Determinants and long‐term costs of early reproduction in males of a long‐lived polygynous mammal

In long‐lived polygynous species, male reproductive success is often monopolized by a few mature dominant individuals. Young males are generally too small to be dominant and may employ alternative tactics; however, little is known about the determinants of reproductive success for young males. Understanding the causes and consequences of variability in early reproductive success may be crucial to assess the strength of sexual selection and possible long‐term trade‐offs among life‐history traits. Selective pressures driven by fluctuating environmental conditions may depend on age class. We evaluated the determinants of reproduction in male bighorn sheep (Ovis canadensis) aged 2–4 years using 30 years of individual‐level data. These young males cannot defend estrous ewes and use alternative mating tactics. We also investigated how the age of first detected reproduction was correlated to lifetime reproductive success and longevity. We found that reproductive success of males aged 3 years was positively correlated to body mass, to the proportion of males aged 2–4 years in the competitor pool, and to the number of females available per adult male. These results suggest that reproductive success depends on both competitive ability and population age–sex structure. None of these variables, however, had significant effects on the reproductive success of males aged 2 or 4 years. Known reproduction before the age of five increased lifetime reproductive success but decreased longevity, suggesting a long‐term survival cost of early reproduction. Our analyses reveal that both individual‐level phenotypic and population‐level demographic variables influence reproductive success by young males and provide a rare assessment of fitness trade‐offs in wild polygynous males.     

Preliminary analysis of reproductive success in a large mammal with alternative mating tactics,the Northern chamois,Rupicapra rupicapra

In polygynous mating systems, reproductive skew depends on the ability of males to monopolize females, which in turn may promote the development of contrasting traits in the two sexes. Although dominant individuals normally enjoy a higher reproductive success (RS) than subordinates, the use of genetic markers has shown that behavioural observations of male mating success may not provide reliable clues of RS. We report the preliminary results of the first DNA‐based paternity analysis on the Northern chamois (Rupicapra rupicapra), a scarcely dimorphic mountain ungulate described as highly polygynous, in relation to mating tactic and age. Because of sampling difficulties, the success in parentage assignment was low, and the interpretation of results requires caution. Territorial males had a greater RS than nonterritorial ones but they were unable to monopolize mating events. Age had a weak effect on paternity outcome but only males ≥ 6 years showed siring success. Although future studies are needed to assess the opportunity for sexual selection in male chamois, the concurrence of limited sexual size dimorphism, compensatory growth, unbiased sex‐specific survival, RS of alternative mating tactics and, possibly, long breeding tenure, may hint at the adoption of a conservative mating strategy in this species.     

Alpine ibex males grow large horns at no survival cost for most of their lifetime

Large horns or antlers require a high energy allocation to produce and carry both physiological and social reproductive costs. Following the principle of energy allocation that implies trade-offs among fitness components, growing large weapons early in life should thus reduce future growth and survival. Evidence for such costs is ambiguous, however, partly because individual heterogeneity can counterbalance trade-offs. Individuals with larger horns or antlers may be of better quality and thus have a greater capacity to survive. We investigated trade-offs between male early horn growth and future horn growth, baseline mortality, onset of actuarial senescence, and rate of ageing in an Alpine ibex (Capra ibex ibex) population. Horn growth of males in early life was positively correlated to their horn length throughout their entire life. Cohort variation and individual heterogeneity both accounted for among-individual variation in horn length, suggesting both long-lasting effects of early life conditions and individual-specific horn growth trajectories. Early horn growth did not influence annual survival until 12 years of age, indicating that males do not invest in horn growth at survival costs over most of their lifetime. However, males with fast-growing horns early in life tended to have lower survival at very old ages. Individual heterogeneity, along with the particular life-history tactic of male ibex (weak participation to the rut until an old age after which they burn out in high mating investment), are likely to explain why the expected trade-off between horn growth and survival does not show up, at least until very old ages.     

Correlates of reproductive success within alternative mating tactics of the common shrew

Male common shrews (Sorex araneus) adopt two discrete matingtactics. The most successful males, in terms of number of offspringfathered, are those that establish large overlapping home rangesin areas of high female density early in the breeding season.An alternative, less successful mating tactic is to travel longdistances in search of mating opportunities. This study is aninvestigation of correlates of reproductive success for malesadopting these different mating tactics. Reproductive successunder natural conditions was assessed using DNA fingerprinting,and survival of offspring was monitored in the field. The numberof offspring fathered by males with overlapping home rangeswas positively correlated with the number of female ranges overlappedduring the breeding season and with testes mass. The numberof offspring fathered by males that made long-distance movementswas positively correlated with their epididymal sperm counts.It is argued that competitively superior (overlapping) malesachieve high reproductive success by competing to maximize thenumber of females inseminated, whereas those adopting an alternativemating tactic instead compete largely via sperm competition,aiming to maximize insemination success with any particularfemale. There was no significant difference in the fluctuatingasymmetry (FA) of males adopting different mating tactics (FAwas measured as the difference in length of the paired lateralscent glands). Fluctuating asymmetry was not related to thenumber of offspring fathered by males adopting either matingtactic, but was significantly correlated with the proportionof male offspring fathered that survived to sexual maturity.Although apparently not correlated with mating success in thisspecies, FA may reflect some aspect of genetic quality thataffects offspring survival. [Behav Ecol 7: 334–340 (1996)]     

Age‐dependent male mating tactics in a spider mite—A life‐history perspective

Males often fight with rival males for access to females. However, some males display nonfighting tactics such as sneaking, satellite behavior, or female mimicking. When these mating tactics comprise a conditional strategy, they are often thought to be explained by resource holding potential (RHP), that is, nonfighting tactics are displayed by less competitive males who are more likely to lose a fight. The alternative mating tactics, however, can also be explained by life‐history theory, which predicts that young males avoid fighting, regardless of their RHP, if it pays off to wait for future reproduction. Here, we test whether the sneaking tactic displayed by young males of the two‐spotted spider mite can be explained by life‐history theory. We tested whether young sneaker males survive longer than young fighter males after a bout of mild or strong competition with old fighter males. We also investigated whether old males have a more protective outer skin—a possible proxy for RHP—by measuring cuticle hardness and elasticity using nanoindentation. We found that young sneaker males survived longer than young fighter males after mild male competition. This difference was not found after strong male competition, which suggests that induction of sneaking tactic is affected by male density. Hardness and elasticity of the skin did not vary with male age. Given that earlier work could also not detect morphometric differences between fighter and sneaker males, we conclude that there is no apparent increase in RHP with age in the mite and age‐dependent male mating tactics in the mite can be explained only by life‐history theory. Because it is likely that fighting incurs a survival cost, age‐dependent alternative mating tactics may be explained by life‐history theory in many species when reproduction of old males is a significant factor in fitness.     

Female survival,lifetime reproductive success and mating status in a passerine bird

In facultatively polygynous birds, secondary females of polygynously mated males typically have reduced annual reproductive success, because polygynous males provide less paternal care than monogamous males. Life history theory predicts that, as a result of increased reproductive investment, secondary females should suffer from reduced survival and lifetime reproductive success, but previous studies provided only weak support for this hypothesis. We used 7 years of data to study the fitness of female collared flycatchers Ficedula albicollis in relation to mating status by estimating survival and lifetime reproductive success. Taking differences in recapture probability into account, a mark-recapture analysis revealed that females observed at least once to breed as secondary female had higher survival than other females. This relationship was not confounded by laying date, because when we assessed the impact of laying date on survival, we found similar survival patterns. Females of polygynous males had reduced breeding success in terms of number of young fledged during the current reproductive event. However, during their lifetime females found at least once in primary or secondary mating status produced significantly more eggs, and at least the same number of fledglings and recruits as monogamous females. Thus, in the collared flycatcher, females of polygynously mated males seem to suffer from mating status during the most recent reproductive event, but considering survival and lifetime reproductive success, the apparently disadvantageous mating event is not necessarily associated with reduced residual reproductive value.     

Sex- and age-specific survival of the highly dimorphic Alpine ibex: evidence for a conservative life-history tactic

1. Age-specific survival of 215 males and 117 females of the highly sexually dimorphic Alpine ibex Capra ibex (L.) was assessed from a 21-year capture-mark-recapture (CMR) programme (1983-2004). The study covered two contrasted periods of population performance (high performance from 1983 to 1997 vs. low performance from 1998 onwards). 2. Based on current life-history theories for sexually dimorphic species, we expected that survival should decrease with age in both sexes, female survival should be buffered against environmental variations, male survival should decrease during the low performance period, and adult survival should be lower in males than females during the low performance period. 3. Survival of both sexes was strongly affected by age, with the four age classes (yearling, prime-aged adults of 2-8 years of age, old adults of 8-13 years of age, and senescent adults from 13 years of age onwards) generally reported for large herbivores. 4. Survival of females at all ages, and of yearling and prime-aged males, was buffered against environmental variations and was the same during periods of high and low population performance. The survival of old males decreased in years of low population performance. 5. All marked yearlings (32 females, 56 males) survived to age 2. Survival of prime-aged females (0.996 +/- 0.011) was higher than for other large herbivores, but similarly to other large herbivore species, it declined slowly and regularly with increasing age afterwards. Male survival was 5-15% higher each year than that of males of other large herbivores. Males enjoyed very high survival when prime-aged (0.981 +/- 0.009) and as old adults (high-performance period: 0.965 +/- 0.028, low-performance period: 0.847 +/- 0.032). 6. The very high survival of males, coupled with their prolonged mass gain, suggests a highly conservative reproductive tactic. Male ibex differ from similar-sized herbivores by showing a nearly indeterminate growth in horn size and body mass. By surviving to an advanced age, males may enjoy high reproductive success because of their large size.     

Male reproductive success and its behavioural correlates in a polygynous mammal,the Galápagos sea lion (Zalophus wollebaeki)

Sexual selection theory predicts competitive males and choosy females. Nevertheless, since molecular marker‐based studies, paternity outside the expected mating patterns has increasingly been described. Even in highly polygynous systems, where paternity is expected to be strongly skewed towards large, dominant males, alternative mating tactics have been suggested. We examined reproductive success in the polygynous Galápagos sea lion (Zalophus wollebaeki). Semiaquatic territoriality allows females to move freely and may lower the degree of polygyny otherwise suggested by both territorial behaviour and strong sexual dimorphism. We assigned paternities with 22 microsatellites and analysed how male reproductive success was related to size, dominance status, intra‐sexual agonistic behaviour, proximity to females, and attendance in the colony. Male behaviour was consistent across two seasons for all parameters under consideration. Attendance was by far the most important determinant of paternal success. Skew in reproductive success towards large, dominant males was weak and dominance status played no role. This appears to be caused by an extremely long reproductive season lasting five or more months, making it difficult for any male to monopolize receptive females. Females seem to choose displaying males that were present in the colony for a long time rather than dominance per se. Sexual dimorphism in Galápagos sea lions may thus be more influenced by selection for fasting than fighting ability. Our data provide further evidence for alternative mating tactics, as several males gained relatively high reproductive success despite short attendance and hardly any involvement in agonistic interactions.     

Influences of Mating Group Composition on the Behavioral Time-Budget of Male and Female Alpine Ibex (Capra ibex) during the Rut

During the rut, polygynous ungulates gather in mixed groups of individuals of different sex and age. Group social composition, which may vary on a daily basis, is likely to have strong influences on individual’s time-budget, with emerging properties at the group-level. To date, few studies have considered the influence of group composition on male and female behavioral time budget in mating groups. Focusing on a wild population of Alpine ibex, we investigated the influence of group composition (adult sex ratio, the proportion of dominant to subordinate males, and group size) on three behavioral axes obtained by Principal Components Analysis, describing male and female group time-budget. For both sexes, the first behavioral axis discerned a trade-off between grazing and standing/vigilance behavior. In females, group vigilance behavior increased with increasingly male-biased sex ratio, whereas in males, the effect of adult sex ratio on standing/vigilance behavior depended on the relative proportion of dominant males in the mating group. The second axis characterized courtship and male-male agonistic behavior in males, and moving and male-directed agonistic behavior in females. Mating group composition did not substantially influence this axis in males. However, moving and male-directed agonistic behavior increased at highly biased sex ratios (quadratic effect) in females. Finally, the third axis highlighted a trade-off between moving and lying behavior in males, and distinguished moving and female-female agonistic behavior from lying behavior in females. For males, those behaviors were influenced by a complex interaction between group size and adult sex ratio, whereas in females, moving and female-female agonistic behaviors increased in a quadratic fashion at highly biased sex ratios, and also increased with increasing group size. Our results reveal complex behavioral trade-offs depending on group composition in the Alpine ibex, and emphasize the importance of social factors in influencing behavioral time-budgets of wild ungulates during the rut.     

Tactic‐specific benefits of polyandry in Chinook salmon Oncorhynchus tshawytscha

This study examined whether polyandrous female Chinook salmon Oncorhynchus tshawytscha obtain benefits compared with monandrous females through an increase in hatching success. Both of the alternative reproductive tactics present in male O. tshawytscha (large hooknoses and small, precocious jacks) were used, such that eggs were either fertilized by a single male (from each tactic) or multiple males (using two males from the same or different tactics). The results show that fertilized eggs from the polyandrous treatments had a significantly higher hatching success than those from the monandrous treatments. It is also shown that sperm speed was positively related with offspring hatching success. Finally, there were tactic‐specific effects on the benefits females received. The inclusion of jacks in any cross resulted in offspring with higher hatching success, with the cross that involved a male from each tactic providing offspring with the highest hatching success than any other cross. This study has important implications for the evolution of multiple mating and why it is so prevalent across taxa, while also providing knowledge on the evolution of mating systems, specifically those with alternative reproductive tactics.     

Mating system, sexual dimorphism, and the opportunity for sexual selection in a territorial ungulate

In mammals, species with high sexual size dimorphism tend tohave highly polygynous mating systems associated with high variancein male lifetime reproductive success (LRS), leading to a highopportunity for sexual selection. However, little informationis available for species with weak sexual size dimorphism. Ina long-term study population, we used parentage analysis basedon 21 microsatellite markers to describe, for the first time,variance in male lifetime breeding success (LBS) of roe deer,a territorial ungulate where males weigh less than 10% morethan females. LBS ranged from 0 to 14 (mean = 4.54, variance= 15.5), and its distribution was highly skewed, with only afew males obtaining high LBS and many males failing to breedor siring only one fawn. As predicted for polygynous specieswith low sexual size dimorphism, the standardized variance inmale LBS was low (I_m = 0.75) and was only slightly higher thanthe standardized variance in female LRS (I_f = 0.53), suggestinga low opportunity for sexual selection. The I_m value reportedhere for roe deer is much lower than values reported for highlydimorphic ungulates such as red deer (I_m > 3). We suggestthat, along a continuum of opportunity for sexual selection,roe deer occupy a position closer to monogamous and monomorphicterritorial ungulates than to highly polygynous, sexually dimorphicungulates with dominance rank–based mating systems suchas harems or roving mating systems.     

Age‐Related Male Reproductive Investment in Courtship Display and Nuptial Gifts in a Moth,Ostrinia scapulalis

Due to a trade‐off between current and future reproduction, costly reproductive investments should be increased towards the end of a lifespan when the probability of reproduction becomes low (terminal investment hypothesis). We investigated age‐related changes in male reproductive investment towards courtship display and the spermatophore in three age classes (young, middle‐aged and old) of a monandrous moth, Ostrinia scapulalis. As predicted, old males had higher mating success than young and middle‐aged males in no‐choice tests. Moreover, two‐choice tests revealed that middle‐aged males had a higher success rate than young males because of their higher courtship frequency rather than any female preference for them. It was found that old males produced a larger spermatophore than young and middle‐aged males, suggesting greater reproductive effort. The protein content of spermatophores also tended to increase with male age. Despite the age‐related variation in spermatophore size and protein content, age did not affect female fecundity or longevity. A decrease in the number of sperm in the older males might counteract the nutritional benefit of larger spermatophores. Alternatively, fitness components other than longevity and fecundity may be influenced by male age.     

Male tactics and reproductive success in the harem polygynous bat Saccopteryx bilineata

Alternative tactics in reproductive behavior enable individualsto maximize their fitness in relation to competitors in thesame population. In many taxa, territoriality is a common tacticof males to increase their reproductive success. In the batSaccopteryx bilineata, territorial males defend roosting areasfor females against other males and court females throughout the year. Peripheral males in the same colonies do not defendterritories but compete with territorial males for reproductionwith females. In this study, we monitored the behavior of themales in a natural colony over three reproductive seasons.We compared morphological and age data and measured the reproductiveoutput of males adopting the territorial or peripheral tactic.No differences in body size or weight were detected betweenmale types, but the probability of adopting a tactic seemedto be age dependent. Peripherals were often young males andreplaced territorials in several cases, whereas the oppositecase was not observed. Peripherals were not excluded from reproduction,but territorials were more likely to reproduce. Variation in reproductive success was high within both male tactics, andthe reproductive success of some peripherals was comparableto territorials, but, on average, the reproductive successof territorials was more than twice as high. Therefore, behavioraltactics do not seem to be equally profitable in general butmay represent different phases in the reproductive life of manyS. bilineata males.     

Male rank and reproductive activity in Savanna baboons

Access to sexually receptive baboon females has been linked to male dominance rank. An intensive 19-month field study of mate choice and mate competition among savanna baboons was undertaken in order to elucidate those factors influencing mating success. During this study, male agonistic rank was not correlated with male mating success among adult males. However, the inclusion of adolescent males into the analysis yielded significant correlations between rank and mating success. Examination of prior fieldwork revealed that no baboon field study has conclusively demonstrated a significant correlation between male rank and reproduction among adult males. Most studies reporting a correlation between male rank and reproduction have included subadult males in the analysis. It is concluded that male rank is an unreliable predictor of male reproductive activity among adult male baboons. A low agonistic rank need not reduce male mating success because adult male baboons utilize a variety of reproductive tactics in gaining access to consort females.     

Alternative male reproductive tactics in a natural population of prairie voles <Emphasis Type="Italic">Microtus ochrogaster</Emphasis>

Alternative reproductive tactics have been described in male mammals, but little information exists regarding fitness benefits and whether males change tactics. Adult male prairie voles Microtus ochrogaster (Wagner, 1842) display alternative tactics described as resident and wanderer. Enclosure studies provide conflicting data concerning the relative success of each tactic and whether males display one tactic throughout adulthood. To characterize further residents and wanderers in this species, we examined data collected during 5 years of monitoring a natural population in Illinois, USA. We found that during the breeding period, wandering males survived longer, moved longer distances, and were more likely than residents to have scrotal testes. During the nonbreeding period, wandering and resident males differed only in whether or not they established residency. Data on sources and fates of resident and wandering males revealed that a substantial proportion of males switched tactics. Our estimate of the reproductive contribution of wandering males to the population, which is based on the premise that wandering males typically mate with single females, suggests that wanderers contribute 34–38% of young recruited during March through October and 4–12% in November, when single females are less common. Parentage studies in natural populations are necessary to test our estimates.     

Females better face senescence in the wandering albatross

Sex differences in lifespan and aging are widespread among animals. Since investment in current reproduction can have consequences on other life-history traits, the sex with the highest cost of breeding is expected to suffer from an earlier and/or stronger senescence. This has been demonstrated in polygynous species that are highly dimorphic. However in monogamous species where parental investment is similar between sexes, sex-specific differences in aging patterns of life-history traits are expected to be attenuated. Here, we examined sex and age influences on demographic traits in a very long-lived and sexually dimorphic monogamous species, the wandering albatross (Diomedea exulans). We modelled within the same model framework sex-dependent variations in aging for an array of five life-history traits: adult survival, probability of returning to the breeding colony, probability of breeding and two measures of breeding success (hatching and fledging). We show that life-history traits presented contrasted aging patterns according to sex whereas traits were all similar at young ages. Both sexes exhibited actuarial and reproductive senescence, but, as the decrease in breeding success remained similar for males and females, the survival and breeding probabilities of males were significantly more affected than females. We discuss our results in the light of the costs associated to reproduction, age-related pairing and a biased operational sex-ratio in the population leading to a pool of non-breeders of potentially lower quality and therefore more subject to death or breeding abstention. For a monogamous species with similar parental roles, the patterns observed were surprising and when placed in a gradient of observed age/sex-related variations in life-history traits, wandering albatrosses were intermediate between highly dimorphic polygynous and most monogamous species.     

Reproductive success in reindeer males in a herd with varying sex ratio

In polygynous species, male reproductive success is often correlated with dominance status of individual males and sex ratio in the population. Reindeer, Rangifer tarandus, is a polygynous species, and here we compared the variation in male reproductive success and dominance status during two successive years in a herd with a male:female sex ratio of 1:7 and 1:3. Copulations were recorded, together with data on male dominance hierarchy and size of mating groups. Male reproductive success was estimated by paternity analysis of calves using microsatellite DNA markers. The distribution of reproductive success among the males was highly skewed for both years with the most dominant male also being the most successful. The largest mating group was established in the herd with the least skew in sex ratio. In this herd some of the adult males present were less reproductively successful than some of the more subordinate younger males. Estimates of the mating group size of males, correcting for dominance status when more than one male is present in the groups, gave good prediction of individual males' reproductive success.     

Best squirrels trade a long life for an early reproduction

Age at primiparity plays a crucial role in population dynamics and life-history evolution. Long-term data on female North American red squirrels were analysed to study the fitness consequences of delaying first reproduction. Early breeders were born earlier, had a higher breeding success and achieved a higher lifetime reproductive success than females who delayed their first reproduction, which suggests a higher quality of early breeders. However, early breeders had similar mass when tagged, and similar number of food caches available at one year of age as late breeders. Nevertheless, we found evidence of survival costs of early primiparity. Early breeders had a lower survival between one and two years of age than late breeders and a lower lifespan. Our study points out that two reproductive tactics co-occurred in this population: a tactic based on early maturity at the cost of a lower survival versus a tactic based on delayed maturity and long lifespan. High quality individuals express the most profitable tactic by breeding early whereas low quality individuals do the best of a bad job by delaying their first reproduction.     

Harvesting of males delays female breeding in a socially monogamous mammal; the beaver

Human exploitation may skew adult sex ratios in vertebrate populations to the extent that males become limiting for normal reproduction. In polygynous ungulates, females delay breeding in heavily harvested populations, but effects are often fairly small. We would expect a stronger effect of male harvesting in species with a monogamous mating system, but no such study has been performed. We analysed the effect of harvesting males on the timing of reproduction in the obligate monogamous beaver (Castor fiber). We found a negative impact of harvesting of adult males on the timing of parturition in female beavers. The proportion of normal breeders sank from over 80%, when no males had been shot in the territories of pregnant females, to under 20%, when three males had been shot. Harvesting of males in monogamous mammals can apparently affect their normal reproductive cycle.     

Males achieve greater reproductive success through multiple broods than through extrapair mating in house wrens

In polygynous species, it is unclear whether extrapair matings provide a better reproductive payoff to males than additional social mates. Male house wrens, Troglodytes aedon, show three types of social mating behaviour: single-brooded monogamy, sequential monogamy (two broods) and polygyny. Thus, male reproductive success can vary depending on the number of mates, the number of broods and the number of extrapair fertilizations. We used microsatellite markers to determine the realized reproductive success (total number of young sired from both within-pair and extrapair fertilizations) of males in these three categories. We found that polygynous males were more likely to be cuckolded than monogamous males; however, half of the polygynous males had a third brood, which resulted in similar reproductive success for sequentially monogamous and polygynous males. Despite the paternity gained from extrapair fertilizations by single-brooded males, males were more successful when they produced multiple broods during a season, either sequentially (monogamy) or simultaneously (polygyny). In our population, multibrooded males were more likely to have prior breeding experience and arrived earlier in the season, which provided a better opportunity to obtain more than one brood and, thus, produce more young.