Sexual Selection In Males Research Articles

Anisogamy and the Darwin–Bateman paradigm

Abstract The Darwin–Bateman paradigm advanced as the central concept to explain the evolutionary origin of sex differences. However, debates regarding its theoretical underpinnings persist, particularly with respect to the role of anisogamy in sexual selection. The theoretical work presented by Lehtonen and Parker suggests that the initial split in gamete production rate drives sex differences in sexual selection but that any further variation in the degree of anisogamy is not expected to alter the strength of sexual selection in males and females. Here, I discuss the historical background of a recently emerged controversy and present empirical data that corroborate the theoretical predictions. Lehtonen and Parker’s contribution refines our understanding of the Darwin–Bateman paradigm by providing a broad theory for large-scale patterns of sex differences that can be observed in nature. Further understanding of how demographic and environmental factors influence sexual selection is essential to predict the vast diversity of sex differences across the tree of life, beyond the primordial impact of anisogamy.

Evidence for stronger sexual selection in males than females using an adapted method of Bateman's classic study of Drosophila melanogaster.

Bateman's principles, originally a test of Darwin's theoretical ideas, has since become fundamental to sexual selection theory and vital to contextualising the role of anisogamy in sex differences of precopulatory sexual selection. Despite this, Bateman's principles have received substantial criticism, and researchers have highlighted both statistical and methodological errors, suggesting that Bateman's original experiment contains too much sampling bias for there to be any evidence of sexual selection. This study uses Bateman's original method as a template, accounting for two fundamental flaws in his original experiments, (i) viability effects and (ii) a lack of mating behaviour observation. Experimental populations of Drosophila melanogaster consisted of wild-type focal individuals and non-focal individuals established by backcrossing the brown eye (bw -) eye-colour marker - thereby avoiding viability effects. Mating assays included direct observation of mating behaviour and total number of offspring, to obtain measures of mating success, reproductive success, and standardised variance measures based on Bateman's principles. The results provide observational support for Bateman's principles, particularly that (i) males had significantly more variation in number of mates compared to females and (ii) males had significantly more individual variation in total number of offspring. We also find significantly steeper Bateman gradient for males compared to females, suggesting that sexual selection is operating more intensely in males. However, female remating was limited, providing the opportunity for future study to further explore female reproductive success in correlation with higher levels of remating.

Population density affects sexual selection in an insect model

Abstract Understanding the impact of demographic and ecological factors on the strength of sexual selection is pivotal to predict eco‐evolutionary dynamics in populations facing environmental change. Density is expected to show pervasive intra‐ and interspecific variation in natural populations, but its effect on sexual selection remains largely unexplored. We tested experimentally the effect of density on standardized metrics of sexual selection in male and female red flour beetles. Specifically, we explored density effects during mating by manipulating the size of mating groups and the mating arena. We found that higher densities imposed by a larger group size amplified the opportunity for pre‐copulatory sexual selection in females and, to a smaller extent, also in males. Moreover, in males, we detected a higher opportunity for post‐copulatory sexual selection in larger groups. By contrast, higher densities imposed by differences in the size of the mating arena resulted in a steeper male sexual selection gradient. Overall, these data suggest that density is an important environmental factor contributing to the tremendous variation in the strength of sexual selection within and among species. Read the free Plain Language Summary for this article on the Journal blog.

Women misjudge men’s physical characteristics based on vocal cues

ABSTRACT Voice is an important biological cue, which may reveal a significant amount of information about an individual. Particularly in males, it plays a crucial role in processes like male competition or sexual selection. Additionally, voice can provide a cue for body size assessment. This study investigates the relationship between male voice characteristics and physical features (assessed by women) and determines the accuracy of these assessments. Three groups of female judges assessed 60 male voices (20 different voices per group) across seven categories of male physical features: height, body fat, musculature, body shape, hirsuteness, age and strength. Recordings of five vowels and sentence and number of anthropometric measurements were made for each of the studied men. Intra- and extragroup agreement of assessments of men’s physical characteristics was demonstrated. Men with lower fundamental frequency (F0 ) and lower formant dispersion (Df ) values were perceived as being heavier, older, stronger and more likely to have chest hair. However, across all the analysed fields of assessment, no accuracy was registered between estimates and men’s actual physical characteristics. These findings suggest that females were guided by stereotypes in their assessment of men’s appearance from voice alone. We propose the size exaggeration hypothesis as an explanation of this phenomenon

Sex-specific selection patterns in a dioecious insect-pollinated plant.

Competition for mate acquisition is the hallmark of any sexual organism. In insect-pollinated plants, competition to attract pollinators is expected to result in pollinator-mediated selection on attractive floral traits. This could overlap with sexual selection if the number of mating partners increases with pollinator attraction, resulting in an improved reproductive success. In this study, we measured a set of floral traits and estimated individual fitness in male and female Silene dioica in an experimental population. Results align with the predictions of Bateman's principles, in the absence of pollen limitation. In females, natural selection acted on traits that are typically linked with fertility (number of flowers and number of gametes), and selection strength was similar in open- and hand-pollinated females, suggesting a limited role of pollinator-mediated selection. In males, flowering duration and corolla width were positively associated with both reproductive success and number of mates, suggesting that sexual selection has played a role in the evolution of these traits. The use of Bateman's metrics further confirmed stronger sexual selection in males than in females. Taken together, our results shed light on the occurrence of sex-specific patterns of selection in an insect-pollinated plant population.

Extra-pair paternity and sexual dimorphism in birds.

Differences in the strength of sexual selection between males and females can lead to sexual dimorphism. Extra-pair paternity (EPP) can increase the variance in male reproductive success and hence the opportunity for sexual selection. Previous research on birds suggests that EPP drives the evolution of dimorphism in plumage colour and in body size. Because EPP increases the intensity of sexual selection in males, it should lead to increased dimorphism in species with larger or more colourful males, but decreased dimorphism in species with larger or more colourful females. We explored the covariation between EPP and sexual dimorphism in wing length and plumage colouration in 401 bird species, while controlling for other, potentially confounding variables. Wing length dimorphism was associated positively with the frequency of EPP, but also with social polygamy, sex bias in parental behaviour and body size and negatively with migration distance. The frequency of EPP was the only predictor of plumage colour dimorphism. In support of our prediction, high EPP levels were associated with sexual dichromatism, positively in species in which males are more colourful and negatively in those in which females are more colourful. Contrary to our prediction, high EPP rates were associated with increased wing length dimorphism in species with both male- and female-biased dimorphism. The results support a role for EPP in the evolution of both size and plumage colour dimorphism. The two forms of dimorphism were weakly correlated and predicted by different reproductive, social and life-history traits, suggesting an independent evolution.

Climate shapes patterns of sexual size and shape dimorphism across the native range of the green anole lizard,Anolis carolinensis(Squamata: Dactyloidae)

AbstractGeographical variation in sexual size dimorphism (SSD) can result from the combined effects of environmental and sexual selection. To understand the determinants of SSD across geographical landscapes, we tested for relationships between SSD and climatic variables in the widespread lizard Anolis carolinensis. To distinguish alternative hypotheses for observed patterns of variation in SSD, we also examined sex-specific patterns of body size evolution and asked whether SSD was associated with certain patterns of sexual shape dimorphism. We found strong evidence for Rensch’s rule (an increase in male-biased SSD with average body size) in A. carolinensis and evidence for the reversed version of Bergmann’s rule (an increase in body size towards warmer environments) in males. Across populations, SSD was positively related to temperature; however, female body size was not related to any climatic variable, suggesting that the latitudinal gradient of SSD might be driven by a gradient in the intensity of sexual selection acting on males. Sexual size dimorphism was positively correlated with sexual dimorphism in head shape and negatively correlated with limb length dimorphism, suggesting that sexual selection in males might drive the evolution of SSD and that differences in size and limb shape between sexes might represent alternative strategies to avoid competition for the same resources.

Sexual selection for males with beneficial mutations

Sexual selection is the process by which traits providing a mating advantage are favoured. Theoretical treatments of the evolution of sex by sexual selection propose that it operates by reducing the load of deleterious mutations. Here, we postulate instead that sexual selection primarily acts through females preferentially mating with males carrying beneficial mutations. We used simulation and analytical modelling to investigate the evolutionary dynamics of beneficial mutations in the presence of sexual selection. We found that female choice for males with beneficial mutations had a much greater impact on genetic quality than choice for males with low mutational load. We also relaxed the typical assumption of a fixed mutation rate. For deleterious mutations, mutation rate should always be minimized, but when rare beneficial mutations can occur, female choice for males with those rare beneficial mutations could overcome a decline in average fitness and allow an increase in mutation rate. We propose that sexual selection for beneficial mutations could overcome the ‘two-fold cost of sex’ much more readily than choice for males with low mutational load and may therefore be a more powerful explanation for the prevalence of sexual reproduction than the existing theory. If sexual selection results in higher fitness at higher mutation rates, and if the variability produced by mutation itself promotes sexual selection, then a feedback loop between these two factors could have had a decisive role in driving adaptation.

Population and reproductive structure in the endangered and highly endemic freshwater crab Aegla concepcionensis (Decapoda:Pleocyemata:Aeglidae) from Chile

AbstractPopulation and reproductive information of highly endemic species allow us to understand their underlying conservation problems. Aegla concepcionensis is restricted to a small and intervened Chilean basin, and its conservation status has varied from extinct in nature to endangered. We characterized their life history measuring population, morphological and environmental variables during an annual cycle capturing individuals with a catch and release method based on electroshocking. Although the maximum water temperature was related to the recruitment, it can be physiologically risky for the remaining macroinvertebrate community. The relationship between abundance and narrow pH variations indicates a condition of unstable equilibrium given the environmental deterioration by deforestation. Sex ratio was predominantly male biased during copulatory activity, and sexually dimorphic body size distributions supported the hypothesis of greater natural selection in females and sexual selection in males. The period of ovigerous females was comparatively restricted, late and consistent with an efficient ecophysiological strategy of reproductive investment. Patterns of pubertal moult, onset of morphometric maturity, absence of morphological differentiation in both sexes suggested that A. concepcionensis tends to maximize reproductive performance favouring the recovery of their relict populations.

Strong sexual selection fails to protect against inbreeding-driven extinction in a moth

Abstract Sexual selection is predicted to influence population persistence because skew in male reproductive success may facilitate the purging of mutation load. We manipulated the strength of sexual selection in populations of Indian meal moths, Plodia interpunctella, by adjusting adult sex ratios to be either male- or female-biased, leading to strong and weak sexual selection in males, respectively. After between 19 and 22 generations of experimental evolution, we examined whether mutation load differed between these populations by enforcing successive generations of inbreeding, tracking extinction events, offspring viability and assaying the effect of inbreeding on male mating success and female choice. We found no effect of the strength of sexual selection on the rate of extinction or offspring viability. We did, however, find changes in both male mating success and female choice, with both being influenced by the sex ratio treatment and the number of generations of inbreeding. Males from male-biased populations were more successful at mating with stock females, and mating success declined rapidly with inbreeding regardless of sex ratio treatment. Females from male-biased populations were less likely to mate with stock males at the onset of the experiment, but tended to mate more frequently with increasing inbreeding compared to females from female-biased populations. Our results demonstrate that while mating behaviors have diverged between male-biased and female-biased lines mutation loads remained similar. This suggests that the benefits of sexual selection to population fitness may be low or slow to accumulate under the benign environmental conditions in which these populations evolved.

Observation of Infanticide in the Particolored Flying Squirrel (Hylopetes alboniger) from a Forest in Northeastern Bangladesh

Infanticide, the intentional killing of conspecific infants, has been observed widely in mammals, including squirrels. Several ground squirrels revealed this behavioral anomaly, yet no report has been published on the flying squirrels. We report an observation of killing an infant of the particolored flying squirrel (Hylopetes alboniger) by a conspecific adult intruder in Satchari National Park of northeast Bangladesh. Among the several adaptive explanations for infanticide, our observations point to sexual selection in males that confers a competitive advantage by making females receptive. However, the resource competition hypothesis, where the intruder's offsprings gain access to resources as a result of the infanticide cannot be ruled out. Extensive studies are needed to document the extent of infanticide in flying squirrels and their adaptive significance.

Heterochiasmy and Sexual Dimorphism: The Case of the Barn Swallow (Hirundo rustica, Hirundinidae, Aves).

Heterochiasmy, a sex-based difference in recombination rate, has been detected in many species of animals and plants. Several hypotheses about evolutionary causes of heterochiasmy were proposed. However, there is a shortage of empirical data. In this paper, we compared recombination related traits in females and males of the barn swallow Hirundo rustica (Linnaeus, 1758), the species under strong sexual selection, with those in the pale martin Riparia diluta (Sharpe and Wyatt, 1893), a related and ecologically similar species with the same karyotype (2N = 78), but without obvious sexual dimorphism. Recombination traits were examined in pachytene chromosome spreads prepared from spermatocytes and oocytes. Synaptonemal complexes and mature recombination nodules were visualized with antibodies to SYCP3 and MLH1 proteins, correspondingly. Recombination rate was significantly higher (p = 0.0001) in barn swallow females (55.6 ± 6.3 recombination nodules per autosomal genome), caused by the higher number of nodules at the macrochromosomes, than in males (49.0 ± 4.5). They also showed more even distribution of recombination nodules along the macrochromosomes. At the same time, in the pale martin, sexual differences in recombination rate and distributions were rather small. We speculate that an elevated recombination rate in the female barn swallows might have evolved as a compensatory reaction to runaway sexual selection in males.

Female size and pre-copulatory sexual selection by males of intertidal snail (Littorina saxatilis)

Littorina saxatilis, the rough periwinkle, is highly promiscuous and polyandrous; female L. saxatilis snails rarely reject male advances. Sexual selection by males has been observed in this species. Sexual selection is one of the driving forces of evolution and may be a significant contributor to partial reproductive isolation between two ecotypes of L. saxatilis. Male sexual selection based on female size was investigated for wave-exposed crab ecotype snails in this study. Males and females were measured and placed in mating arenas. Males were presented with a choice of a smaller or larger female relative to themselves. Mating frequency and duration was recorded. A total of 19 successful trials were performed. A significantly higher mating frequency (p<0.005) was associated with larger females, indicating that males exhibit strong pre-copulatory sexual selection. Mating duration was significantly longer for larger female mating events (p<0.05) but was also equally determined by male size (p<0.05) as larger males tended to mate for longer. These results indicate that a strong sexual selection by males exists for L. saxatilis, in which larger females are preferred. This behavior may be a response to perceived fecundity of females, and/or may be a product of selection against hybrids.

Does operational sex ratio influence relative strength of purging selection in males versus females?

According to theory, sexual selection in males may efficiently purge mutation load of sexual populations, reducing or fully compensating 'the cost of males'. For this to occur, mutations not only need to be deleterious to both sexes, they also must affect males more than females. A frequently overlooked problem is that relative strength of selection on males versus females may vary between environments, with social conditions being particularly likely to affect selection in males and females differently. Here, we induced mutations in red flour beetles (Tribolium castaneum) and tested their effect in both sexes under three different operational sex ratios (1:2, 1:1 and 2:1). Induced mutations decreased fitness of both males and females, but their effect was not stronger in males. Surprisingly, operational sex ratio did not affect selection against deleterious mutations nor its relative strength in the sexes. Thus, our results show no support for the role of sexual selection in the evolutionary maintenance of sex.

How conflict shapes evolution in poeciliid fishes

In live-bearing animal lineages, the evolution of the placenta is predicted to create an arena for genomic conflict during pregnancy, drive patterns of male sexual selection, and increase the rate of speciation. Here we test these predictions of the viviparity driven conflict hypothesis (VDCH) in live-bearing poecilid fishes, a group showing multiple independent origins of placentation and extreme variation in male sexually selected traits. As predicted, male sexually selected traits are only gained in lineages that lack placentas; while there is little or no influence of male traits on the evolution of placentas. Both results are consistent with the mode of female provisioning governing the evolution of male attributes. Moreover, it is the presence of male sexually selected traits (pre-copulatory), rather than placentation (post-copulatory), that are associated with higher rates of speciation. These results highlight a causal interaction between female reproductive mode, male sexual selection and the rate of speciation, suggesting a role for conflict in shaping diverse aspects of organismal biology.

The role of male coloration and ornamentation in potential alternative mating strategies of the dimorphic jumping spider, Maevia inclemens

Polymorphism can arise across taxa due to various selection pressures and potentially lead to alternative mating or antipredator strategies. For male jumping spiders, sexual selection and predation risk are often intertwined when courting cannibalistic females and may be a driving factor in the polymorphism of the jumping spider, Maevia inclemens. The dimorphic males of M. inclemens differ dramatically in their complex courtship behavior and display traits that may function as alternative mating strategies to reduce female aggression and maximize mating success. We hypothesized that males of the “tufted” morph honestly communicate condition or body size to females with three conspicuous tufts of setae on their head and males of the “striped” morph reduce female aggression with coloration commonly found in aposematic animals (here, yellow-orange pedipalps and striped legs). We examined correlations between tuft length and symmetry and metrics of body size and condition in field-collected spiders and conducted prey color choice tests (with live color-manipulated prey) to determine if yellow-orange and striped prey are avoided. Tuft length was variable and correlated with male size (but not condition). All prey color types were attacked at equal rates, but spiders oriented to striped prey more often, suggesting that male stripes may attract female attention without increasing predation. This study provides insight into the potential functions of the different courtship and visual displays of M. inclemens males. Using jumping spiders to study polymorphism can provide new insight into how multiple morphs can evolve, as males use mating strategies not only to impress females but also avoid getting eaten by their potential mates.Significance statementUnderstanding the selection pressures that shape and maintain polymorphisms in natural populations is an active area of inquiry, yet most of what we know comes from a small handful of well-studied vertebrate taxa. The unique biology of jumping spiders and the fact that males have to avoid cannibalism during courtship, makes them well-suited to provide novel insights into the functions and maintenance of dimorphic male traits. The unusual male dimorphism of M. inclemens captured the attention of naturalists as early as the 1800s, yet we still do not understand why the two male morphs differ so dramatically in morphology and courtship behavior. Here, we propose and test a novel hypothesis that provides insight into the long-studied but still largely unexplained phenomenon of male dimorphism in this species.

Environmental and demographic drivers of male mating success vary across sequential reproductive episodes in a polygynous breeder.

Ecological and social factors underpinning the inequality of male mating success in animal societies can be related to sex ratio, sexual conflict between breeders, effects of nonbreeders, resource dispersion, climatic conditions, and the various sequential stages of mating competition that constitute the sexual selection process. Here, we conducted an individual‐based study to investigate how local resource availability and demography interact with annual climate conditions to determine the degree of male mating inequality, and thus opportunity for sexual selection across two sequential reproductive episodes (harem and subsequent mate acquisition) in a naturally regulated (feral) horse population in Sable Island National Park Preserve, Canada. Using a 5‐year, spatially explicit, mark‐resight dataset and hierarchical mixed‐effects linear modeling, we evaluated the influence of adult sex ratio (ASR) on mating success and then tested for effects of freshwater availability, density, unpaired male abundance, and precipitation during each breeding season. Unpaired male abundance, freshwater availability, and ASR differed in their effects on male mating success according to year and selection episode. Opportunity for sexual selection in males associated with harem acquisition increased with ASR, and unpaired male abundance further explained weather‐related interannual variation after accounting for ASR. In contrast, once a harem was secured, ASR had little effect on male mating inequality in regard to acquiring additional females, while interannual variation in mating inequality increased with decreasing freshwater availability. Our findings show that local demography, resource availability, and weather effect opportunity for sexual selection in males differently depending on selection episode, and can attenuate or accentuate effects of ASR.

The evolution and diversity of intra-male sperm translocation in Odonata: a unique behaviour in animals

Behavioural diversity is a basic component of biodiversity, with implications in ecological interactions at the intra- and interspecific levels. The reproductive behaviour of Odonata (dragonflies and damselflies) is unique among insects and conditioned by the anatomical separation between the male’s reproductive organs and the intromittent organ. Prior to mating, males must translocate sperm from the genital pore in the ninth abdominal segment to the seminal vesicle located ventrally in the second abdominal segment. This behaviour, exclusive to odonates, is known as intra-male sperm translocation (ST). Here, we review the literature on ST and use phylogenetic comparative analyses to investigate the evolution of ST within the Odonata. Information on ST was compiled for 176 species, with the commonest variant being ST once per mating, after tandem formation (66%). Other variants found were ST involving precopulatory genital touching (10%), ST by the male alone before tandem (16%) or after copulation (5%), and repetition of ST during the same copulation (3%). The precopulatory genital touching might have evolved to detect female receptivity. ST before tandem formation might be favoured when mating opportunities are scarce and copulations are brief. ST after mating might be favoured if males need to be ready to copulate fast. Finally, repeated ST could have evolved through postcopulatory sexual selection in males with limited sperm removal ability, as a means to improve their sperm competition. The most plausible scenario for the evolution of ST is that the ancestors of the Odonata produced a spermatophore and attached it to the body, leading towards the evolution of the secondary genitalia in males. Our study emphasises the role of behavioural diversity to understand behavioural evolution. Unique behaviours are exclusive of a few individuals, populations and/or species. The intra-male sperm translocation (ST) of dragonflies and damselflies is a unique behaviour in animals: before mating, males need to transfer sperm from the primary to the secondary genitalia, which are anatomically separated. Thus, the viability and quality of sperm (i.e. fertility) will depend on the timing of ST relative to copulation. Our literature review found a variety of ST variants, being ST in tandem and before copulation the ancestral strategy. We discuss putative evolutionary routes for all the variants found and emphasise the importance of retrieving detailed observations of such unique behaviours in the field, which could help to better understand behavioural evolution in this insect group. Behavioural diversity is rarely addressed by conservation strategies, despite unique behaviours being at a higher risk of extinction.

Mating System, Reproductive Success, and Sexual Selection in Bluntnose Klipfishes (Clinus cottoides).

A critical part of the sexual selection process in animals is the genetic mating system. Quantifying mating systems, especially in species with cryptic life histories can be challenging. One approach is to use genotypic markers and accurate parentage analysis, along with methods to account for bias when sampling natural populations, to calculate sexual selection metrics derived from Bateman's principles. In this study, 3 microsatellites were used to genotype 48 adults (23 female and 25 male) and 342 offspring from known mothers of live-bearing bluntnose klipfish. Parentage analysis was performed to interpret mating and reproductive success for both sexes. Metrics quantified were the opportunity for selection (I), the opportunity for sexual selection (Is), absolute (βss), and standardized (β'ss) Bateman gradients and the maximum intensity of precopulatory sexual selection (s'max). Multiple mating by both sexes were revealed by parentage analysis. However, females did not show significant Bateman gradients or a significant maximum intensity of precopulatory sexual selection (s'max), whereas male sexual selection metrics were all significantly greater than 0. These results suggest a polygynandrous mating system for this species. There is an opportunity for sexual selection to act on males but not females in this population, which is evolutionary tied to anisogamy, parental investment, and sex roles.

Sexual selection and its evolutionary consequences in female animals.

For sexual selection to act on a given sex, there must exist variation in the reproductive success of that sex as a result of differential access to mates or fertilisations. The mechanisms and consequences of sexual selection acting on male animals are well documented, but research on sexual selection acting on females has only recently received attention. Controversy still exists over whether sexual selection acts on females in the traditional sense, and over whether to modify the existing definition of sexual selection (to include resource competition) or to invoke alternative mechanisms (usually social selection) to explain selection acting on females in connection with reproduction. However, substantial evidence exists of females bearing characters or exhibiting behaviours that result in differential reproductive success that are analogous to those attributed to sexual selection in males. Here we summarise the literature and provide substantial evidence of female intrasexual competition for access to mates, female intersexual signalling to potential mates, and postcopulatory mechanisms such as competition between eggs for access to sperm and cryptic male allocation. Our review makes clear that sexual selection acts on females and males in similar ways but sometimes to differing extents: the ceiling for the elaboration of costly traits may be lower in females than in males. We predict that current and future research on female sexual selection will provide increasing support for the parsimony and utility of the existing definition of sexual selection.