Reproductive Competition Research Articles

Geographic variation of reproductive traits and competition for pollinators in a bird-pollinated plant.

Geographic variation in the reproductive traits of animal‐pollinated plants can be shaped by spatially variable selection imposed by differences in the local pollination environment. We investigated this process in Babiana ringens (Iridaceae), an enigmatic species from the Western Cape region of South Africa. B. ringens has evolved a specialized perch facilitating cross‐pollination by sunbirds and displays striking geographic variation in perch size and floral traits. Here, we investigate whether this variation can be explained by geographic differences in the pollinator communities. We measured floral and inflorescence traits, and abiotic variables (N, P, C, and rainfall) and made observations of sunbirds in populations spanning the range of B. ringens. In each population, we recorded sunbird species identity and measured visitation rates, interfloral pollen transfer, and whether the seed set of flowers was pollen limited. To evaluate whether competition from co‐occurring sunbird‐pollinated species might reduce visitation, we quantified nectar rewards in B. ringens and of other co‐flowering bird‐pollinated species in local communities in which populations occurred. Variation in abiotic variables was not associated with geographical variation of traits in B. ringens. Malachite sunbirds were the dominant visitor (97% of visits) and populations with larger‐sized traits exhibited higher visitation rates, more between‐flower pollen transfer and set more seed. No sunbirds were observed in four populations, all with smaller‐sized traits. Sunbird visitation to B. ringens was not associated with local sunbird activity in communities, but sunbird visitation was negatively associated with the amount of B. ringens sugar relative to the availability of alternative nectar sources. Our study provides evidence that B. ringens populations with larger floral traits are visited more frequently by sunbirds, and we propose that visitation rates to B. ringens may be influenced, in part, by competition with other sunbird‐pollinated species.

The Young Male Syndrome-An Analysis of Sex, Age, Risk Taking and Mortality in Patients With Severe Traumatic Brain Injuries.

Higher risk taking is particularly characteristic for males between 15 and 35 years, the age when intrasexual competition is the strongest. This fitness-maximizing strategy, however, also has negative consequences; previous data revealed that males have a significantly higher tendency to die in accidents. This retrospective study aimed to assess whether age-related risk taking, often associated with the reproductive competition between males, and referred to as the Young Male Syndrome (YMS), may play a role in the high incidence of severe traumatic brain injury (sTBI) in young males. Derived from the available evidence and the main assumptions of the YMS, we expected that men, especially when they are in the age when their reproductive potential peaks, are more likely to suffer sTBI from highly risky behaviors that also lead to higher mortality. It was also expected that alcohol intoxication makes the demographic pattern of sTBI even more similar to what previous research on the YMS implies. We analyzed demographic data of patients with sTBI (N = 365) registered in a clinical database. To this end, we built Generalized Linear Mixed Models (GLMM) to reveal which of the demographic characteristics are the best predictors for risky behaviors leading to sTBI and death as a consequence of the injury. The data suggest that younger people acquired sTBI from riskier behaviors compared to members of older age groups, irrespective of their sex. Moreover, being male and being alcohol intoxicated also contributed significantly to risk-taking behavior. Mortality rate after the injury, however, increased with the age of the patient and did not depend on the riskiness of the behavior. The results indicate that the demographic distribution of the specific patient population in our focus cannot be simply explained by the YMS. However, higher incidence rates of males among the patients are in line with the core assumptions of the YMS. These data indicate that epidemiological studies should also take into consideration evolutionary theories and highlight the importance of age and sex specific prevention strategies.

Plasticity of Mating Duration in Response to Slightly Biased Operational Sex Ratios in the Water Strider (Aquarius remigis): The Effect of Cohabitation Under Standard Laboratory Conditions

In polygynandrous species, males face the trade-off between the pursuit of increased mating opportunities and securing paternity. Within such systems, males need to accurately assess the social composition of the local environment to maximize fitness. Here, we investigated this capability in the water strider (Aquarius remigis), a semi-aquatic insect known to exhibit a broad spectrum of mating behaviors and inhabit a socially diverse and changing environment. Using a combination of methodological designs to track both within- and between-subject effects, individuals remained in same-sex housing prior to being exposed to slightly biased operational sex ratios (2:1 vs. 1:2) with or without prior cohabitation to determine the effects on mating duration. Results show that males were sensitive to these subtle differences in social conditions, mating for longer periods within male-biased environments, but this was true only under conditions with prior cohabitation. In particular, when individuals could acclimate to the testing environment, mating duration dropped precipitously in female-biased conditions. These findings do not support the view that male water striders have consistent behavioral syndromes, and instead show that individuals are able to differentiate between, and adaptively respond to, small changes in the local sex ratio. In addition to improving our understanding of the plasticity of male mating behavior in this species, this study offers new insights for future laboratory research studying reproductive competition across a diverse range of polygynandrous animals.

Social Cues of Future Sperm Competition Received during Development Affect Learning in Adult Male Fruit Flies, Drosophila melanogaster

The social environment provides males with information about the likelihood of reproductive competition. However, social context can be highly variable, and males must track their environment in order to alter reproductive investment appropriately. In addition to using information gained as adults to adjust reproductive strategies, males can use cues in early life to anticipate future mating competition and alter development of reproductive tissue. As responding to variable levels of competition may be cognitively challenging, and early life environments could influence neural development, cues of future competition during development could influence adult cognitive capacity. Male Drosophila melanogaster fruit flies reared with cues of future reproductive competition, high larval density or in the presence of adult males, develop larger accessory glands. We examined whether these early life conditions affect adult male learning ability. We assessed the learning ability of adults reared under different larval social conditions in a non-sexual and sexual context. We also measured gene expression in learning, memory and synapse-related genes previously found to respond to the adult social environment. The presence of adult males during development had no effect. Males from low larval densities, however, had better learning ability in the sexual-context assay and showed relatively higher gene expression compared to flies from high larval densities. This could suggest a trade-off between reproductive investment into accessory gland growth or an increased investment into neural plasticity at low density.

Oestrous females avoid mating in front of adult male bystanders in wild chacma baboons.

In social species, female mating strategies can be constrained by both male and female groupmates through sexual conflict and reproductive competition, respectively. This study tests if females adjust their sexual behaviour according to the presence of male and female bystanders in wild chacma baboons (Papio ursinus) and assesses their relative importance. Our results show that oestrous females initiate fewer copulations in the presence of adult male bystanders, irrespective of whether they are mate-guarded or not. This inhibitory effect probably reflects a response to indirect sexual coercion by males, whose close proximity may dissuade females to initiate copulations with rival males to avoid punishment and/or aggressive mating interference. By contrast, females initiate more matings with their mate-guard in the presence of higher-ranking female bystanders, which may reflect an attempt to secure bodyguard services from their mate when they feel threatened. These results emphasize the importance of intra- and intersexual conflicts in shaping female sexual behaviour in this promiscuous society.

Reproductive control via the threat of eviction in the clown anemonefish.

In social groups, high reproductive skew is predicted to arise when the reproductive output of a group is limited, and dominant individuals can suppress subordinate reproductive efforts. Reproductive suppression is often assumed to occur via overt aggression or the threat of eviction. It is unclear, however, whether the threat of eviction alone is sufficient to induce reproductive restraint by subordinates. Here, we test two assumptions of the restraint model of reproductive skew by investigating whether resource limitation generates reproductive competition and whether the threat of eviction leads to reproductive restraint in the clown anemonefish Amphiprion percula First, we use a feeding experiment to test whether reproduction is resource limited, which would create an incentive for the dominant pair to suppress subordinate reproduction. We show that the number of eggs laid increased in the population over the study period, but the per cent increase in fed groups was more than twice that in unfed groups (205% and 78%, respectively). Second, we use an eviction experiment to test whether the dominant pair evicts mature subordinates, which would create an incentive for the subordinates to forgo reproduction. We show that mature subordinates are seven times more likely to be evicted than immature subordinates of the same size. In summary, we provide experimental support for the assumptions of the restraint model by showing that resource limitation creates reproductive competition and a credible threat of eviction helps explain why subordinates forego reproduction. Transactional models of reproductive skew may apply well to this and other simple systems.

Toward Implementation of Mosquito Sterile Insect Technique: The Effect of Storage Conditions on Survival of Male Aedes aegypti Mosquitoes (Diptera: Culicidae) During Transport.

Sterile insect technique (SIT) is a promising, environmentally friendly alternative to the use of pesticides for insect pest control. However, implementing SIT with Aedes aegypti (Linnaeus) mosquitoes presents unique challenges. For example, during transport from the rearing facility to the release site and during the actual release in the field, damage to male mosquitoes should be minimized to preserve their reproductive competitiveness. The short flight range of male Ae. aegypti requires elaborate release strategies such as release via Unmanned Aircraft Systems, more commonly referred to as drones. Two key parameters during transport and release are storage temperature and compaction rate. We performed a set of laboratory experiments to identify the optimal temperatures and compaction rates for storage and transport of male Ae. aegypti. We then conducted shipping experiments to test our laboratory-derived results in a ‘real-life’ setting. The laboratory results indicate that male Ae. aegypti can survive at a broad range of storage temperatures ranging from 7 to 28°C, but storage time should not exceed 24 h. Male survival was high at all compaction rates we tested with a low at 40 males/cm3. Interestingly, results from our ‘real-life’ shipping experiment showed that high compaction rates were beneficial to survival. This study advances key understudied aspects of the practicalities of moving lab-reared insects into the field and lies the foundation for further studies on the effect of transport conditions on male reproductive fitness.

More than kin: subordinates foster strong bonds with relatives and potential mates in a social bird

Social interactions shape relationships between individuals in complex societies. Affiliative interactions are associated with benefits and strengthen social bonds, while aggressive interactions are costly and negatively affect social bonds. Individuals may attempt to reduce aggressive encounters through submissive displays directed at higher-ranking individuals. Thus, fine-scale patterns of affilia-tive, aggressive, and submissive interactions may reflect costly and beneficial social relationships within groups, providing insight into the benefits of group living and the mechanisms of conflict resolution. So far, however, most studies have looked at social interactions and benefits of group living in isolation. We investigated how the strength of social bonds (affiliative vs. aggressive interactions) and submissive displays varied with kin-selected and potential mating benefits, and with reproductive conflict in the cooperatively breeding purple-crowned fairy-wren, Malurus coronatus. Our results revealed that subordinates formed equally strong social bonds with kin and potential mates (unrelated opposite-sex individuals) while they formed antagonistic relationships with reproductive competitors that offered no kin-selected or mating benefits (unrelated same-sex individuals). Submissive displays were directed exclusively at same-sex breeders, regardless of relatedness. Affiliation and submission were associated with reduced foraging time when food was limited, indicating a cost to maintaining positive relationships. Together, our results suggest that the strength of social bonds is determined by (potential) benefits obtained from group members, while submission likely serves to reduce conflict. Our findings highlight the importance of time-costly social interactions for maintaining relationships with group members, providing insight into how social groups of individuals with (partly) divergent interests can remain stable.

A competitive environment influences sperm production, but not testes tissue composition, in house mice.

Due to the physiological cost of sperm production, males are expected to be prudent in their expenditure and adjust their investment according to current social conditions. Strategic adjustments in sperm expenditure during development can be made via changes in testes size, sperm production rates or testes tissue composition. Here, using house mice, we test the hypothesis that elevated sperm production is driven by a plastic response in the spatial organization of the testes. We reared males under different social conditions (competitive vs. noncompetitive) and quantified sperm number and the proportion of sperm-producing tissue within the testes. Further, because sperm quality is a critical determinant of competitive fertilization success, we used computer-assisted sperm analysis to quantify six sperm motility traits. Our investigation revealed that males reared in an environment with a perceived risk of reproductive competition produced more sperm in the absence of changes in testes morphology. We discuss this result in relation to fixed and flexible phenotypically plastic responses to future competitive conditions, and conclude that adaptive adjustments in sperm number in response to the social environment are likely attributable to variation in sperm production rate. Further, we found no difference in invitro sperm motility parameters among males from the different social environment regimes. Overall, this investigation improves our understanding of the mechanisms of male plasticresponses to reproductive competition experienced during sexual development.

Group size, but not manipulated whole-clutch egg color, contributes to ovicide in joint-nesting Smooth-billed Anis

Reproductive competition in the form of ovicide is common in some joint-nesting birds, species in which multiple females lay eggs in a single nest. Joint-nesting Smooth-billed Anis (Crotophaga ani) often bury eggs under a new nest floor prior to laying their own eggs. Anis apparently cannot recognize their own eggs, which raises the question of how individuals can minimize their loss of young due to egg burial or consequences of hatching asynchrony. Newly laid eggs are coated with a white layer of vaterite (calcium) while older eggs may be almost entirely blue. Leaving older, bluer eggs in the nest presumably leads to a more competitive nest environment for the female's own young because newer eggs hatch later, producing smaller chicks at risk of getting trampled or bumped out of the nest. We hypothesized that Smooth-billed Anis use egg color as a cue for egg age. We predicted females not yet laying would bury older-looking blue eggs and tested this by removing the vaterite layer from all eggs in selected nests. Contrary to our prediction, altering egg color of whole clutches to make them look bluer, and thus older, did not trigger egg burial. The number of eggs buried increased with increasing female group size, however, consistent with previous work on this species.

Developmental and social constraints on early reproduction in an asocial ground squirrel

AbstractFor short‐lived species, selection for early reproduction should be strong, yet females often delay their first reproductive bout. Delay in age of first reproduction due to developmental constraints, such as food availability, or social constraints, such as the inhibitory presence of breeding adults, has been documented for social mammals, but effects on asocial species are less well known. We evaluated the influence of developmental and social factors on early reproduction in a short‐lived, asocial species, the golden‐mantled ground squirrel (Callospermophilus lateralis). We found that females who reproduced as yearlings had been weaned earlier in their natal summer and experienced early snow melt during their yearling spring, suggesting the importance of access to high‐quality food at critical stages. Females were more likely to reproduce as yearlings when there were more adult males present during the breeding season, possibly because exposure to males accelerates reproductive maturity. Maternal presence had no effect on yearling reproduction, but yearlings with a littermate sister present were only 22% as likely to reproduce as females without a sister present, suggesting the effect of sibling competition well past weaning. Furthermore, the negative effect of a sister's presence, but not the presence of other females, suggests that relatedness affects reproductive competition in this asocial species.

Sex differences in the drivers of reproductive skew in a cooperative breeder

Many cooperatively breeding societies are characterized by high reproductive skew, such that some socially dominant individuals breed, while socially subordinate individuals provide help. Inbreeding avoidance serves as a source of reproductive skew in many high-skew societies, but few empirical studies have examined sources of skew operating alongside inbreeding avoidance or compared individual attempts to reproduce (reproductive competition) with individual reproductive success. Here, we use long-term genetic and observational data to examine factors affecting reproductive skew in the high-skew cooperatively breeding southern pied babbler (Turdoides bicolor). When subordinates can breed, skew remains high, suggesting factors additional to inbreeding avoidance drive skew. Subordinate females are more likely to compete to breed when older or when ecological constraints on dispersal are high, but heavy subordinate females are more likely to successfully breed. Subordinate males are more likely to compete when they are older, during high ecological constraints, or when they are related to the dominant male, but only the presence of within-group unrelated subordinate females predicts subordinate male breeding success. Reproductive skew is not driven by reproductive effort, but by forces such as intrinsic physical limitations and intrasexual conflict (for females) or female mate choice, male mate-guarding and potentially reproductive restraint (for males). Ecological conditions or "outside options" affect the occurrence of reproductive conflict, supporting predictions of recent synthetic skew models. Inbreeding avoidance together with competition for access to reproduction may generate high skew in animal societies, and disparate processes may be operating to maintain male vs. female reproductive skew in the same species.

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.

Context dependence of female reproductive competition in wild chacma baboons

Recent research reveals that female reproductive competition is common and may shape the social and reproductive strategies of female mammals. This study explores the determinants and intensity of female intrasexual conflicts in a wild promiscuous primate, the chacma baboon, Papio ursinus. We tested a suite of hypotheses to assess whether female–female aggression was primarily driven by instantaneous competition for food, mates or paternal care, or aimed at reducing future competition among offspring via reproductive suppression. Behavioural data were gathered from 53 females in two groups over two contrasting 2-year periods (2005–2006, 2013–2014): the first characterized by stability in the male dominance hierarchies, the second by instability induced by several immigration events and male take-overs. In both periods, we found that sexually receptive females received high levels of aggression from other sexually receptive females, consistent with competition over mating opportunities. In the unstable period, females exchanged higher rates of aggression than in the stable period, regardless of reproductive state, but lactating females received most aggression, consistent with higher competition over social access to male partners in response to increased infanticide risk. There was no evidence that aggression between females reflected either competition over food or reproductive suppression. These findings indicate that patterns of aggression between females fluctuate with sociodemographic factors affecting sexual and social access to males and reflect reproductive competition more closely than resource competition in this promiscuous primate society.

Sexual conflict and ecology: Species composition and male density interact to reduce male mating harassment and increase female survival.

Sexual conflict is a pervasive evolutionary force that can reduce female fitness. Experimental evolution studies in the laboratory might overestimate the importance of sexual conflict because the ecological conditions in such settings typically include only a single species. Here, we experimentally manipulated conspecific male density (high or low) and species composition (sympatric or allopatric) to investigate how ecological conditions affect female survival in a sexually dimorphic insect, the banded demoiselle (Calopteryx splendens). Female survival was strongly influenced by an interaction between male density and species composition. Specifically, at low conspecific male density, female survival increased in the presence of heterospecific males (C. virgo). Behavioral mating experiments showed that interspecific interference competition reduced conspecific male mating success with large females. These findings suggest that reproductive interference competition between con- and heterospecific males might indirectly facilitate female survival by reducing mating harassment from conspecific males. Hence, interspecific competitors can show contrasting effects on the two sexes thereby influencing sexual conflict dynamics. Our results call for incorporation of more ecological realism in sexual conflict research, particularly how local community context and reproductive interference competition between heterospecific males can affect female fitness.

Skew in ovarian activation depends on domicile size in phyllode-glueing thrips

Costs and benefits of group living are a fundamental topic in behavioural ecology. Resource availability affects individuals’ breeding prospects alone and in groups, as well as how reproduction is distributed within groups (“reproductive skew”). Here, in facultatively social thrips, we provide correlational evidence that breeding resources are associated with (1) whether solitary or social living is favoured, and (2) the degree of ovarian skew. Dunatothrips aneurae (Thysanoptera, Phlaeothripidae) cooperatively build silk “domiciles” on Australian Acacias, feeding exclusively from internal phyllode surfaces. Per capita productivity scaled differently with group size depending on domicile volume — females in small domiciles did better alone than in groups, whereas in large domiciles single and group-nesting females did equally well. Ovarian dissections revealed that in small domiciles some females were nonreproductive, indicating ovarian (i.e. reproductive) skew. Skew increased as domicile size decreased and group size increased. Breeders had smaller oocyte volume in smaller domiciles, especially those containing nonreproductives. These findings suggest group formation and reproductive skew in D. aneurae may be influenced by reproductive competition for breeding resources. Nonreproductive females in small domiciles may be reproductively suppressed, subfertile, or accumulating resources to reproduce.

Impact of male presence on female sociality and stress endocrinology in wild house mice (Mus musculus domesticus)

In group living animals, reproductive competition plays an important role in shaping social relationships and associations among female group members. In this study, we investigated the impact of male presence on the development of female-female competition and female sociality in groups of female wild house mice, using physiological and behavioral parameters. We predicted that, by eliciting intra-sexual competition, males influence social relationships among female group members and thus affect female associations to potential cooperation partners. To test this hypothesis we compared stress hormone production, the frequency of agonistic interactions, social hierarchies and social partner preferences in groups of unrelated, unfamiliar females in the absence and presence of males. Our results revealed no indication that the introduction of males into all-female groups of wild house mice elicited increased competition among female group members, neither on the physiological nor on the behavioral level. We found no effect of male presence on female glucocorticoid secretion, aggression, dominance hierarchies or on the females' sociability. Females thus seem not to intensely compete over access to males. This female ability to behaviorally and physiologically deal with even previously unfamiliar same-sex group members may be an important feature of female house mouse societies. In fact, it could be a necessary prerequisite to establish cooperative relationships between females in the context of reproduction, such as communal nursing of young.

Should I stay or should I go? The settlement-inducing protein complex guides barnacle settlement decisions.

Reproduction in barnacles relies on chemical cues that guide their gregarious settlement. These cues have been pinned down to several sources of settlement pheromones, one of which is a protein termed settlement-inducing protein complex (SIPC), a large glycoprotein acting as a pheromone to induce larval settlement and as an adhesive in surface exploration by the cyprids. Settlement assays in laboratory conditions with Amphibalanus (=Balanus) amphitrite cyprids in the presence of SIPC showed that cyprids exhibit settlement preference behaviour at lower concentrations of SIPC [half maximal effective concentration (EC50)=3.73 nmol l-1] and settlement avoidance behaviour at higher concentrations (EC50=101 nmol l-1). By using truncated fragments of SIPC in settlement assays, we identify that domains at the N-terminus of SIPC transduce settlement preference cues that mask the settlement avoidance cues transduced by domains at its C-terminus. Removing the N-terminal 600 amino acids from SIPC resulted in truncated fragments that transduced only settlement avoidance cues to the cyprids. From the sexual reproduction point of view, this bimodal response of barnacles to SIPC suggests that barnacles will settle gregariously when conspecific cues are sparse but will not settle if conspecific cues inform of overcrowding that will increase reproductive competition and diminish their reproductive chances.

Paternity and kin structure among neighbouring groups in wild bonobos at Wamba.

Although both bonobos and chimpanzees are male-philopatric species, outcomes of male–male reproductive competition seem to be more closely associated with mating success in chimpanzees. This suggests that the extent of male reproductive skew is lower in bonobos. In addition, between-group male–male reproductive competition is more lethal in chimpanzees. This suggests that between-group differentiation in male kinship is lower in bonobos. We analysed the paternity of 17 offspring in two bonobo groups and estimated the relatedness of individuals among three neighbouring groups by using DNA extracted from non-invasive samples at Wamba, in the Democratic Republic of the Congo. The alpha males sired at least nine of 17 offspring. This supports a previous finding that the male reproductive skew is higher in bonobos than that in chimpanzees. Average relatedness among males within groups was significantly higher than that among males across groups, whereas there was no significant difference among females between within and across groups. These results are consistent with male philopatry, highly skewed reproductive success of males and female dispersal. Higher average relatedness among males within groups suggest that the differences in hostility towards males of different groups between bonobos and chimpanzees may be explained by factors other than kinship.

Effects of female reproductive competition on birth rate and reproductive scheduling in a historical human population

Personality affects response to alarm calls. This study reveals that boldness explains how vigilant chipmunks behave in response to alarm calls, and that vigilance diminishes in response to shyer callers. Chipmunks thus evaluate the personality of callers and discount the danger associated with calls from highly risk-sensitive individuals. Adjusting responsiveness relative to caller reliability improves foraging while reducing the risk of predation.