Facultative adjustment of the offspring sex ratio and male attractiveness: a systematic review and meta‐analysis

Females can benefit from mate choice for male traits (e.g. sexual ornaments or body condition) that reliably signal the effect that mating will have on mean offspring fitness. These male‐derived benefits can be due to material and/or genetic effects. The latter include an increase in the attractiveness, hence likely mating success, of sons. Females can potentially enhance any sex‐biased benefits of mating with certain males by adjusting the offspring sex ratio depending on their mate's phenotype. One hypothesis is that females should produce mainly sons when mating with more attractive or higher quality males. Here we perform a meta‐analysis of the empirical literature that has accumulated to test this hypothesis. The mean effect size was small (r = 0.064–0.095; i.e. explaining <1% of variation in offspring sex ratios) but statistically significant in the predicted direction. It was, however, not robust to correction for an apparent publication bias towards significantly positive results. We also examined the strength of the relationship using different indices of male attractiveness/quality that have been invoked by researchers (ornaments, behavioural displays, female preference scores, body condition, male age, body size, and whether a male is a within‐pair or extra‐pair mate). Only ornamentation and body size significantly predicted the proportion of sons produced. We obtained similar results regardless of whether we ran a standard random‐effects meta‐analysis, or a multi‐level, Bayesian model that included a correction for phylogenetic non‐independence. A moderate proportion of the variance in effect sizes (51.6–56.2%) was due to variation that was not attributable to sampling error (i.e. sample size). Much of this non‐sampling error variance was not attributable to phylogenetic effects or high repeatability of effect sizes among species. It was approximately equally attributable to differences (occurring for unknown reasons) in effect sizes among and within studies (25.3, 22.9% of the total variance). There were no significant effects of year of publication or two aspects of study design (experimental/observational or field/laboratory) on reported effect sizes. We discuss various practical reasons and theoretical arguments as to why small effect sizes should be expected, and why there might be relatively high variation among studies. Currently, there are no species where replicated, experimental studies show that mothers adjust the offspring sex ratio in response to a generally preferred male phenotype. Ultimately, we need more experimental studies that test directly whether females produce more sons when mated to relatively more attractive males, and that provide the requisite evidence that their sons have higher mean fitness than their daughters.     

Quantity matters: male sex pheromone signals mate quality in the parasitic wasp Nasonia vitripennis

Sexual selection theory asserts that females are well adapted to sense signals indicating the quality of potential mates. One crucial male quality parameter is functional fertility (i.e. the success of ejaculates in fertilizing eggs). The phenotype-linked fertility hypothesis (PLFH) predicts that functional fertility of males is reflected by phenotypic traits that influence female mate choice. Here, we show for Nasonia vitripennis, a parasitic wasp with haplodiploid sex determination and female-biased sex ratios, that females use olfactory cues to discriminate against sperm-limited males. We found sperm limitation in newly emerged and multiply mated males (seven or more previous matings) as indicated by a higher proportion of sons in the offspring fathered by these males. Sperm limitation correlated with clearly reduced pheromone titres. In behavioural bioassays, females oriented towards higher doses of the synthetic pheromone and were attracted more often to scent marks of males with a full sperm load than to those of sperm-limited males. Our data support the PLFH and suggest that N. vitripennis females are able to decrease the risk of getting constrained to produce suboptimal offspring sex ratios by orienting towards gradients of the male sex pheromone.     

圆盘菌科无性型有性生殖能力评估

本文评估了分离自子囊孢子和分生孢子的圆盘菌科无性型有性生殖能力。结果表明,由子囊孢子和分生孢子萌发获得的菌株的有性生殖能力具有显著差异,这可能决定于不同的遗传特性。该试验支持了一种假说：仅能进行无性生殖的无性型菌株,很可能来源于逐渐丧失了有性生殖能力的全型菌株。     

Unifying cornerstones of sexual selection: operational sex ratio,Bateman gradient and the scope for competitive investment

What explains variation in the strength of sexual selection across species, populations or differences between the sexes? Here, we show that unifying two well‐known lines of thinking provides the necessary conceptual framework to account for variation in sexual selection. The Bateman gradient and the operational sex ratio (OSR) are incomplete in complementary ways: the former describes the fitness gain per mating and the latter the potential difficulty of achieving it. We combine this insight with an analysis of the scope for sexually selected traits to spread despite naturally selected costs. We explain why the OSR sometimes does not affect the strength of sexual selection. An explanation of sexual selection becomes more logical when a long ‘dry time’ (‘time out’, recovery after mating due to e.g. parental care) is understood to reduce the expected time to the next mating when in the mating pool (i.e. available to mate again). This implies weaker selection to shorten the wait. An integrative view of sexual selection combines an understanding of the origin of OSR biases with how they are reflected in the Bateman gradient, and how this can produce selection for mate acquisition traits despite naturally selected costs.     

Sex roles and sex ratios in animals

In species with separate sexes, females and males often differ in their morphology, physiology and behaviour. Such sex-specific traits are functionally linked to variation in reproductive competition, mate choice and parental care, which have all been linked to sex roles. At the 150th anniversary of Darwin's theory on sexual selection, the question of why patterns of sex roles vary within and across species remains a key topic in behavioural and evolutionary ecology. New theoretical, experimental and comparative evidence suggests that variation in the adult sex ratio (ASR) is a key driver of variation in sex roles. Here, we first define and discuss the historical emergence of the sex role concept, including recent criticisms and rebuttals. Second, we review the various sex ratios with a focus on ASR, and explore its theoretical links to sex roles. Third, we explore the causes, and especially the consequences, of biased ASRs, focusing on the results of correlational and experimental studies of the effect of ASR variation on mate choice, sexual conflict, parental care and mating systems, social behaviour, hormone physiology and fitness. We present evidence that animals in diverse societies are sensitive to variation in local ASR, even on short timescales, and propose explanations for conflicting results. We conclude with an overview of open questions in this field integrating demography, life history and behaviour.     

Sex is not a solution for reproduction: the libertine bubble theory

Here, I propose a new hypothesis: sex originated from an archaic gene transfer process among prebiotic bubbles without the prerequisite for reproduction. This de‐coupling from reproduction might make the thorny problem of accounting for the evolution of sex, despite the apparent advantages of parthenogenicity, more tractable.     

Intralocus sexual conflict and offspring sex ratio

Males and females frequently have different fitness optima for shared traits, and as a result, genotypes that are high fitness as males are low fitness as females, and vice versa. When this occurs, biasing of offspring sex-ratio to reduce the production of the lower-fitness sex would be advantageous, so that for example, broods produced by high-fitness females should contain fewer sons. We tested for offspring sex-ratio biasing consistent with these predictions in broad-horned flour beetles. We found that in both wild-type beetles and populations subject to artificial selection for high- and low-fitness males, offspring sex ratios were biased in the predicted direction: low-fitness females produced an excess of sons, whereas high-fitness females produced an excess of daughters. Thus, these beetles are able to adaptively bias sex ratio and recoup indirect fitness benefits of mate choice.     

Within-clutch variation in offspring sex determined by differences in sire body size: cryptic mate choice in the wild

Sexual selection theory predicts that paternal quality should drive female investment in progeny. We tested whether polyandrous female side-blotched lizards, Uta stansburiana, would adjust within-clutch progeny investment according to sire phenotypes. In two different years, polyandrous females selectively used sperm from larger sires to produce sons and used sperm from smaller sires to produce daughters. This cryptic sperm choice had significant effects on progeny survival to maturity that were consistent with sexually antagonistic effects associated with sire body size. Large sires produced sons with high viability and small sires produced daughters with high viability. These results are consistent with our previous findings that alleles for male body size have different fitness effects in male and female progeny. Breeding experiments in the laboratory indicate that results from the wild are more likely due to female choice than biased sperm production by males. Our results demonstrate highly refined gender-specific female choice for sperm and indicate that sire body size may signal the quality of sons or daughters that a sire will produce.     

Anisogamy,sexual selection,and the evolution and maintenance of sex

Summary In the present paper we distinguish between two aspects of sexual reproduction. Genetic recombination is a universal features of the sexual process. It is a primitive condition found in simple, single-celled organisms, as well as in higher plants and animals. Its function is primarily to repair genetic damage and eliminate deleterious mutations. Recombination also produces new variation, however, and this can provide the basis for adaptive evolutionary change in spatially and temporally variable environments.The other feature usually associated with sexual reproduction, differentiated male and female roles, is a derived condition, largely restricted to complex, diploid, multicellular organisms. The evolution of anisogamous gametes (small, mobile male gametes containing only genetic material, and large, relatively immobile female gametes containing both genetic material and resources for the developing offspring) not only established the fundamental basis for maleness and femaleness, it also led to an asymmetry between the sexes in the allocation of resources to mating and offspring. Whereas females allocate their resources primarily to offspring, the existence of many male gametes for each female one results in sexual selection on males to allocate their resources to traits that enhance success in competition for fertilizations. A consequence of this reproductive competition, higher variance in male than female reproductive success, results in more intense selection on males.The greater response of males to both stabilizing and directional selection constitutes an evolutionary advantage of males that partially compensates for the cost of producing them. The increased fitness contributed by sexual selection on males will complement the advantages of genetic recombination for DNA repair and elimination of deleterious mutations in any outcrossing breeding system in which males contribute only genetic material to their offspring. Higher plants and animals tend to maintain sexual reproduction in part because of the enhanced fitness of offspring resulting from sexual selection at the level of individual organisms, and in part because of the superiority of sexual populations in competition with asexual clones.     

On the logic of Fisherian sexual selection*

In Fisher's model of sexual selection, a female preference for a male trait spreads together with the trait because their genetic bases become correlated. This can be interpreted as a “greenbeard” system: a preference gene, by inducing a female to mate with a trait-bearing male, favors itself because the male is disproportionately likely also to carry the preference gene. Here, we use this logic to argue that Fisherian sexual selection in diploids proceeds via two channels: (i) trait-bearing males are disproportionately the product of matings between preference-bearing mothers and trait-bearing fathers, and thus trait and preference genes are correlated “in trans”; (ii) trait and preference genes come into gametic phase disequilibrium, and thus are correlated “in cis.” Gametic phase disequilibrium is generated by three distinct mechanisms that we identify. The trans channel does not operate when sexual selection is restricted to the haploid phase, and therefore represents a fundamental difference between haploid and diploid models of sexual selection. We show that the cis and trans channels contribute equally to the spread of the preference when recombination between the preference and trait loci is free, but that the trans channel is substantially more important when linkage is tight.     

The evolution of obligate sex: the roles of sexual selection and recombination

The evolution of sex is one of the greatest mysteries in evolutionary biology. An even greater mystery is the evolution of obligate sex, particularly when competing with facultative sex and not with complete asexuality. Here, we develop a stochastic simulation of an obligate allele invading a facultative population, where males are subject to sexual selection. We identify a range of parameters where sexual selection can contribute to the evolution of obligate sex: Especially when the cost of sex is low, mutation rate is high, and the facultative individuals do not reproduce sexually very often. The advantage of obligate sex becomes larger in the absence of recombination. Surprisingly, obligate sex can take over even when the population has a lower mean fitness as a result. We show that this is due to the high success of obligate males that can compensate the cost of sex.     

The mismeasurement of sexual selection

Sexual selection can explain major micro‐ and macro‐evolutionary patterns. Much of current theory predicts that the strength of sexual selection (i) is driven by the relative abundance of males and females prepared to mate (i.e. the operational sex ratio, OSR) and (ii) can be generally estimated by calculating intra‐sexual variation in mating success (e.g. the opportunity for sexual selection, I_s). Here, we demonstrate the problematic nature of these predictions. The OSR and I_s only accurately predict sexual selection under a limited set of circumstances, and more specifically, only when mate monopolization is extremely strong. If mate monopolization is not strong, using OSR or I_s as proxies or measures of sexual selection is expected to produce spurious results that lead to the false conclusion that sexual selection is strong when it is actually weak. These findings call into question the validity of empirical conclusions based on these measures of sexual selection.     

Operational sex ratio influences the opportunity for sexual selection in guppies

The opportunity for sexual selection was greater when the operational sex ratio (OSR) in guppies Poecilia reticulata was biased towards males. This could be due to an increase in both male-male competition and female mate choice under male-biased OSR.     

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.     

Mate sampling and the sexual conflict over mating in seaweed flies

The order in which females encounter, or sample, males in apopulation may have important consequences for mate choice,with the information gathered about males influencing boththe preference function and degree of choosiness of females.Sexual selection may be affected as a result. Sampling of particularsubsets of males may be a crucial component of individual variation in mate preferences within populations. However, the sequencein which males are sampled may also be important in specieswithout traditional, active mate choice, such as when sexualselection involves sexual conflict over mating. This wouldoccur if the likelihood of a female mating with a male of acertain phenotype changes as a result of previous encounters.We examined the effects of encountering males differing inbody size, a sexually selected phenotype, in the seaweed flyCoelopa frigida. Sexual selection occurs in this species asa result of a sexual conflict over mating. We show that theoutcome of the sexual conflict is independent of the orderin which males are encountered by female seaweed flies, withthe overall mating advantage to large males being unaffected.In addition, we explored female preference functions and evaluatethe heterogeneity in female willingness to mate. We suggestthat consideration of mate sampling theory is valuable whenexamining mate choice in species in which sexual selectionis driven by sexual conflict.     

Sexual selection for bright females prevails under light pollution

The functions of sexually selected traits are particularly sensitive to changes in the environment because the traits have evolved to in-crease mating success u...     

Male choice generates stabilizing sexual selection on a female fecundity correlate

We know very little about male mating preferences and how they influence the evolution of female traits. Theory predicts that males may benefit from choosing females on the basis of traits that indicate their fecundity. Here, we explore sexual selection generated by male choice on two components of female body size (wing length and body mass) in Drosophila serrata. Using a dietary manipulation to alter female size and 828 male mate choice trials, we analysed linear and nonlinear sexual selection gradients on female mass and wing length. In contrast to theoretical expectations and prevailing empirical data, males exerted stabilizing rather than directional sexual selection on female body mass, a correlate of fecundity. Sexual selection was detected only among females with access to standard resource levels as an adult, with no evidence for sexual selection among resource-depleted females. Thus the mating success of females with the same body mass differed depending upon their access to resources as an adult. This suggests that males in this species may rely on signal traits to assess body mass rather than assessing it directly. Stabilizing rather than directional sexual selection on body mass together with recent evidence for stabilizing sexual selection on candidate signal traits in this species suggests that females may trade-off resources allocated to reproduction and sexual signalling.     

Cycle of gonadal development in Eunicella singularis (Cnidaria: Octocorallia): trends in sexual reproduction in gorgonians

Abstract. Eunicella singularis is a gorgonian species whose members are abundant in hard-bottom sublittoral communities of the Mediterranean Sea. The reproductive biology in this species has been examined to better understand the ability in this species to recover from recent mass mortality events. Eunicella singularis is a stable, gonochoric, iteroparous species that reproduces annually and exhibits a seasonal pattern of gametogenesis characterized by a single annual maturation of the gametes. The sex ratio did not significantly differ from 1:1. Oogenesis lasted 13–17 months, beginning between February and June, and ending with the release of 0.7 planula larvae per polyp between late May and July of the following year. The diameter of mature oocytes ranged 450–860 μm. Spermatogenesis was much shorter than oogenesis and occurred over 5–6 months. Gonadal production of both sexes increased in spring and culminated with the spawning of male colonies in late May–June. Fertilization of oocytes and development of the planula larvae occurred within the polyps of female colonies. Planula release was observed in June and July. The patterns emerging from this and previous studies on sexual reproduction of Mediterranean gorgonians suggest that investment in gonad development appears to be related to resource availability.     

甘草有性生殖特性研究

本文利用扫描电子显微镜对乌拉尔甘草、光果甘草和胀果甘草花粉的超微结构进行观察;利用荧光显微镜确定乌拉尔甘草的授粉方式、花粉生活力和柱头活性以及授粉后受精时间。结果表明花粉超微结构为甘草的鉴别提供了一定的形态学依据;甘草的授粉方式属于闭花受精;花粉生活力在每天12:00时最强,去雄后超过四天的柱头已经不具备接受花粉的能力;对授粉后不同时间的雌蕊进行研究得出授粉后6h花粉管进入胚珠进行受精。本文主要对甘草的有性生殖特性进行了研究,为未来制定正确的选、育种策略提供理论依据。     

甘草有性生殖特性研究

本文利用扫描电子显微镜对乌拉尔甘草、光果甘草和胀果甘草花粉的超微结构进行观察;利用荧光显微镜确定乌拉尔甘草的授粉方式、花粉生活力和柱头活性以及授粉后受精时间。结果表明花粉超微结构为甘草的鉴别提供了一定的形态学依据;甘草的授粉方式属于闭花受精;花粉生活力在每天12:00时最强,去雄后超过四天的柱头已经不具备接受花粉的能力;对授粉后不同时间的雌蕊进行研究得出授粉后6h花粉管进入胚珠进行受精。本文主要对甘草的有性生殖特性进行了研究,为未来制定正确的选、育种策略提供理论依据。