Rival Males Research Articles

Sexual trait may simultaneously indicate sperm production and nutritional fitness in uniparental nest‐guarding fish: a case study on Amur sleeper

AbstractThe reproductive success of uniparental males depends much on their nutritional stage (i.e. body condition). Therefore, secondary sexual traits should convey information not only on fecundity but also on nutritional stage. To test this hypothesis, we evaluate relationships between head crest height (HCH), as a secondary sexual trait, relative testes mass (an indicator of sperm production), body condition (an indicator of nutritional status) and body mass of males of uniparental Amur sleeper Perccottus glenii in two contrasting habitats. Furthermore, we examined whether head crest is only a pure investment to advertise male fitness – either to females, rival males or other fish approaching the nest – or it comprises some regainable energy as well. We found that HCH is closely related to relative testes mass, and body condition especially at the beginning of the reproductive period. The head crest consisted of a swollen connective tissue in the supraorbital region of the head, and an oedematous epaxial muscle in the nuchal region. Furthermore, the head crest also comprised of adipose tissue, although not as much as assumed. Therefore, we argue that HCH represents a reliable signal of multiple aspects of male quality; it indicates readiness to spawn and could potentially effectively facilitate female choice towards large males with high fecundity and great nutritional stage, which is essential to good guarding performance. Moreover, the head crest itself also could contribute to nest‐guarding performance by virtually enlarging body size and by representing a minor fat reserve.

Reproductive behavior of Spix’s Whiptails in the wild: understanding the costs and benefits of mate-guarding

Across animal taxa, females of non-territorial species have potential opportunities to mate with multiple partners; hence, the primary mechanism available for males to ensure paternity is to guard the receptive female after copulation and repel other males. Hypothetically, mate-guarding is costly for males in terms of energy acquisition and increased risk of injury, and beneficial for females in terms of decreased harassment by other males and an increase in available foraging time. Here, we provide a detailed description of mating behavior and test these hypotheses in the Spix’s Whiptail (Ameivula ocellifera). Mating behavior is characterized by the following events: (1) a male courts a female in the entrance of her burrow; (2) if courtship is accepted by the female, a consensual copulation occurs; (3) after copulation the male accompanies the female during her daily activity, being aggressive towards other males; (4) when the female returns to the burrow, the companion male remains vigilant at the entrance and repels rival males. Besides the mate-guarding strategy, alternative mating tactics are adopted by some males that do not guard females after courtship and consensual copulation, while others try to copulate opportunistically with a female without prior courtship. Companion males spent more time vigilant, less time actively foraging, and captured less prey when compared to solitary males. Accompanied females captured prey in a similar proportion to solitary females but spent more time vigilant and less time foraging. Companion males won 100% of their interactions with rival males, chasing them away from the females. Accompanied females hence did not suffer harassment from other males when companion males were close. Our results evidence energetic costs of mate-guarding for males but not increased risk of injuries. By accepting mate-guarding, females do not appear to have energetic gains and lose the advantage of cryptic mate choice but can benefit from access to high-quality males and protection from harassment.

Rutting vocal display in male impala (Aepyceros melampus) and overlap with alarm context

BackgroundThe rutting vocal display of male impala Aepyceros melampus is unique for its complexity among ruminants. This study investigates bouts of rutting calls produced towards potential mates and rival males by free-ranging male impala in Namibia. In particular, a comparison of male rutting and alarm snorts is conducted, inspired by earlier findings of mate guarding by using alarm snorts in male topi Damaliscus lunatus.ResultsRutting male impala produced 4–38 (13.5 ± 6.5) rutting calls per bout. We analyzed 201 bouts, containing in total 2709 rutting calls of five types: continuous roars produced within a single exhalation-inhalation cycle; interrupted roars including few exhalation-inhalation cycles; pant-roars distinctive by a pant-phase with rapidly alternating inhalations and exhalations; usual snorts lacking any roar part; and roar-snorts starting with a short roar part. Bouts mostly started and ended with usual snorts. Continuous roars were the shortest roars. The average duration of the exhalatory phase was longest in the continuous roars and shortest in the pant-roars. The average fundamental frequency (49.7–51.4 Hz) did not differ between roar types. Vocal tract length, calculated by using measurements of the first four vocal tract resonances (formants), ranged within 381–382 mm in all roar types. In the studied male impala, rutting snorts within bouts of rutting calls were longer and had higher values of the upper quartile in the call spectra than alarm snorts produced towards potential danger.ConclusionsAdditional inhalations during the emission of the interrupted and pant-roars prolong their duration compared to the continuous roars but do not affect the fundamental frequency or the degree of larynx retraction while roaring. Alarm snorts are separated from one another by large intervals, whereas the intervals between rutting snorts within bouts are short. Sometimes, rutting snorts alternate with roars, whereas alarm snorts do not. Therefore, it is not the acoustic structure of individual snorts but the temporal sequence and the occasional association with another call type that defines snorts as either rutting or alarm snorts. The rutting snorts of male impala may function to attract the attention of receptive females and delay their departure from a male’s harem or territory.

Divergence of responses to variable socio‐sexual environments in laboratory populations of Drosophila melanogaster evolving under altered operational sex ratios

Post-copulatory sexual selection (PSS) is an important selective force that determines fitness in polyandrous species. PSS can be intense in some cases and can drive the evolution of remarkable ejaculate properties. In males, investment in ejaculate plays an important role in the outcome of PSS. Thus, males are expected to adaptively tailor their ejaculate according to the perceived competition in their vicinity. Plastic responses in ejaculate investment to variation in intrasexual competition are disparate and widespread in males. We investigated the evolution of plasticity in reproductive traits using Drosophila melanogaster populations evolving for more than 150 generations under male- or female-biased sex ratios. When exposed to different numbers of competitors early in their life, males from these two regimes responded differently in terms of their copulation duration and sperm competitive ability. In addition, the effect of this early life experience wore off at different rates in males of male-biased and female-biased regimes with increasing time from the removal of competitive cues. Furthermore, our study finds that males change their reproductive strategies depending upon the identity of rival males. Together, our results provide evidence of the evolution of male reproductive investment that depends on socio-sexual cues experienced early in life.

The potential role of reproductive interference in the decline of native green treefrogs following Cuban treefrog invasions

Reproductive interference is increasingly implicated in the decline of native taxa following alien species invasions. We examined reproductive interference in the context of acoustic modulation of hormone levels and declines in native green treefrogs (Hyla cinerea) following invasions of Cuban treefrogs (Osteopilus septentrionalis) in the southeastern United States. The motivation for our study stemmed from similarities in spectro-temporal properties of Cuban treefrog courtship calls and green treefrog aggressive calls. The aggressive calls of green treefrogs stimulate glucocorticoid production in rival conspecific males, which suppresses androgen production and reproductive behavior. We thus hypothesized that native male green treefrogs exposed to advertisement calls of this invasive species exhibit increased levels of circulating glucocorticoids. We found that broadcast aggressive calls of green treefrogs stimulated glucocorticoid production in conspecific males but that Cuban treefrog vocalizations did not increase glucocorticoid levels in green treefrogs. In natural choruses, the density of calling male green treefrogs and the proportion of non-calling males were positively correlated with glucocorticoid levels and negatively correlated with androgens, whereas body size was positively correlated with androgens. After controlling for these variables, there was no evidence that hormone levels or behavior differed in choruses of green treefrogs in the presence and absence of Cuban treefrogs. Together, our results suggest that interactions among male green treefrogs modulate hormone levels but that the presence of Cuban treefrogs, calling or not, is not altering levels of glucocorticoids or androgens in breeding male green treefrogs.

Revealing mechanisms of mating plug function under sexual selection

Mating plugs are produced by many sexually reproducing animals and are hypothesized to promote male fertilization success under promiscuous mating. However, tests of this hypothesis have been constrained by an inability to discriminate ejaculates of different males in direct competition. Here, we use stable isotope labeling in vivo and proteomics to achieve this in a promiscuous rodent, Myodes glareolus We show that, although the first male's plug is usually dislodged, it can be retained throughout the second male's copulation. Retained plugs did not completely block rival sperm but did significantly limit their numbers. Differences in the number of each male's sperm progressing through the female reproductive tract were also explained by natural variation in the size of mating plugs and reproductive accessory glands from which major plug proteins originate. Relative sperm numbers in turn predicted the relative fertilization success of rival males. Our application of stable isotopes to label ejaculates resolves a longstanding debate by revealing how rodent mating plugs promote fertilization success under competitive conditions. This approach opens new opportunities to reveal cryptic mechanisms of postcopulatory sexual selection among diverse animal taxa.

How sperm competition shapes the evolution of testes and sperm: a meta-analysis.

Females of many species mate with multiple males, thereby inciting competition among ejaculates from rival males for fertilization. In response to increasing sperm competition, males are predicted to enhance their investment in sperm production. This prediction is so widespread that testes size (correcting for body size) is commonly used as a proxy of sperm competition, even in the absence of any other information about a species' reproductive behaviour. By contrast, a debate about whether sperm competition selects for smaller or larger sperm has persisted for nearly three decades, with empirical studies demonstrating every possible response. Here, we synthesize nearly 40 years of sperm competition research in a meta-analytical framework to determine how the evolution of sperm number (i.e. testes size) and sperm size (i.e. sperm head, midpiece, flagellum and total length) is influenced by varying levels of sperm competition across species. Our findings support the long-held assumption that higher levels of sperm competition are associated with relatively larger testes. We also find clear evidence that sperm competition is associated with increases in all components of sperm length. We discuss these results in the context of different theoretical predictions and general patterns in the breeding biology and selective environment of sperm. This article is part of the theme issue 'Fifty years of sperm competition'.

Of mice and women: advances in mammalian sperm competition with a focus on the female perspective.

Although initially lagging behind discoveries being made in other taxa, mammalian sperm competition is now a productive and advancing field of research. Sperm competition in mammals is not merely a 'sprint-race' between the gametes of rival males, but rather a race over hurdles; those hurdles being the anatomical and physiological barriers provided by the female reproductive tract, as well as the egg and its vestments. With this in mind, in this review, I discuss progress in the field while focusing on the female perspective. I highlight ways by which sperm competition can have positive effects on female reproductive success and discuss how competitive outcomes are not only owing to dynamics between the ejaculates of rival males, but also attributable to mechanisms by which female mammals bias paternity toward favourable sires. Drawing on examples across different species-from mice to humans-I provide an overview of the accumulated evidence which firmly establishes that sperm competition is a key selective force in the evolution of male traits and detail how females can respond to increased sperm competitiveness with increased egg resistance to fertilization. I also discuss evidence for facultative responses to the sperm competition environment observed within mammal species. Overall, this review identifies shortcomings in our understanding of the specific mechanisms by which female mammals 'select' sperm. More generally, this review demonstrates how, moving forward, mammals will continue to be effective animal models for studying both evolutionary and facultative responses to sperm competition. This article is part of the theme issue 'Fifty years of sperm competition'.

Illuminating the incredible journey of pollen

Illuminating the incredible journey of pollen

The effect of social odour context on the amount of time male meadow voles, Microtus pennsylvanicus, self-groom

Abstract Communicational behaviours by individuals provide information for not only the intended target(s) of the signal but any non-target individual(s) that may be nearby. For terrestrial mammals a major form of communication and social information is through odours via scent marking and self-grooming. Self-grooming is a ubiquitous behaviour in mammals with the function thought to primarily be centred on personal care. But it has been found in rodents that self-grooming will occur in the presence of social odours thus potentially serving a communicative role. For example, male meadow voles (Microtus pennsylvanicus) self-groom in the presence of a female conspecific odour but not a male conspecific odour. Most studies examining self-grooming as a form of olfactory communication have used single odour donors but in a natural environment individuals will come across complex social odour situations. Therefore, we examined how male meadow voles respond to complex social odours with regards to their self-grooming behaviour. We tested the hypothesis that self-grooming can act as a form of olfactory communication and that male meadow voles will control this behaviour measured by differences in self-grooming rates based on social contexts. Male meadow voles did not show differences in the amount of time spent self-grooming to social odours that contained a female and varying number of rival males (0, 1, 3, or 5) or if the social odour contained an acquainted or novel male. Male meadow voles did self-groom more to a social odour that contained a female and a younger male compared to when the social odour contained a female and older male. Male meadow voles appear to adjust their self-grooming behaviour based on the context of the social information. This may be a strategy that can maximize that individual’s fitness by adjusting how much information is provided to potential rivals and mates.

Plastic male mating behavior evolves in response to the competitive environment.

Male reproductive phenotypes can evolve in response to the social and sexual environment. The expression of many such phenotypes may also be plastic within an individual's lifetime. For example, male Drosophila melanogaster show significantly extended mating duration following a period of exposure to conspecific male rivals. The costs and benefits of reproductive investment, and plasticity itself, can be shaped by the prevailing sociosexual environment and by resource availability. We investigated these ideas using experimental evolution lines of D. melanogaster evolving under three fixed sex ratios (high, medium, and low male-male competition) on either rich or poor adult diets. We found that males evolving in high-competition environments evolved longer mating durations overall. In addition, these males expressed a novel type of plastic behavioral response following exposure to rival males: they both significantly reduced and showed altered courtship delivery, and exhibited significantly longer mating latencies. Plasticity in male mating duration in response to rivals was maintained in all of the lines, suggesting that the costs of plasticity were minimal. None of the evolutionary responses tested were consistently affected by dietary resource regimes. Collectively, the results show that fixed behavioral changes and new augmentations to the repertoire of reproductive behaviors can evolve rapidly.

Females of the red damselfly Mnesarete pudica are attracted to more ornamented males and attract rival males

Male calopterygid damselflies often exhibit colourful wings used during aggressive contests and courtship displays. Evidence suggests that male wing coloration is a secondary sexual character assessed by males and females to identify male quality. In some species, males adopt a lekking strategy, where females visit exhibition arenas and choose the best mate. Here, we addressed whether the behaviour of Mnesarete pudica males is influenced by female visitation when gathering in leks. We hypothesized that female visitation would increase male investment in courtship and fighting, while reducing patrolling flights and harassment attempts. Moreover, we tested the hypothesis that more ornamented males attract more females to the territory, following the hotshot model of lek evolution. Our results suggest that, indeed, males with more pigmented wings attract more visiting females, independently of male size. Our results also show that the number of females in a territory attracts more males and elicits male contest behaviour, reducing male harassment. We conclude that male ornament and male clustering is a good predictor of female visitation rates, suggesting that females may exert mate choice.

Cost of an elaborate trait: a trade-off between attracting females and maintaining a clean ornament

AbstractMany sexually selected ornaments and weapons are elaborations of an animal’s outer body surface, including long feathers, colorful skin, and rigid outgrowths. The time and energy required to keep these traits clean, attractive, and in good condition for signaling may represent an important but understudied cost of bearing a sexually selected trait. Male fiddler crabs possess an enlarged and brightly colored claw that is used both as a weapon to fight with rival males and also as an ornament to court females. Here, we demonstrate that males benefit from grooming because females prefer males with clean claws over dirty claws but also that the time spent grooming detracts from the amount of time available for courting females. Males, therefore, face a temporal trade-off between attracting the attention of females and maintaining a clean claw. Our study provides rare evidence of the importance of grooming for mediating sexual interactions in an invertebrate, indicating that sexual selection has likely shaped the evolution of self-maintenance behaviors across a broad range of taxa.

Drosophila seminal sex peptide associates with rival as well as own sperm, providing SP function in polyandrous females.

When females mate with more than one male, the males' paternity share is affected by biases in sperm use. These competitive interactions occur while female and male molecules and cells work interdependently to optimize fertility, including modifying the female's physiology through interactions with male seminal fluid proteins (SFPs). Some modifications persist, indirectly benefiting later males. Indeed, rival males tailor their ejaculates accordingly. Here, we show that SFPs from one male can directly benefit a rival's sperm. We report that Sex Peptide (SP) that a female Drosophila receives from a male can bind sperm that she had stored from a previous male, and rescue the sperm utilization and fertility defects of an SP-deficient first-male. Other seminal proteins received in the first mating 'primed' the sperm (or the female) for this binding. Thus, SP from one male can directly benefit another, making SP a key molecule in inter-ejaculate interaction.

Rival assessment by territorial southern white rhinoceros males via eavesdropping on the contact and courtship calls

Eavesdropping on vocal signals allows animals to gather information about conspecifics. For males, eavesdropping can be a low-risk method for determining the dominance status (e.g. territorial or subordinate) and motivation (e.g. mate seeking) of rivals. Adult southern white rhino males, Ceratotherium simum, are territorial and, in addition to other vocalizations, use contact and courtship calls when communicating with females. Although male territories are exclusive, the owners may tolerate up to three resident subordinate males. However, rival males sometimes intrude. Moreover, these intrusions may lead to rivals interacting with females. We investigated whether territorial males eavesdrop on vocal signals directed towards females by intruding males to determine their dominance status (territorial or subordinate) and motivation (contact calling an anoestrous female or approaching a female in oestrus during courtship). To do this, we first recorded and analysed contact and courtship calls of adult southern white rhino males and determined that these calls signal the males' dominance status and motivation. Playback trials revealed that territorial males differentiated between the calls of subordinate and other territorial males, showing a shorter latency to approach and longer searching behaviour (i.e. walking and running) after the playback of a subordinate's call. The reason for this response could be that the intruding subordinate male might be looking to challenge the territorial male for his territory. However, subordinates probably pose the lowest risk to the resident male in terms of fighting ability. In contrast, the reactions of the territorial males to the calls of other territorial males suggest that the presence and not the motivation of an intruding male was the most important factor influencing the male's reaction. We conclude that territorial males eavesdrop on the acoustic signals of trespassing males to gather information about these rivals, which can help them to better defend their territory.

Social environment modulates investment in sex trait versus lifespan: red deer produce bigger antlers when facing more rivalry

Theory predicts that the plastic expression of sex-traits should be modulated not only by their production costs but also by the benefits derived from the presence of rivals and mates, yet there is a paucity of evidence for an adaptive response of sex-trait expression to social environment. We studied antler size, a costly and plastic sex trait, and tooth wear, a trait related to food intake and longevity, in over 4,000 male Iberian red deer (Cervus elaphus hispanicus) from 56 wild populations characterized by two contrasting management practices that affect male age structure and adult sex-ratio. As a consequence, these populations exhibit high and low levels of male-male competition for mating opportunities. We hypothesized that males under conditions of low intra-sexual competition would develop smaller antlers, after controlling for body size and age, than males under conditions of high intra-sexual competition, thus reducing energy demands (i.e. reducing intake and food comminution), and as a consequence, leading to less tooth wear and a concomitant longer potential lifespan. Our results supported these predictions. To reject possible uncontrolled factors that may have occurred in the wild populations, we carried out an experimental design on red deer in captivity, placing males in separate plots with females or with rival males during the period of antler growth. Males living with rivals grew larger antlers than males living in a female environment, which corroborates the results found in the wild populations. As far as we know, these results show, for the first time, the modulation of a sexual trait and its costs on longevity conditional upon the level of intra-sexual competition.

Testosterone and the dark ventral patch of male red deer: the role of the social environment.

The expression of male sexual traits, which is stimulated by testosterone, entails significant costs for individuals. Consequently, natural selection is expected to favour the modulation of sexual trait development according to the balance between its costs and benefits. The proportion of rivals in a population may affect this balance by increasing or decreasing the reproductive benefits associated with the development of sex traits. Here, we explore the relationship between testosterone level and sex trait size under two populational conditions of mate competition: fenced (i.e. high male-male competition; all male age groups are present) and unfenced (i.e. low competition; most males present are juveniles). Our model species is the Iberian red deer (Cervus elaphus hispanicus), and the sex trait is the dark ventral patch that males exhibit during the rutting season. Our results showed that the positive relationship between testosterone levels and the size of the dark ventral patch depends on the environmental level of male-male competition. Only in populations where the operational sex ratio was high (i.e. high proportion of rival males), individuals with high levels of testosterone developed the sex trait. Conversely, when mate competition was low, there was no significant relationship between testosterone level and trait size. This result reinforces the idea that the effect of testosterone in promoting the development of sex traits may be mediated by the intensity of mate competition in the population, as well as the role of sexual selection in the evolution of the dark ventral patch in red deer.

Dominance status and copulatory vocalizations among male stump-tailed macaques in Thailand

Male copulation calls sometimes play important roles in sexual strategies, attracting conspecific females or advertising their social status to conspecific males. These calls generally occur in sexually competitive societies such as harem groups and multi-male and multi-female societies. However, the call functions remain unclear because of limited availability of data sets that include a large number of male and female animals in naturalistic environments, particularly in primates. Here, we examined the possible function of male-specific copulation calls in wild stump-tailed macaques (Macaca arctoides) by analyzing the contexts and acoustic features of vocalizations. We observed 395 wild stump-tailed macaques inhabiting the Khao Krapuk Khao Taomor Non-Hunting Area in Thailand and recorded all occurrences of observed copulations. We counted 446 male-specific calls in 383 copulations recorded, and measured their acoustic characteristics. Data were categorized into three groups depending on their social status: dominant (alpha and coalition) males and non-dominant males. When comparing male status, alpha males most frequently produced copulation calls at ejaculation, coalition males produced less frequent calls than alpha males, and other non-dominant males rarely vocalized, maintaining silence even when mounting females. Acoustic analysis indicated no significant influence of status (alpha or coalition) on call number, bout duration, or further formant dispersion parameters. Our results suggest that male copulation calls of this species are social status-dependent signals. Furthermore, dominant males might actively transmit their social status and copulations to other male rivals to impede their challenging attacks, while other non-dominant males maintain silence to prevent the interference of dominants.

Males optimally balance selfish and kin-selected strategies of sexual competition in the guppy.

Resolving the strategies by which organisms compete for limited resources is key to understanding behavioural and social evolution. When competing for matings, males in many species allocate mating effort preferentially towards higher-quality females. How males balance this against avoiding competition with rival males, who should also prefer high-quality females, is poorly understood. Kin selection theory further complicates these dynamics: males should avoid competition with close relatives especially because of added, indirect fitness costs. However, whether between-male relatedness modulates the intensity of intrasexual competition is equivocal. Here, we develop and test an analytical model describing how males should optimally allocate their mating efforts in response to information about differences in female quality, competitor presence/absence and competitor relatedness. Using freely interacting groups of Trinidadian guppies (Poecilia reticulata), we show concordance between observed and predicted mating effort allocation across all combinations of these factors. Thus, male mating effort is sensitive to variation in female quality, competitor presence and competitor relatedness, which is consistent with a kin-selected strategy of male-male competition. The fit of our model's predictions demonstrates that males integrate assessments of female quality and competitive context in a quantitatively meaningful way, implicating a competitive strategy that has been fine-tuned to maximize inclusive fitness gains.

Older males are more competitive in male fights and more aggressive toward females in the broad-horned flour beetle Gnatocerus cornutus

In theory, a male should change the allocation of fighting and mating efforts in relation to his age. Thus, the consequences of sexual selection may be complicated by changes in the male resource allocation due to aging. However, previous studies have focused on changes in female mate choice and male-male competition with aging separately, and the impact of aging on the relationship between mate choice and male competition is unknown. Here, we examined how male competitiveness and attractiveness and their relationship changes over male lifespan in Gnatocerus cornutus. In this species, males perform courtship displays and fight rival males for mates. Older males are more competitive in male fighting and aggressive toward females than younger males. The aggression is also directed toward females. Almost all older males who attacked a female failed to copulate, while younger males never attacked the females. As a result, copulation success decreased with age. When an older male did not mistake a female for a male, he exhibited more frequent courtship. However, mating with older males imposed direct costs on females in terms of both fecundity and lifespan, with no offsetting indirect benefits for her offspring. The courtship behavior of older males does not supply females with cues for mate-choice benefits but are used to coerce females into mating. Our results suggest that male–male competition constrains female preference for older males. Thus, female choice and male–male competition may not be reinforcing in older G. cornutus males. When males get older, they often pay more attention to females in a variety of ways, such as courting and fighting for access. This is because older males have not long to live. In Gnatocerus cornutus as well, older males attend to fighting and courting. The older males seem to be competitive in male fights and attractive to females. However, they are not only aggressive toward rival males but also sometimes use violence on females. As a result, these older males are rejected by the assaulted females and cannot mate. Additionally, the violence of older males can reduce female fecundity and lifespan. Thus, mating with older males is costly to females in G. cornutus, and a female preference for older males is not expected to evolve.