It takes two: Seasonal variation in sexually dimorphic weaponry results from divergent changes in males and females

Sexually dimorphic weaponry often results from intrasexual selection, and weapon size can vary seasonally when costs of bearing the weapon exceed the benefits outside of the reproductive season. Weapons can also be favored in competition over nonreproductive resources such as food or shelter, and if such nonreproductive competition occurs year‐round, weapons may be less likely to vary seasonally. In snapping shrimp (Alpheus angulosus), both sexes have an enlarged snapping claw (a potentially deadly weapon), and males of many species have larger claws than females, although females are more aggressive. This contrasting sexual dimorphism (larger weaponry in males, higher aggression in females) raises the question of whether weaponry and aggression are favored by the same mechanisms in males and females. We used field data to determine whether either sex shows seasonal variation in claw size such as described above. We found sexual dimorphism increased during the reproductive season due to opposing changes in both male and female claw size. Males had larger claws during the reproductive season than during the nonreproductive season, a pattern consistent with sexual selection. Females, however, had larger claws during the nonreproductive season than during the reproductive season—a previously unknown pattern of variation in weapon size. The observed changes in female weapon size suggest a trade‐off between claw growth and reproduction in the reproductive season, with investment in claw growth primarily in the nonreproductive season. Sexually dimorphic weaponry in snapping shrimp, then, varies seasonally due to sex differences in seasonal patterns of investment in claw growth, suggesting claws may be advantageous for both sexes but in different contexts. Thus, understanding sexual dimorphisms through the lens of one sex yields an incomplete understanding of the factors favoring their evolution.     

Sex-specific spatio-temporal variability in reproductive success promotes the evolution of sex-biased dispersal

Inbreeding depression, asymmetries in costs or benefits of dispersal, and the mating system have been identified as potential factors underlying the evolution of sex-biased dispersal. We use individual-based simulations to explore how the mating system and demographic stochasticity influence the evolution of sex-specific dispersal in a metapopulation with females competing over breeding sites, and males over mating opportunities. Comparison of simulation results for random mating with those for a harem system (locally, a single male sires all offspring) reveal that even extreme variance in local male reproductive success (extreme male competition) does not induce male-biased dispersal. The latter evolves if the between-patch variance in reproductive success is larger for males than females. This can emerge due to demographic stochasticity if the habitat patches are small. More generally, members of a group of individuals experiencing higher spatio-temporal variance in fitness expectations may evolve to disperse with greater probability than others.     

Seasonal variation in male alternative reproductive tactics

Genetic parentage analyses reveal considerable diversity in alternative reproductive behaviours (e.g. sneaking) in many taxa. However, little is known about whether these behaviours vary seasonally and between populations. Here, we investigate seasonal variation in male reproductive behaviours in a population of two‐spotted gobies (Gobiusculus flavescens) in Norway. Male two‐spotted gobies guard nests, attract females and care for fertilized eggs. We collected clutches and nest‐guarding males early and late in the breeding season in artificial nests and used microsatellite markers to reconstruct parentage from a subset of offspring from each nest. We hypothesized that mating, reproductive success and sneaking should be more prevalent early in the breeding season when competition for mates among males is predicted to be higher. However, parentage analyses revealed similar values of mating, reproductive success and high frequencies of successful sneaking early (30% of nests) and late (27% of nests) in the season. We also found that multiple females with eggs in the same nest were fertilized by one or more sneaker males, indicating that some males in this population engage in a satellite strategy. We contrast our results to previous work that demonstrates low levels of cuckoldry in a population in Sweden. Our results demonstrate marked stability in both the genetic mating system and male alternative reproductive tactics over the breeding season. However, sneaking rates may vary geographically within a species, likely due to local selection influencing ecological factors encountered at different locations.     

Mate and territory availability affect breeding dispersal and divorce in a resident Southern House Wren Troglodytes aedon musculus population

Breeding dispersal is the movement of an individual between breeding attempts and is usually associated with the disruption of the social pair bond, although mates may disperse together as a social unit. In monogamous territorial species, the decision to disperse may be affected by individual attributes such as sex, age and condition of the disperser. However, environmental and social contexts may also play a crucial role in the decision to disperse. We analysed capture‐resighting data collected over 9 years to study breeding dispersal and divorce rates of a Southern House Wren Troglodytes aedon musculus population in South Temperate Argentina. Between‐season dispersal was more frequent than within‐season dispersal, with females dispersing more often than males, both between and within seasons. Both within‐season and between‐season breeding dispersal probability was affected by territory availability, but not by previous breeding success. When the adult sex ratio (ASR) was more skewed towards males, male between‐season dispersal was also affected by mating status, with widowed and single males dispersing more often than paired males. Within‐season divorce increased the reproductive success of females but not males, and was affected by the availability of social partners (with increasingly male‐skewed ASR). Our results suggest that territorial vacancies and mating opportunities affect dispersal and divorce rates in resident Southern House Wrens, highlighting the importance of social and environmental contexts for dispersal behaviour and the stability of social pair bonds.     

Male competition and its hormonal correlates in Assamese macaques (Macaca assamensis)

In polygynous mammals, where males compete over access to females, the potential of males to monopolize reproductive females largely depends on the spatio-temporal distribution of reproductive females. We investigated mechanisms of male reproductive competition and its hormonal basis in a cercopithecine species with reduced contest potential owing to female reproductive synchrony and concealed ovulation. Over 16 months including two mating seasons we collected 1218 h of observational focal animal data and 1254 fecal samples of 11-12 adult and large subadult male Assamese macaques (Macaca assamensis) living in their natural habitat in Thailand. Androgen output along with aggressive behavior showed a seasonal pattern, with highest values being obtained by all males during the mating season and by those males experiencing acute social challenges, e.g. rank change and dispersal. Individual androgen levels and rates of attacks were linked across the study period, suggesting a promoting function of androgens for aggressive behavior. Dominance rank predicted neither mating success nor androgen levels consistently, indicating a reduced selective advantage of high social status for general mating access. However, high ranking males engaged in extended consortships with reproductive females. Distribution of consortships across males followed a priority of access distribution, with the two top ranking males accounting for 75% of consort activity, suggesting that high social status also carries fitness benefits in a species characterized by low contest potential.     

Seasonal trade-offs in cell-mediated immunosenescence in ruffs (Philomachus pugnax)

The immune system is an energetically expensive self-maintenance complex that, given the risks of parasitism, cannot be carelessly compromised. Life-history theory posits that trade-offs between fitness components, such as self-maintenance and reproduction, vary between genders and age classes depending on their expected residual lifetime reproductive success, and seasonally as energetic requirements change. Using ruff (Philomachus pugnax), a bird with two genetically distinct male morphs, we demonstrate here a decrease in male immunocompetence during the breeding season, greater variance in immune response among males than females, immunosenescence in both sexes and male morphs, and a seasonal shift in the age range required to detect senescence. Using a phytohaemagglutinin delayed hypersensitivity assay, we assessed cell-mediated immunity (CMI) of males of typical breeding age during the breeding and nonbreeding seasons, and of a larger sample that included females and birds of a greater age range during the non-breeding period. CMI was higher for breeding-aged males in May than in November, but the increase was not related to age or male morph. In November, mean CMI did not differ between the sexes, but the variance was higher for males than for females, and there were no differences in mean or variance between the two male morphs. For both sexes and male morphs, CMI was lower for young birds than for birds of typical breeding ages, and it declined again for older birds. In males, senescence was detected in the non-breeding season only when very old birds were included. These results, generally consistent with expectations from life-history theory, indicate that the immune system can be involved in multifarious trade-offs within a yearly cycle and along an individual's lifetime, and that specific predictions about means and variances in immune response should be considered in future immunoecological research.     

Seasonal sex role changes in the blenniid Petroscirtes breviceps, a nest brooder with paternal care

The plasticity of the sex roles in the blenniid fish Petroscirtes breviceps , a nest brooder with exclusive paternal care, was studied throughout an 8 month breeding season. Males performed most courtships early and late in the breeding season, whereas females performed most in the middle of the season. These results indicated that the sex of individuals initiating courtship changed seasonally, with courtship role reversal in the middle of the season. Intrasexual aggression in both sexes occurred much more frequently in mid-season than in the early and late seasons. Males frequently fought when available nest sites were limited, regardless of the presence of females, suggesting that males competed for nests in order to qualify to mate (resource competition). In contrast, courting females fought only in mid-season, when females' relative success in entering nests decreased, indicating that females competed for limited mating opportunities (mating competition). The reversed courtship roles and female mating competition in mid-season suggested that the sex roles in P. breviceps changed seasonally from the conventional roles to reversed roles and back again during one breeding season. This study provides the first empirical evidence of multiple changes in the sex roles of animals within a breeding season.     

Mechanisms and reproductive consequences of breeding dispersal in a specialist predator under temporally varying food conditions

Individual variation in breeding dispersal has extensive ecological and evolutionary consequences, but the factors driving individual dispersal behaviour and their fitness consequences remain poorly understood. Our data on dispersal events of a rodent‐specialist predator, the Eurasian kestrel Falco tinnunculus, over 20 years in western Finland offers a unique opportunity to explore the mechanisms underlying breeding dispersal behaviour and its reproductive consequences in a wild bird population. Sex, age, body condition and previous breeding success affected breeding dispersal. Dispersal distances were longer in females than in males as well as longer in yearlings than in older individuals. Body condition was positively correlated to breeding dispersal distances, particularly for females. The lowest dispersal distances were recorded for intermediate brood sizes in the year preceding dispersal. Our results highlight sex‐ and environment‐specific consequences of breeding dispersal on reproductive performance. During increase phases of the three‐year vole cycles, males dispersing further had lower reproductive performance after dispersal, whereas in females, long breeding dispersal distances were associated with increased breeding success under all environmental conditions. These results suggest benefits associated to breeding dispersal in females, potentially related to large spatio‐temporal variation in main food abundance and intensity of intra‐specific competition. Breeding dispersal of males was costly during increasing food abundance, indicating the potential fitness benefits of environmental familiarity in this migratory species. Overall, our results indicate that both individual traits and environmental factors interact to shape breeding dispersal strategies in wide‐ranging predator populations under fluctuating food conditions.     

Seasonality, sociality, and reproduction: Long-term stressors of ring-tailed lemurs (Lemur catta)

Fecal glucocorticoid (fGC) concentrations are reliable, non-invasive indices of physiological stress that provide insight into an animal's energetic and social demands. To better characterize the long-term stressors in adult members of a female-dominant, seasonally breeding species - the ring-tailed lemur (Lemur catta) - we first validated fecal samples against serum samples and then examined the relationship between fGC concentrations and seasonal, social, demographic, genetic, and reproductive variables. Between 1999 and 2006, we collected 1386 fecal samples from 32 adult, semi-free-ranging animals of both sexes. In males and non-pregnant, non-lactating females, fGC concentrations were significantly elevated during the breeding season, specifically during periods surrounding known conceptions. Moreover, group composition (e.g., multi-male versus one-male) significantly predicted the fGC concentrations of males and females in all reproductive states. In particular, the social instability introduced by intra-male competition likely created a stressor for all animals. We found no relationship, however, between fGC and the sex, age, or heterozygosity of animals. In reproducing females, fGC concentrations were significantly greater during lactation than during the pre-breeding period. During pregnancy, fGC concentrations were elevated in mid-ranking dams, relative to dominant or subordinate dams, and significantly greater during the third trimester than during the first or second trimesters. Thus, in the absence of nutritional stressors, social dominance was a relatively poor predictor of fGC in this female-dominant species. Instead, the animals were maximally challenged by their social circumstances and reproductive events—males by competition for mating opportunities and females by late-term gestation and lactation.     

Mating Group Size and Stability in Reindeer Rangifer tarandus: The Effects of Male Characteristics,Sex Ratio and Male Age Structure

In polygynous mating systems, males compete intensely for mates and may mate several females during a single reproductive season. Accordingly, factors influencing the ability of males to control a larger number of females during the breeding season can provide information on the processes underlying sexual selection. In ungulates, age, body mass and social rank are considered good predictors of the reproductive success of males, but how male age structure and sex ratio in the population influence mating group (MG) dynamics has received little empirical testing. Between 1996 and 2005, we manipulated male age‐ and sex structure and monitored MG dynamics in a reindeer (Rangifer tarandus) population. We investigated the influence of male characteristics, percentage of males and male age structure on MG size and stability. We found that males with higher social rank (that were also older and heavier) controlled larger MGs (therefore had greater mating opportunities) and had more stable MGs (corresponding to a higher ability to maintain and control females) than males of lower social rank. Moreover, MG size and MG stability decreased as the percentage of males in the population increased, most likely resulting from greater male–male competition and increased female movements. Male age structure did not influence MG stability. Given the positive relationship between mating success and MG size (and likely MG stability), frequent female movements and intense competition among males to control females seem to be the principal components of reindeer MGs dynamic.     

Circulating LH levels and the response to exogenous GnRH in the common mole-rat: implications for reproductive regulation in this social, seasonal breeding species

The effects of breeding season and reproductive status on male and female reproduction were investigated in the common mole-rat, Cryptomys hottentotus hottentotus, a cooperatively breeding rodent which exhibits a unique combination of seasonal breeding and a reproductive division of labor. Pituitary function was examined by measuring the luteinizing hormone (LH) responses to single doses of 2 microg exogenous gonadotrophin-releasing hormone (GnRH) and physiological saline in 69 males and 58 females from 35 wild caught colonies. Neither males nor females exhibited any apparent manifestation of season on basal LH concentrations or on pituitary sensitivity to stimulation by exogenous GnRH. The continuance of reproductive function during the nonbreeding period is essential in common mole-rat males and females, as this period coincides with the period of maximal dispersal opportunity in the winter rainfall area they inhabit. Normal circulating levels of reproductive hormones in dispersing animals may aid intersexual recognition, assist pairbond formation, and thus prime animals for independent reproduction. Circulating basal concentrations of LH as well as LH levels measured in response to a single exogenous GnRH challenge were not significantly different between the reproductive and non-reproductive groups of either sex, suggest the absence of a physiologically well-defined suppression of reproduction in subordinate common mole-rats.     

Reproductive ecology of the jacky dragon (Amphibolurus muricatus): an agamid lizard with temperature‐dependent sex determination

Abstract The jacky dragon, Amphibolurus muricatus (White, ex Shaw 1790) is a medium sized agamid lizard from the southeast of Australia. Laboratory incubation trials show that this species possesses temperature‐dependent sex determination. Both high and low incubation temperatures produced all female offspring, while varying proportions of males hatched at intermediate temperatures. Females may lay several clutches containing from three to nine eggs during the spring and summer. We report the first field nest temperature recordings for a squamate reptile with temperature‐dependent sex determination. Hatchling sex is determined by nest temperatures that are due to the combination of daily and seasonal weather conditions, together with maternal nest site selection. Over the prolonged egg‐laying season, mean nest temperatures steadily increase. This suggests that hatchling sex is best predicted by the date of egg laying, and that sex ratios from field nests will vary over the course of the breeding season. Lizards hatching from eggs laid in the spring (October) experience a longer growing season and should reach a larger body size by the beginning of their first reproductive season, compared to lizards from eggs laid in late summer (February). Adult male A. muricatus attain a greater maximum body size and have relatively larger heads than females, possibly as a consequence of sexual selection due to male‐male competition for territories and mates. If reproductive success in males increases with larger body size, then early hatching males may obtain a greater fitness benefit as adults, compared to males that hatch in late summer. We hypothesize that early season nests should produce male‐biased sex ratios, and that this provides an adaptive explanation for temperature‐dependent sex determination in A. muricatus.     

The sex lives of parasites: Investigating the mating system and mechanisms of sexual selection of the human pathogen Schistosoma mansoni

The mating systems of internal parasites are inherently difficult to investigate although they have important implications for the evolutionary biology of the species, disease epidemiology, and are important considerations for control measures. Using parentage analyses, three topics concerning the mating biology of Schistosoma mansoni were investigated: the number of mates per adult male and female, variance in reproductive success among individuals, and the potential role for sexual selection on male body size and also mate choice for genetically dissimilar individuals. Results indicated that schistosomes were mostly monogamous, and evidence of only one mate change occurred over a period of 5-6 weeks. One male was polygynous and contained two females in its gynecophoral canal although offspring were only detected for one of the females. Even though they were primarily monogamous and the sex ratio near even, reproductive success was highly variable, indicating a potential role for sexual selection. Male body size was positively related to reproductive success, consistent with sexual selection via male-male competition and female choice for large males. However, relatedness of pairs was not associated with their reproductive success. Finally, genetically identical individuals differed significantly in their reproductive output and identical males in their body size, indicating important partner and environmental effects on these traits.     

Mate guarding, competition and variation in size in male orb-web spiders, Metellina segmentata: a field experiment

In the common orb-web spider Metellina segmentata, males are more powerfully built with longer legs, although females are heavier because of their egg load. Males guard females before attempting to mate, and there is considerable male-male competition because of the male-biased operational sex ratio. We used a field removal experiment to examine (1) seasonal changes in the average morphology of guarding males and (2) whether there is a pool of small males that is excluded from the webs of females. Morphological measures were subjected to a principal components analysis and changes in PC scores were examined for seasonal effects and the effects of previous removal of males. The size of guarding males (PC1) increased over the season, suggesting that smaller males were increasingly excluded from webs, but the condition of guarding males (PC2) decreased, indicating that energy reserves are depleted because the males gain little access to food during the reproductive season. When guarding males were removed, smaller males were able to take up residence. Our results show that large males have a clear advantage in monopolizing females. We discuss the manner in which selection acts to maintain large male size in this spider.Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Seasonal Variation in Female Mate Choice and Operational Sex Ratio in Wild Populations of an Annual Fish,Austrolebias reicherti

The intensity of mating competition and the potential benefits for female of mating with certain males can be influenced by several extrinsic factors, such that behavioral decisions can be highly context-dependent. Short-lived species with a single reproductive season are a unique model to study context-sensitive mating decisions. Through exhaustive sampling in the field and simultaneous choice tests in the laboratory, we evaluated operational sex ratio (OSR) and female mate choice at the beginning and end of the reproductive season in the annual killifish Austrolebias reicherti. We found seasonal change in both OSR and female mate choice. At the start of the reproductive season the OSR did not deviate from parity, and females preferred larger males. Later in the reproductive season, while the proportion of males in the ponds decreased, females became unselective with respect to male size. The particular biological cycle of annual killifish, where both life expectancy and mating opportunities decline sharply over a short timescale, could account for the seasonal change in female choice. Reduction in choosiness could arise from diminished reproductive prospects due to a decline in male availability. Moreover, as the end of the season approaches, any benefits of choosiness are presumably reduced: a female’s fitness will be higher if she mates with any male than if she forgoes reproduction and dies. Future work will disentangle the mechanisms underlying seasonal changes in mating preferences, notably direct responses to demographic factors, environmental cues, or intrinsic changes during development.     

Early growth,dominance acquisition and lifetime reproductive success in male and female cooperative meerkats

In polygynous species, variance in reproductive success is higher in males than females. There is consequently stronger selection for competitive traits in males and early growth can have a greater influence on later fitness in males than in females. As yet, little is known about sex differences in the effect of early growth on subsequent breeding success in species where variance in reproductive success is higher in females than males, and competitive traits are under stronger selection in females. Greater variance in reproductive success has been documented in several singular cooperative breeders. Here, we investigated consequences of early growth for later reproductive success in wild meerkats. We found that, despite the absence of dimorphism, females who exhibited faster growth until nutritional independence were more likely to become dominant, whereas early growth did not affect dominance acquisition in males. Among those individuals who attained dominance, there was no further influence of early growth on dominance tenure or lifetime reproductive success in males or females. These findings suggest that early growth effects on competitive abilities and fitness may reflect the intensity of intrasexual competition even in sexually monomorphic species.     

Plumage redness predicts breeding onset and reproductive success in the House Finch: a validation of Darwin's theory

Darwin (1871) and later Fisher (1958) suggested that sexual selection can drive the evolution of ornamental traits in monogamous species when female preferences for these traits allow well-ornamented males to begin breeding earlier in a season and, as a result, gain reproductive advantages over poorly ornamented males. However, few studies have been conducted to test this fundamental concept upon which much of the sexual selection theory for monogamous species has been based. In this study, we examined the relationship between breeding onset, reproductive success, and male ornamentation in the House Finch Carpodacus mexicanus , a species in which males display bright carotenoid-based plumage pigmentation. In previous work, it has been shown that bright male House Finches are preferred as social mates by females and, as a result, begin nesting earlier in the season than do drab orange and yellow males. Here we show that, by initiating breeding earlier in the season, brightly colored males fledge more offspring in a season than do drab males. Thus, differential timing of breeding generates considerable variance in reproductive success among male House Finches and contributes to sexual selection for male plumage ornamentation in this species.     

The costs of risky male behaviour: sex differences in seasonal survival in a small sexually monomorphic primate

Male excess mortality is widespread among mammals and frequently interpreted as a cost of sexually selected traits that enhance male reproductive success. Sex differences in the propensity to engage in risky behaviours are often invoked to explain the sex gap in survival. Here, we aim to isolate and quantify the survival consequences of two potentially risky male behavioural strategies in a small sexually monomorphic primate, the grey mouse lemur Microcebus murinus: (i) most females hibernate during a large part of the austral winter, whereas most males remain active and (ii) during the brief annual mating season males roam widely in search of receptive females. Using a 10-year capture-mark-recapture dataset from a population of M. murinus in Kirindy Forest, western Madagascar, we statistically modelled sex-specific seasonal survival probabilities. Surprisingly, we did not find any evidence for direct survival benefits of hibernation-winter survival did not differ between males and females. By contrast, during the breeding season males survived less well than females (sex gap: 16%). Consistent with the 'risky male behaviour' hypothesis, the period for lowered male survival was restricted to the short mating season. Thus, sex differences in survival in a promiscuous mammal can be substantial even in the absence of sexual dimorphism.     

Spatial and temporal components of the mating systems of kudu bulls and red deer stags

Observations were made on greater kudu (Tragelaphus strepsiceros) in the Kruger National Park in South Africa. Data on movement patterns, courtship, dominance interactions and proportion of time spent in various activities by males during the breeding season are presented. Comparative data on the apportionment of time by red deer (Cervus elaphus) setages were obtained on the Isle of Rhum, Scotland. While spatial components of male reproductive behaviour were similar in the two species, time-investments differed markedly. Kudu bulls showed little change in time spent feeding and moving during the breeding season, did not herd females and tolerated the presence of younger males. In contrast, red deer stags almost ceased feeding and greatly increased their time spent moving and in sexual or dominance-related activities. Thus the spatial and temporal components of male mating strategies can vary independently and require separate evolutionary explanaions. Comparative data for other ungulates are sparse, but suggest that time-investments are influenced by the duration of the breeding season and the breeding sex ratio. However, kudu bulls incur high mortality costs despite their low time-investments in reproductive activities.     

Reproductive strategies of rhesus macaques

Reproductive strategies incorporate a multitude of mechanisms that have evolved to promote the reproductive success of individuals. Evolutionary perspectives tend to emphasize the advantages of male-male competition and female choice as mediators of differential reproduction. Male rhesus macaques have not been observed to fight for access to sexually receptive females, although they suffer more wounds during the mating season. An increased likelihood of attacks appears to coincide with male troop entry. Males who spend more time in consort and mate with more females tend to sire more offspring. Genetic analysis of paternity has pinpointed age and endurance rivalry, rather than agonistic competition, as key variables associated with variation in progeny production. Female rhesus macaques often copulate with multiple males during their ovulatory period, and tend to conceive on the first cycle of the mating season. Female reproductive success is more likely to be a function of offspring survivorship than the identity of particular male partners. The role of female choice as a direct mediator of male reproductive success is unresolved, but female mate selection seems to indirectly affect male reproductive success because female preference for mating with novel males seems to foster male dispersal. Evaluating whether mating preferences for particular male phenotypes affectsfemale reproductive success is a task for the future. A common denominator to the reproductive strategies of both female and male rhesus macaques is that feeding patterns affect body condition which influences reproductive output and regulates relative reproductive success.