Male-biased Operational Sex Ratio Research Articles

Anuran swingers: misdirected mating attempts occurred early during anuran diversification

Abstract Promiscuity, explosive breeding and male-biased operational sex-ratios can affect the strength of male selectivity and may play major roles in the expression of misdirected matings (with conspecific males, other species, corpses or objects) in anuran amphibians. Yet, misdirected amplexus occur in multiple species diverging from these reproductive traits, suggesting that the expression of such behaviour is widespread, and may have occurred early during anuran diversification. Using two methods of ancestral-trait reconstruction which predict unknown states, we found a very high probability that most anuran genera express misdirected amplexus, suggesting that this by-product of anuran reproductive strategies is likely to have occurred early during anuran diversification. The persistence of misdirected amplexus suggests that its infrequent occurrence may outweigh individual costs of breeding attempts with unfit mates. We found a recent exponential increase in reported observations of misdirected amplexus, which, along with increased research effort and publication rate, may reveal an effect of environmental perturbations known to promote the occurrence of these behaviours.

Persistence of a highly monoandrous mating system despite an extremely male-biased operational sex ratio in the firefly squid Watasenia scintillans

Persistence of a highly monoandrous mating system despite an extremely male-biased operational sex ratio in the firefly squid Watasenia scintillans

Male mating success evolves in response to increased levels of male-male competition.

Male-biased operational sex ratios can increase male-male competition and can potentially select for both increased pre- and postcopulatory male success. In the present study, using populations of Drosophila melanogaster evolved under male-biased (M) or female-biased (F) sex ratios, we asked whether (a) male mating success can evolve, (b) males are better at mating females that they have coevolved with, (c) males mating success is affected by female mating status, and (d) male mating success is correlated with their courtship effort. We directly competed M and F males for mating with (a) virgin ancestral (common) females, (b) virgin females from the M and F populations, and (c) singly mated females from the M and F populations. We also assessed the courtship frequency of the males when paired with mated M or F females. Our results show that M males, evolving under an increased level of male-male competition, have higher mating success than F males irrespective of the female evolutionary history. However, the difference in mating success is more pronounced if the females had mated before. M males also have a higher courtship frequency than F males, but we did not find any correlation between mating success and courtship frequency.

Testing the Role of Environmental Harshness and Sexual Selection in Limb Muscle Mass in Anurans

Sexual dimorphism is regarded as the consequence of differential responses by males and females to selection pressures. Limb muscle plays a very important role during amplexus, which is likely to be under both natural and sexual selection in anurans. Here, we studied the effects of natural and sexual selection on limb muscle mass in males and females across 64 species of anurans. The results showed that there were non-significant differences in relative limb muscle mass between the sexes among species, exhibiting no sexual dimorphism in limb muscle. Absolute and relative limb muscle mass positively displayed correlations with snout-vent length (SVL)for both sexes. However, neither male-biased operational sex ratio (OSR) nor environmental harshness [e.g., coefficient of variation (CV) in temperature and CV in rainfall] can explain relative limb muscle mass (e.g., forelimb, hindlimb, and total limb muscle) within each sex. The findings suggest that environmental harshness and sexual selection cannot play important roles in promoting variations in limb muscle among anuran species.

Body Size, Not Personality, Explains Both Male Mating Success and Sexual Cannibalism in a Widow Spider.

Simple SummaryThe role of personality in sexual selection has mostly been investigated on vertebrate species, in which males provide direct benefits to females or offspring. Less is known about the links between behavioral variation and sexual selection in species where males provide only sperm, while the advantages of female-choice are due to male genes that increase offspring fitness. Our study is centered on a sexually-size dimorphic spider species, the Mediterranean black widow, which is ideal to investigate how sexual selection shapes behavior. In this species, a male-biased operational sex-ratio leads to male-male competition, and aggressive and/or large males should have a selective advantage. Females are selected for fecundity, which should correlate with selection for higher voraciousness. Theory predicts that voracity “spills-over” into the mating context, such that voracity towards prey correlates with voracity towards mates. We tested how body size and two behaviors, male aggression toward rivals and female voracity toward prey, influence mating behavior, mating success, and sexual cannibalism. We show that individual variation in aggression does not play a direct role in the mating behavior of this species. Instead, body size affects male mating success and the occurrence of sexual cannibalism in females.Theory suggests that consistent individual variation in behavior relates to fitness, but few studies have empirically examined the role of personalities in mate choice, male-male competition and reproductive success. We observed the Mediterranean black widow, Latrodectus tredecimguttatus, in the individual and mating context, to test how body size measures and two functionally important aggressive behaviors, i.e., male aggression towards rivals and female voracity towards prey, affect mating behaviors, mating success and sexual cannibalism. We specifically selected voracity towards prey in females to test the “aggressive spillover hypothesis”, suggesting that more voracious females are more sexually cannibalistic. Both females and males exhibit consistent individual differences in the examined aggressive behaviors. While larger males win contests more often and achieve more copulations, neither male nor female size measures correlate to aggression. Female voracity does not correlate with aggression towards mates and sexual cannibalism, rejecting the “spillover hypothesis”. However, occurrence of sexual cannibalism positively relates to longer insertion duration. Furthermore, the smaller the ratio between male and female body length the more likely a female attacked and cannibalized a mate. We show that individual variation in aggression levels plays no direct role in the mating behavior of the Mediterranean black widow. Instead, body size affects male mating success and occurrences of sexual cannibalism in females.

The size of signal detection and emission organs in a synchronous firefly: sexual dimorphism, allometry and assortative mating.

The size of the organs responsible for emitting and detecting sexual communication signals is a likely target for selection. Communication via bioluminescent signals in synchronous fireflies is a promising model to test hypotheses regarding differences between males and females in the effect of the size of signal emission and detection organs on fitness components. Synchronous firefly species congregate in large numbers during the mating season, displaying bioluminescent signals aimed at potential mates during relatively short nightly periods. Operational sex ratios are male-biased and, thus, the so-called typical sex roles (indiscriminate males and choosy females) are expected to evolve. We studied the synchronous firefly Photinus palaciosi, a species that during the mating season congregates in forests of central Mexico offering a magnificent natural show that attracts numerous tourists. P. palaciosi females have reduced wings (brachyptery) and cannot fly. Our field study tested the hypothesis that the male-biased operational sex ratio and the short daily mating period result in strong male-male competition that selects for males with larger lanterns and larger eyes, and against male mate choice, whereas female-female mate competition is absent and, thus, no selection on lantern or eye size is expected. Even though lantern, eye or body size do not predict the probability of being found in copula for either sex, sexual dimorphism in these features, along with allometric slopes of lantern size and assortative mating in terms of relative lantern size, support not only the hypothesis of intense sexual selection among males, but the possibility of subtle mechanisms of sexual selection among females. Trade-offs between investment in signaling (lanterns) versus detection (eyes) structures, or with pressures different from sexual selection such as those imposed by predators, are also likely to be important in shaping the evolution of sexual signaling in these fireflies.

Effects of global warming on sex ratios in fishes.

In fishes, sex is determined by genetics, the environment or an interaction of both. Temperature is among the most important environmental factors that can affect sex determination. As a consequence, changes in temperature at critical developmental stages can induce biases in primary sex ratios in some species. However, early sex ratios can also be biased by sex-specific tolerances to environmental stresses that may, in some cases, be amplified by changes in water temperature. Sex-specific reactions to environmental stress have been observed at early larval stages before gonad formation starts. It is therefore necessary to distinguish between temperature effects on sex determination, generally acting through the stress axis or epigenetic mechanisms, and temperature effects on sex-specific mortality. Both are likely to affect sex ratios and hence population dynamics. Moreover, in cases where temperature effects on sex determination lead to genotype-phenotype mismatches, long-term effects on population dynamics are possible, for example temperature-induced masculinization potentially leading to the loss of Y chromosomes or feminization to male-biased operational sex ratios in future generations. To date, most studies under controlled conditions conclude that if temperature affects sex ratios, elevated temperatures mostly lead to a male bias. The few studies that have been performed on wild populations seem to confirm this general trend. Recent findings suggest that transgenerational plasticity could mitigate the effects of warming on sex ratios in some populations.

Sex ratio is variable and increasingly male biased at two colonies of Magellanic Penguins.

Sex ratios are commonly skewed and variable in wild populations, but few studies track temporal trends in this demographic parameter. We examined variation in the operational sex ratio at two protected and declining breeding colonies of Magellanic Penguins (Spheniscus magellanicus) in Chubut, Argentina. Penguins from the two colonies, separated by 105km, migrate north in the non-breeding season and have overlapping distributions at sea. Conditions during the non-breeding season can impact long-term trendsin operational sex ratio (i.e., through sex-specific survival) and interannual variation in operational sex ratio (i.e., through sex-specific breeding decisions). We found an increasingly male-biased operational sex ratio at the two disparate colonies of Magellanic Penguins, which may contribute to continued population decline. We also found that the two colonies showed synchronous interannual variation in operational sex ratio, driven by variation in the number of females present each year. This pattern may be linked to sex-specific overwintering effects that cause females to skip breeding, i.e., to remain at sea rather than returning to the colony to breed, more often than males. Contrary to our predictions, colony-wide reproductive success was not lower in years with a more male-biased operational sex ratio. We did find that males showed more evidence of fighting and were less likely to pair when the operational sex ratio was more male biased. Our results highlight an indirect mechanism through which variation in the operational sex ratio can influence populations, through a higher incidence of fighting among the less abundant sex. Because biased sex ratios can reduce the size of the breeding population and influence rates of conflict, tracking operational sex ratio is critical for conservation.

Deer Indirectly Alter the Reproductive Strategy and Operational Sex Ratio of an Unpalatable Forest Perennial.

Environmental conditions impose restrictions and costs on reproduction. Multiple reproductive options exist when increased reproductive costs drive plant populations toward alternative reproductive strategies. Using 4 years of demographic data across a deer impact gradient, where deer alter the abiotic environment, we parameterize a size-dependent integral projection model for a sexually labile and unpalatable forest perennial to investigate the demographic processes driving differentiation in the operational sex ratio (OSR) of local populations. In addition to a relative increase in asexual reproduction, our results illustrate that nontrophic indirect effects by overabundant deer on this perennial result in delayed female sex expression to unsustainably large plant sizes and lead to more pronounced plant shrinkage following female sex expression, effectively increasing the cost of reproduction. Among plants of reproductive age, increased deer impact decreases the size-dependent probability of flowering and reduces reproductive consistency over time. This pattern in sex expression skews populations toward female-biased OSRs at low deer impact sites and male-biased OSRs at intermediate and high deer impact sites. While this shift toward a male-biased OSR may ameliorate pollen limitation, it also decreases the effective population size when coupled with increased asexual reproduction. The divergence of reproductive strategies and reduced lifetime fitness in response to indirect deer impacts illustrate the persistent long-term effects of overabundant herbivores on unpalatable understory perennials.

Emergence and mating behavior of the oriental fruit moth Cydia molesta (Lepidoptera: Tortricidae) and its potential for reproduction

SummaryThe Oriental fruit moth, Cydia molesta (Busck, 1916) (Lepidoptera: Tortricidae), is a key pest of fruit and is widely distributed around the world. There are important connections between its behavior and biology and its management in agriculture, but few studies have investigated the associations between adult behaviors and oviposition. In this study, adult emergence, mating, and reproduction were investigated under laboratory and field conditions. The ratio of females to males at eclosion was approximately 1:1. When one virgin female had access to one virgin male, 66% and 34% of the couples copulated just once and twice, respectively; and the infertility rate of eggs (21.39 ± 1.25%) did not vary daily. Males, given access to one new female daily, could copulate multiple times, whereas females seldom mated more than once, indicating a male-biased operational sex ratio, but mating status of the male parent had no effect on progeny egg reproduction. Also, the number of eggs that hatched by all female partners of a male was inversely proportional to copulation duration for the female laying the eggs for total female reproductive success; and the number of eggs laid by all female partners of a male was proportional to their number of matings for total male reproductive success. However, the total number of eggs that hatched did not significantly differ for eggs laid by a female given new virgin males daily for mating (17.75 ± 4.28) versus eggs laid by virgin females (19.17 ± 7.51) presented daily with a male that re-mated daily with the series of females. Therefore, our results showed that females engaged in mate choice and males engaged in mate competition, affecting egg production, a factor that may be used to enhance mating disruption technology against Cydia molesta.

Male black widows parasitize mate-searching effort of rivals to find females faster.

Mate-searching success is a critical precursor to mating, but there is a dearth of research on traits and tactics that confer a competitive advantage in finding potential mates. Theory and available empirical evidence suggest that males locate mates using mate-attraction signals produced by receptive females (personal information) and avoid inadvertently produced cues from rival males (social information) that indicate a female has probably already mated. Here, we show that western black widow males use both kinds of information to find females efficiently, parasitizing the searching effort of rivals in a way that guarantees competition over mating after reaching a female's web. This tactic may be adaptive because female receptivity is transient, and we show that (i) mate searching is risky (88% mortality) and (ii) a strongly male-biased operational sex ratio (from 1.2 : 1 to more than 10 : 1) makes competition inevitable. Males with access to rivals' silk trails moved at higher speeds than those with only personal information, and located females even when personal information was unreliable or absent. We show that following rivals can increase the potential for sexual selection on females as well as males and argue it may be more widespread in nature than is currently realized.

Operational sex ratio and density predict the potential for sexual selection in the broad-horned beetle

Sexual selection can act on all aspects of the phenotype and the opportunity for selection (Is) sets its maximal strength. Popular approaches to alter Is include the manipulation of the operational sex ratio (OSR) and/or density, with an increase in Is predicted with a male-biased OSR and at higher density. However, debate continues regarding the utility of Is to measure meaningful changes in the strength of selection, as changes in Is with OSR and density may only reflect stochastic processes. Here we tested whether the manipulation of OSR and density alters Is in the broad-horned flour beetle, Gnatocerus cornutus, a species where males are under intense sexual selection and the targets of selection are known. We also recorded the average number of fights and mating behaviour of individuals in our competitive arenas. We found significant main effects of OSR and density on Is, with the opportunity for selection being highest in male-biased high-density treatments. There were also significant effects of OSR and density on the average number of matings, whereas only density influenced the average number of fights. These results suggest that manipulation of OSR and density influence the opportunity for sexual selection in G. cornutus and our observations of fighting and mating behaviour provide a proximate mechanism for the change in Is.

Spatial variation in sex ratio and density explains subtle changes in the strength of size-assortative mating in Edessa contermina (Hemiptera: Pentatomidae)

Size-assortative mating (SAM) is usually explained by the mate-choice hypothesis. However, this hypothesis does not consider the effects of variations in the intensity of mating competition on mate choice and SAM. For example, in populations with male-biased operational sex ratios (OSR) and high densities, large males will have more advantages during mating competition and will have access to the most mating opportunities with large, preferred females (i.e. mating competition hypothesis). In this study, we investigated the effects of mating competition and mate choice on the strength of SAM in Edessa contermina (Hemiptera: Pentatomidae). We also described sexual size dimorphism and the mating system of this Neotropical stink bug in a conservation area of the Brazilian savanna. We used density as a proxy for mating competition intensity because it was positively correlated with OSR. Size-assortative mating was more consistent under intense mating competition. However, males copulated with relatively larger females as population density increased. Males assortatively mated based on size in the first and second copulation events observed, while both female matings were random. Thus, male mate choice may promote SAM in E. contermina, but its strength is affected by variations in the intensity of mating competition. Hence, we provided empirical support for mating competition as a potential mechanism promoting subtle changes in SAM. We discussed potential implications of this mechanism on the mating patterns of pentatomids.

Dietary methoprene supplement promotes early sexual maturation of male Queensland fruit fly Bactrocera tryoni

Sterile insect technique (SIT) is an environmentally benign pest management technique that relies on released sterile male insects mating with, and curtailing reproduction of, wild females. However, for species with high mortality rates and long adult maturation phases, a large proportion of the released insects can die before maturing and so fail to contribute to SIT. To counter this problem, inclusion of yeast hydrolysate in pre-release diets and treatment of pupae or adults with methoprene, a juvenile hormone analogue, have been investigated as means of accelerating development of some fruit flies, including Queensland fruit fly, Bactrocera tryoni (Froggatt) (‘Q-fly’). Methoprene has most often been administered topically in acetone solution, which is toxic, flammable, and impractical for operational settings. As a practical alternative, we incorporated methoprene (0, 0.05, 0.1, and 0.5%) into Q-fly adult diet of sugar only or sugar mixed with yeast hydrolysate for 2 days, and then provided sugar only for the rest of the trial period. Mating performance of males and females was tested from 4 to 30 days of age. Flies provided sugar mixed with yeast hydrolysate had increased mating propensity in comparison with flies that were provided sugar only. At all ages and for both diets, all methoprene doses increased male mating probability. Methoprene treatment did not affect copula latency of males that received yeast hydrolysate, but males that received only sugar mated earlier if they had received 0.05% methoprene. Methoprene treatment of males was also associated with longer copulations, which may affect fertility of females that later remate. Females differed from males in that methoprene treatment did not significantly affect mating probability or latency, but resembled males in that methoprene treatment resulted in longer copulations. Sex differences in response to methoprene may lead to male-biased operational sex ratio when bisex Q-fly strains are used in SIT. Yeast hydrolysate increased longevity of both males and females, but methoprene treatment did not affect longevity. Overall, findings of the present study indicate that Q-fly sexual maturation can be accelerated, and SIT might hence be enhanced, by incorporation of methoprene and yeast hydrolysate in pre-release diet.

Experimental evolution with an insect model reveals that male homosexual behaviour occurs due to inaccurate mate choice

The existence of widespread male same-sex sexual behaviour (SSB) is puzzling: why does evolution allow costly homosexual activity to exist, when reproductive fitness is primarily achieved through heterosexual matings? Here, we used experimental evolution to understand why SSB occurs in the flour beetle Tribolium castaneum. By varying the adult operational sex ratio across 82–106 generations, we created divergent evolutionary regimes that selected for or against SSB depending upon its function. Male-biased (90:10 M:F) regimes generated strong selection on males from intrasexual competition, and demanded improved ability to locate and identify female mates. By contrast, Female-biased regimes (10:90 M:F) generated weak male–male competition, and relaxed selection on mate-searching abilities in males. If male SSB functions through sexually selected male–male competition, it should be more evident within Male-biased regimes, where reproductive competition is nine times greater, than in the Female-biased regimes. By contrast, if SSB exists due to inaccurate mate choice, it should be reduced in Male-biased regimes, where males experience stronger selection for improved mate finding and discrimination abilities than in the Female-biased regime, where most potential mating targets are female. Following these divergent evolutionary regimes, we measured male engagement in SSB through choice experiments simultaneously presenting female and male mating targets. Males from both regimes showed similar overall levels of mating activity. However, there were significant differences in levels of SSB between the two regimes: males that evolved through male-biased operational sex ratios located, mounted and mated more frequently with the female targets. By contrast, males from female-biased selection histories mated less frequently with females, exhibiting almost random choice between male and female targets in their first mating attempt. Following experimental evolution, we therefore conclude that SSB does not function through sexually selected male–male competition, but instead occurs because males fail to perfectly discriminate females as mates.

The association between male-biased sex ratio and indicators of stress in red-spotted newts

In populations with a male-biased operational sex ratio, coercive mating by males can have fitness consequences for females. One component of reduced fitness for females in populations with a male-biased OSR may be greater activation of the stress response, resulting in higher corticosterone release rates (CORT; a glucocorticoid stress hormone in amphibians). We test the hypothesis that a male-biased sex ratio affects female activity and release rates of CORT and testosterone (T) in male and female red-spotted newts (Notophthalmus viridescens). First, we evaluated if chemical cues from a male-biased sex ratio affect activity and CORT release rates in females. We predicted that females exposed to chemical cues of three males would be less active and have higher CORT release rates than those exposed to chemical cues of one male. Second, we measured CORT release rates of red-spotted newts in field enclosures with either a male-biased or a female-biased sex ratio. We predicted that females in the male-biased treatment would have higher CORT and T release rates than those in a female-biased treatment, owing to higher levels of male harassment. We also predicted that males would have higher CORT and T release rates in male-biased treatments due to higher levels of male-male competition. Females were not less active in response to chemical cues from more males over fewer males, but there was a positive relationship between female activity and CORT when they were exposed to the cues of three males. We also found that females, but not males, in the male-biased sex ratio treatment had higher CORT and T release rates than those in the female-biased treatment. Our results support the hypothesis that a male-biased sex ratio leads to a higher stress response, which may underlie the observed decrease in immune function and body condition in previous work exposing female red-spotted newts to a male-biased sex ratio. This study furthers our understanding of the mechanistic basis for costs associated with a male-biased sex ratio in a pond-breeding amphibian.

Male-biased operational sex ratios and the Viking phenomenon: an evolutionary anthropological perspective on Late Iron Age Scandinavian raiding

In this paper, we use a combination of evolutionary theory, ethnographic data, written sources, and archaeological evidence to develop a new explanation for the origins of Viking raiding. Our argum ...

Low reproductive skew despite high male-biased operational sex ratio in a glass frog with paternal care.

BackgroundReproductive skew, the uneven distribution of reproductive success among individuals, is a common feature of many animal populations. Several scenarios have been proposed to favour either high or low levels of reproductive skew. Particularly a male-biased operational sex ratio and the asynchronous arrival of females is expected to cause high variation in reproductive success among males. Recently it has been suggested that the type of benefits provided by males (fixed vs. dilutable) could also strongly impact individual mating patterns, and thereby affecting reproductive skew. We tested this hypothesis in Hyalinobatrachium valerioi, a Neotropical glass frog with prolonged breeding and paternal care.ResultsWe monitored and genetically sampled a natural population in southwestern Costa Rica during the breeding season in 2012 and performed parentage analysis of adult frogs and tadpoles to investigate individual mating frequencies, possible mating preferences, and estimate reproductive skew in males and females. We identified a polygamous mating system, where high proportions of males (69 %) and females (94 %) reproduced successfully. The variance in male mating success could largely be attributed to differences in time spent calling at the reproductive site, but not to body size or relatedness. Female H. valerioi were not choosy and mated indiscriminately with available males.ConclusionsOur findings support the hypothesis that dilutable male benefits - such as parental care - can favour female polyandry and maintain low levels of reproductive skew among males within a population, even in the presence of direct male-male competition and a highly male-biased operational sex ratio. We hypothesize that low male reproductive skew might be a general characteristic in prolonged breeders with paternal care.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0469-z) contains supplementary material, which is available to authorized users.

The effect of sex ratio on size-assortative mating in two explosively breeding anurans

Size-assortative mating (SAM) is a widespread phenomenon related to individual fitness. In our study, we examined: (i) the appearance of SAM, and (ii) the effect of sex ratio on intensity of SAM in wild populations of two explosively breeding anurans, common frogs,Rana temporaria, and common toads,Bufo bufo. Despite a higher male-biased operational sex ratio (OSR) in toads, the body lengths of the paired males and females were significantly correlated only in frogs. Increasing male-male competition, assessed via the OSR, resulted in a stronger correlation also in frogs only. Thus, great variability in the presence and intensity of SAM has been observed within both studied species.

Female polyandry and size-assortative mating in isolated local populations of the Japanese common toadBufo japonicus

In anurans, female polyandry under male harassment is distributed across taxa because of external aquatic fertilization. According to the sexual selection theory, male–male competition for access to females is affected by the operational sex ratio (OSR) and population density. The Japanese common toad, Bufo japonicus, is widespread in mainland Japan, and like the European common toad, B. bufo, it engages in explosive breeding. In this study, we observed the breeding behaviour of B. japonicus in isolated local populations for over four years in two breeding ponds with different population sizes and densities: large-low (L-pond) and small-high (S-pond). We analysed the relative polyandry ratio in egg clutches laid by females and estimated the size-assortative mating pattern to be an indicator of male–male competition in the two ponds. Both ponds tended to exhibit a size-assortative mating pattern; however, the frequency of polyandry was different in the two ponds (L-pond = 20% and S-pond = 90%). Our results showed that polyandry could occur without multiple amplexus with a high population density, i.e. eggs were often fertilized by free-swimming sperm in the small shallow pond. We propose that high female polyandry ratios without continuous male harassment are generated because of a male-biased OSR and a high population density in the small pond. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 236–242.