级上显著偏雄性。综上, 不同密叶红豆杉种群的大小、性比、雌雄个体的大小级结构以及空间分布格局等均表现出不同。因此, 需要结合各个种群本身的发展动态、受干扰的类型以及各区域环境因子的差异进行有针对性的保护。     

Effective size of fluctuating populations with two sexes and overlapping generations

We derive formulas that can be applied to estimate the effective population size N(e) for organisms with two sexes reproducing once a year and having constant adult mean vital rates independent of age. Temporal fluctuations in population size are generated by demographic and environmental stochasticity. For populations with even sex ratio at birth, no deterministic population growth and identical mean vital rates for both sexes, the key parameter determining N(e) is simply the mean value of the demographic variance for males and females considered separately. In this case Crow and Kimura's generalization of Wright's formula for N(e) with two sexes, in terms of the effective population sizes for each sex, is applicable even for fluctuating populations with different stochasticity in vital rates for males and females. If the mean vital rates are different for the sexes then a simple linear combination of the demographic variances determines N(e), further extending Wright's formula. For long-lived species an expression is derived for N(e) involving the generation times for both sexes. In the general case with nonzero population growth and uneven sex ratio of newborns, we use the model to investigate numerically the effects of different population parameters on N(e). We also estimate the ratio of effective to actual population size in six populations of house sparrows on islands off the coast of northern Norway. This ratio showed large interisland variation because of demographic differences among the populations. Finally, we calculate how N(e) in a growing house sparrow population will change over time.     

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.     

A predictive relationship between population and genetic sex ratios in clonal species

Sexual reproduction depends on mate availability that is reflected by local sex ratios. In species where both sexes can clonally expand, the population sex ratio describes the proportion of males, including clonally derived individuals (ramets) in addition to sexually produced individuals (genets). In contrast to population sex ratio that accounts for the overall abundance of the sexes, the genetic sex ratio reflects the relative abundance of genetically unique mates, which is critical in predicting effective population size but is difficult to estimate in the field. While an intuitive positive relationship between population (ramet) sex ratio and genetic (genet) sex ratio is expected, an explicit relationship is unknown. In this study, we determined a mathematical expression in the form of a hyperbola that encompasses a linear to a nonlinear positive relationship between ramet and genet sex ratios. As expected when both sexes clonally have equal number of ramets per genet both sex ratios are identical, and thus ramet sex ratio becomes a linear function of genet sex ratio. Conversely, if sex differences in ramet number occur, this mathematical relationship becomes nonlinear and a discrepancy between the sex ratios amplifies from extreme sex ratios values towards intermediate values. We evaluated our predictions with empirical data that simultaneously quantified ramet and genet sex ratios in populations of several species. We found that the data support the predicted positive nonlinear relationship, indicating sex differences in ramet number across populations. However, some data may also fit the null model, which suggests that sex differences in ramet number were not extensive, or the number of populations was too small to capture the curvature of the nonlinear relationship. Data with lack of fit suggest the presence of factors capable of weakening the positive relationship between the sex ratios. Advantages of this model include predicting genet sex ratio using population sex ratios given known sex differences in ramet number, and detecting sex differences in ramet number among populations.     

Adult sex ratio variation: implications for breeding system evolution

Adult sex ratio (ASR) exhibits immense variation in nature, although neither the causes nor the implications of this variation are fully understood. According to theory, the ASR is expected to influence sex roles and breeding systems, as the rarer sex in the population has more potential partners to mate with than the more common sex. Changes in mate choice, mating systems and parental care suggest that the ASR does influence breeding behaviour, although there is a need for more tests, especially experimental ones. In the context of breeding system evolution, the focus is currently on operational sex ratios (OSRs). We argue that the ASR plays a role of similar importance and urge researchers to study the ASR and the OSR side by side. Finally, we plead for a dynamic view of breeding system evolution with feedbacks between mating, parenting, OSR and ASR on both ecological and evolutionary time scales.     

Demography of the Heike firefly Luciola lateralis (Coleoptera: Lampyridae), a representative species of Japan’s traditional agricultural landscape

Populations of the Heike firefly, Luciola lateralis, a representative species of Japan’s traditional agricultural landscape (known as satoyama), have recently experienced rapid declines in many areas of Japan. Owing to the popularity of this firefly, many local communities have increased conservation efforts through the restoration of aquatic habitat complexes in satoyama. To provide fundamental parameters to predict population dynamics of the firefly, we conducted a mark–recapture study in restored paddy fields, and we estimated adult population parameters such as population size, survival, recruitment, sex ratio, and body size. We found that capture probability generally decreased as the season advanced, probably because of seasonal changes in detectability and/or firefly behavior. The daily survival rate of adults decreased over the season and may be related to a seasonal decline in adult body size. Adult population exhibited a highly male-biased sex ratio. Firefly abundance in the restored paddy fields doubled during the 4-year study period. Our analysis showed that adult detectability, recruitment, and survival rate are seasonally variable and could affect population size estimates obtained by a simple flash census. The mark–recapture technique can provide precise estimates of adult L. lateralis population characteristics and, thus, is a valuable method for predicting firefly populations and assessing the success of the restoration program.     

Sexual selection accounts for the geographic reversal of sexual size dimorphism in the dung fly, sepsis punctum (Diptera: Sepsidae)

Sexual size dimorphism (SSD) varies widely across and within species. The differential equilibrium model of SSD explains dimorphism as the evolutionary outcome of consistent differences in natural and sexual selection between the sexes. Here, we comprehensively examine a unique cross-continental reversal in SSD in the dung fly, Sepsis punctum. Using common garden laboratory experiments, we establish that SSD is male-biased in Europe and female-biased in North America. When estimating sexual (pairing success) and fecundity selection (clutch size of female partner) on males under three operational sex ratios (OSRs), we find that the intensity of sexual selection is significantly stronger in European versus North American populations, increasing with male body size and OSR in the former only. Fecundity selection on female body size also increases strongly with egg number and weakly with egg volume, however, equally on both continents. Finally, viability selection on body size in terms of intrinsic (physiological) adult life span in the laboratory is overall nil and does not vary significantly across all seven populations. Although it is impossible to prove causality, our results confirm the differential equilibrium model of SSD in that differences in sexual selection intensity account for the reversal in SSD in European versus North American populations, presumably mediating the ongoing speciation process in S. punctum.     

Climate fluctuations interact with local demography and resources to predict spatially dynamic adult sex ratios in a megaherbivore

Adult sex ratio (ASR) is a fundamental concept in population and evolutionary biology, with implications for management and conservation. Although ASR is typically measured at the population‐level, local mate competition points toward spatial variation in ASR within populations, the causes of which remain unclear. Over five breeding seasons (2008–2012), we tracked the life histories and movements of all male and female feral horses known to be alive (n = 721) on Sable Island, Canada, to investigate determinants of spatially explicit ASRs. We show that local demographic traits (density, adult female abundance, and abundance of unpaired males (e.g. floaters, adult bachelors)) operate together with inter‐annual changes in weather to determine asymmetrical ASRs across time and space that deviate from the population‐level mean. While accounting for possible confounding effects of unpaired male movements and weather, we also show that local demographics are best explained by different responses to an environmental gradient (distance to surface water). Our results demonstrate that local demographic traits operate as mechanisms by which environmental gradients and weather can shape spatial variation in ASR within wild populations, which has important implications for predicting how opportunities for sexual selection may follow from changes in resource availability and climate.     

Conservation implications of a long-term decline in body condition of the Brothers Island tuatara (Sphenodon guntheri)

Understanding the factors that drive the dynamics of remnant populations of long-lived species presents a unique challenge for conservation management. The long-lived Brothers Island tuatara Sphenodon guntheri is represented by one natural, self-sustaining population on 4-ha North Brother Island, New Zealand, and two small, translocated populations. The North Brother Island population was almost driven to extinction by extreme habitat modification and collecting in the late 19th century. Analysis of a long-term (1957–2001) dataset, following the population's recovery, reveals a significant decline in tuatara body condition over time, which is more pronounced in females. Declining body condition, coupled with very low reproductive output, may be symptomatic of a density-dependent response to elevated population size exacerbated by resource limitation. Sex-specific effects that disadvantage females could compromise this small population, particularly as it exhibits a male-biased sex ratio. We recommend removal of infrequently used structures and habitat restoration to alleviate intense resource competition. Population-level manipulation should be considered if future monitoring indicates an increasingly male-biased sex ratio and continued decline of female body condition.     

Lack of Sex-Biased Maternal Investment in spite of a Skewed Birth Sex Ratio in White-Headed Langurs (Trachypithecus leucocephalus)

Numerous hypotheses have been developed to explain sex allocation. In male-dispersing, female cooperatively breeding species, the local resource competition model predicts male-biased birth sex ratio, the local resource enhancement model predicts female-biased birth sex ratio, and the population adjustment model predicts that biased birth sex ratio should not be favored if the two sexes are equally costly to rear. The male quality model predicts that, in polygynous species, females in better physical condition will either produce more sons than daughters or invest more heavily in sons than in daughters. White-headed langurs are a female philopatry and female cooperatively breeding species. During a 11-yr study, a total of 133 births were recorded, among which birth sex ratio (M:F = 73:49) was significantly male-biased. This is consistent with the prediction of the local resource competition model. On the other hand, if mothers balanced their investment between the two sexes, according to Fisher's population adjustment model, males should be the less-costly-to-rear sex. However, we found no sex difference for infant mortality (12.3% in males and 12.2% in females), and sons induced slightly longer interbirth interval (son: 26.4 ± 1.1 mo, daughter: 24.1 ± 0.6 mo) and lactational period (son: 20.9 ± 1.0 mo, daughters: 19.6 ± 0.5 mo) for their mothers. Thus, the population adjustment model was not supported by this study. The local resource enhancement model was not supported because birth sex ratio did not bias to females who provided more reproductive assistance. On the individual level, probit regression showed no relation between birth sex ratio and group size. Because the group size was considered to be negatively related to female physical condition, our study did not support the male-quality model. We suggested several possibilities to explain these results.     

雌雄异熟植物露蕊乌头开花时间对雌雄功能期及表型性别的影响

开花时间决定了植物雌雄功能的交配机会, 最终影响繁殖成功。交配环境假说认为雌雄异熟植物开花时间的差异能引起植物表型性别的变异, 改变种群内的交配环境, 影响植物对雌雄功能的最佳性分配。为了研究开花时间对雌雄异熟植物的雌雄性别时期及表型性别的影响, 本文以毛茛科雄性先熟植物露蕊乌头(Aconitum gymnandrum)为实验材料, 记录了雄性和雌性功能期, 分析了植株开花时间、花的雌雄功能期和表型性别的关系。结果表明: 在植物同一花序内, 较晚开放的花有更长的雄性期和更短的雌性期, 性分配在时间上偏雄。雌雄功能期在时间上的相对分配随植物开花时间的变化表现出相似的趋势： 较晚开的花或较晚开花的个体, 花的雄性功能期相对于雌性功能期更长, 在时间上更偏向雄性功能。而且, 开花时间的差异影响种群内花的性比和植物个体的表型性别动态。随着开花时间由早到晚的变化, 种群内早期以雄花为主,末期以雌花为主, 种群内性别环境由偏雄向偏雌变化, 因此植株个体的平均表型性别则从偏雌转向偏雄。本文结果支持交配环境假说, 雄性先熟的露蕊乌头开花早期, 种群内花的性别比偏雄, 种群表型性别环境偏雄, 因而植物个体平均表型性别偏雌, 性别分配(即时间分配)偏向雌性功能, 而晚开花个体的平均性别偏雄, 更偏向雄性功能的分配。     

Demographic origins of skewed operational and adult sex ratios: perturbation analyses of two-sex models

Skewed sex ratios – operational (OSR) and Adult (ASR) - arise from sexual differences in reproductive behaviours and adult survival rates due to the cost of reproduction. However, skewed sex-ratio at birth, sex-biased dispersal and immigration, and sexual differences in juvenile mortality may also contribute. We present a framework to decompose the roles of demographic traits on sex ratios using perturbation analyses of two-sex matrix population models. Metrics of sensitivity are derived from analyses of sensitivity, elasticity, life-table response experiments and life stage simulation analyses, and applied to the stable stage distribution instead of lambda. We use these approaches to examine causes of male-biased sex ratios in two populations of green-rumped parrotlets ( Forpus passerinus ) in Venezuela. Female local juvenile survival contributed the most to the unbalanced OSR and ASR due to a female-biased dispersal rate, suggesting sexual differences in philopatry can influence sex ratios more strongly than the cost of reproduction.     

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.