Patterns of paternity skew in Formica ants

Reproductive skew among cooperatively breeding animals has recently attracted considerable interest. In social insects reproductive skew has been studied in females but not in males. However, cooperative breeding of males occurs when two males mate with the same queen and father offspring. Here we present the first analysis of comparative data on paternity skew in ants. We show that, across seven species of Formica ants, the average skew in paternity among worker offspring of doubly mated queens is negatively correlated with the population-wide frequency of multiple (mostly double) mating. We also demonstrate that this trend is relatively robust in additional analyses taking phylogenetic relationships between species into account. The observed trend is opposite to the one normally found in non-social insects with second-male precedence through sperm displacement, but agrees with predictions based on queen-male conflict over sperm allocation as a consequence of facultative, worker controlled, sex allocation – an interpretation which assumes first-male precedence. However, alternative (but not mutually exclusive) explanations are possible and further studies will be needed to discriminate between these alternatives. Received: 16 May 1997 / Accepted after revision: 26 September 1997     

Sex-specific reproductive behaviours and paternity in free-ranging Barbary macaques (Macaca sylvanus)

In a wide variety of species, male reproductive success is determined by contest for access to females. Among multi-male primate groups, however, factors in addition to male competitive ability may also influence paternity outcome, although their exact nature and force is still largely unclear. Here, we have investigated in a group of free-ranging Barbary macaques whether paternity is determined on the pre- or postcopulatory level and how male competitive ability and female direct mate choice during the female fertile phase are related to male reproductive success. Behavioural observations were combined with faecal hormone analysis for timing of the fertile phase (13 cycles, 8 females) and genetic paternity analysis (n = 12). During the fertile phase, complete monopolisation of females did not occur. Females were consorted for only 49% of observation time, and all females had ejaculatory copulations with several males. Thus, in all cases, paternity was determined on the postcopulatory level. More than 80% of infants were sired by high-ranking males, and this reproductive skew was related to both, male competitive ability and female direct mate choice as high-ranking males spent more time in consort with females than low-ranking males, and females solicited copulations mainly from dominant males. As most ejaculatory copulations were female-initiated, female direct mate choice appeared to have the highest impact on male reproductive success. However, female preference was not directly translated into paternity, as fathers were not preferred over non-fathers in terms of solicitation, consortship and mating behaviour. Collectively, our data show that in the Barbary macaque, both sexes significantly influence male mating success, but that sperm of several males generally compete within the female reproductive tract and that therefore paternity is determined by mechanisms operating at the postcopulatory level.     

Factors predicting male fertilization success in an external fertilizer

In postcopulatory sexual selection both sperm competition and cryptic female choice are considered to be important selective agents, but their relative importance for male fertilization success has received little attention. We tested whether sperm quality, male spawning coloration, male heterozygosity, and genetic overlap with the female explained a male’s fertilization success in controlled in vitro fertilization competition trials between equal numbers of sperm from pairs of male Arctic charr (Salvelinus alpinus), an external fertilizer. Offspring were genotyped to determine each males’ share of paternity. The velocity of a male’s sperm relative to the velocity of the competing male’s sperm was the best predictor of male fertilization success. Yet, sperm velocity was not related to spawning coloration or male heterozygosity. In fact, the most brightly colored male in a pair had the lowest fertilization probability. This could result from cryptic female choice for pale males, but might rather be a result of paler males producing more competitive sperm than more colored males. Furthermore, the more microsatellite alleles a male shared with the female relative to the competing male, the higher fertilization success he had. We argue that this latter may be an effect of assortative cryptic female choice, which might prevent hybridization with sympatric Arctic charr morphs or one form of kin selection.     

Male genital traits and mating interval affect male fertilization success in the water strider Gerris lacustris

Parker's seminal work brought attention to the possibility of postmating sexual selection by non-random fertilization success. Mechanisms for these processes are still only partly understood and there is clearly a need for more studies of intraspecific variation in sperm precedence. Here, we report results from an experimental study of the variation in fertilization success between males of the water strider Gerris lacustris. Genital morphology, male body size, and copulation duration were examined as possible correlates of paternity. The significance of guarding duration was also analysed. Only male genital morphology was correlated to fertilization success. This is one of the first studies showing a relationship between male genital traits and fertilization success, supporting the view that sexual selection may be responsible for the rapid and divergent evolution of genital structures in animals with internal fertilization. The fertilization success of last males varied considerably after double matings with a short mating interval (10 min). Last-male priority ranged from 0 to 100% and usually one of the males involved fertilized almost all the eggs. After double matings with a short mating interval, the proportion of eggs fertilized by the last male averaged 0.68 and was greater than 0.5. In contrast, the average fertilization success was biased towards the first male when the matings were more spread out over time (24 h). These results do not support earlier suggestions of a widespread last-male sperm priority in water striders. Received: 28 July 1998 / Received in revised form: 15 March 1999 / Accepted: 28 March 1999     

Differences in reproductive success between laboratory and wild-derived golden hamsters (Mesocricetus auratus) as a consequence of inbreeding

All laboratory golden hamsters (Mesocricetus auratus) originated from a sibling pairing back in 1930. Due to this extreme founder event, domestic golden hamsters are presumed to be one of the most bottlenecked animal populations. Nevertheless, domestic hamsters show no obvious signs of inbreeding depression in commonly used breeding stocks. To explore the existence of potentially masked inbreeding effects, we compared the reproductive success of laboratory (lab) and wild-derived (wild) golden hamsters. We allowed oestrus females to mate consecutively with lab and wild males. The resulting offspring was genotyped using microsatellites to assess paternity. Finally, we compared male reproductive success to genetic variability, sexual behaviour and different sperm characteristics. Both hamster strains exhibited the expected large difference in genetic diversity (H _wild =0.712±0.062 vs H _lab =0.007±0.007. The reproductive success of wild males dramatically exceeded that of lab males (87% of pups were sired by wild males). Sexual behaviour of wild and lab males only varied in the number of long intromissions (intromissions without ejaculation at the end of the mating). No significant differences were observed in relation to mounting, ejaculation and intromission. There were also no apparent differences in sperm motility, velocity and density or testis histology between wild and lab hamsters. We conclude that the reduced reproductive success of lab males represents a hidden inbreeding effect, although its precise physiological cause remains unclear. These results provide first evidence for a major fitness disadvantage in captive golden hamsters.     

Male reproductive success in free-ranging feral horses

In the social organization of feral horses, adult males compete to monopolize groups or bands of females, sometimes called harems. Alternative male strategies are to remain alone or with other bachelors or, less commonly, to accept subordinate status within a harem. The hypothesis that dominant harem stallion status confers a reproductive advantage was tested in free-ranging feral horses. The presence of foals in harems headed by vasectomized (VSX) versus intact stallions was used to assess the ability of these stallions to control reproduction in their harems. Of harems headed by VSX stallions, 17 and 33% contained foals during years 2 and 3 post-treatment, respectively. In contrast, 86 and 80% of harems headed by non-VSX stallions contained foals in those years. Acquisition of pregnant mares appeared more likely than sneak copulations by bachelor stallions to account for foals in harems with a single stallion. However, most foals were born into harems that included a subordinate stallion, an occurrence that was undoubtedly exacerbated by the extended breeding season resulting from the sterility of the harem stallion. Thus, in comparing alternative reproductive tactics, bachelors appeared less successful than subordinate stallions within a harem. However, the highest reproductive success was achieved by the harem stallion, further demonstrating that alternative tactics are not equally profitable. Received: 13 July 1999 / Received in revised form: 24 July 1999 / Accepted: 24 July 1999     

Alternative reproductive tactics in male common shrews: relationships between mate-searching behaviour,sperm production,and reproductive success as revealed by DNA fingerprinting

The common shrew (Sorex araneus) is a solitary small mammal with a promiscuous mating system. Previous studies of this species suggest that females typically mate multiply, and that males may adopt alternative mate-searching tactics. We studied two generations of common shrews in a population near Oxford, England. Males were found to adopt two different mate-searching tactics. Those classed as type A occupied relatively small exclusive ranges during March, and made repeated long-distance movements to visit female ranges around the time of first oestrus in April. Males classed as type B established large overlapping ranges in areas of relatively high female density during March, and maintained these ranges throughout April. Type B males were larger than type A males at an early stage of sexual maturation, but there was no difference in the adult body size of the two types of male. Type A males had significantly higher epididymal sperm counts than type B males. Paternity analyses of litters born during the first year of the study reveal that the mean number of offspring fathered by type B males was greater than the mean number fathered by type A males. It is concluded that different mate-searching tactics may be conditional upon the timing of sexual maturation. Differences in sperm production are discussed in relation to sperm competition theory.     

Alternative reproductive tactics and male-dimorphism in the horned beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae)

Adult dung beetles (Onthophagus acuminatus) exhibit continuous variation in body size resulting from differential nutritional conditions experienced during larval development. Males of this species have a pair of horns that protrude from the base of the head, and the lengths of these horns are bimodally distributed in natural populations. Males growing larger than a threshold body size develop long horns, and males that do not achieve this size grow only rudimentary horns or no horns at all. Previous studies of other horned beetle species have shown that horned and hornless males often have different types of reproductive behavior. Here I describe the mating behaviors of the two male morphs of O. acuminatus during encounters with females. Females excavate tunnels beneath dung, where they feed, mate and provision eggs. Large, horned males were found to guard entrances to tunnels containing females. These males fought with all other males that attempted to enter these tunnels. In contrast, small, hornless males encountered females by sneaking into tunnels guarded by other males. In many instances, this was accomplished by digging new tunnels that intercepted the guarded tunnels below ground. Side-tunneling behavior allowed sneaking males to enter tunnels beneath the guarding male, and mate with females undetected. Both overall body size and relative horn length significantly affected the outcome of fights over tunnel ownership. These results suggest that alternative reproductive tactics may favor divergence in male horn morphology, with long horns favored in males large enough to guard tunnels, and hornlessness favored in smaller males that adopt the “sneaking” behavioral alternative. Received: 12 October 1996 / Accepted after revision: 8 August 1997     

Survival and lifetime reproductive success in dispersing and resident red squirrels

Dispersal in red squirrels (Sciurus vulgaris) is not sex-biased and strict philopatry is rare. The immigration pattern suggests that nearly all animals have to disperse away from the natal site and that dispersal in this species is the outcome of local (intrasexual) competition. If this interpretation is correct, we predict that dispersers and residents, of both sexes, should have equal survival rates and lifetime reproductive success. Body mass, longevity, reproductive success and dominance rank of 34 resident offspring (settling within 400 m of the natal range) and 70 immigrants (dispersers) were compared. Immigrants did not weigh less than residents as adults, nor did they have a higher mortality during the pre-setding period. Survival rate, lifetime reproductive success (females) and the proportion of males obtaining a high dominance rank were similar for residents and dispersers, and no sex effect was found on either of the parameters studied. These results are consistent with the hypothesis that local competition determines whether an individual disperses further away or settles close to its birthplace.     

Sperm characteristics associated with different male reproductive tactics in bluegills (Lepomis macrochirus)

We examined the availability and motility of sperm from parental and sneaker male bluegills (Lepomis macrochirus), a colonially nesting sunfish (Family Centrarchidae) with male parental care and a high incidence of cuckoldry by both sneaker and satellite males. We found no differences between sneakers and parentals in length and swimming speed of sperm, or percent and duration of sperm activity. In sneaker milt, however, sperm was almost 50% more concentrated than in parental milt (16.5×10⁶ vs 11.5×10⁶ sperm/μl of milt, respectively). Despite this difference in sperm concentration, stripped ejaculates from sneakers contained almost 400 million fewer sperm (only 32% as many sperm) than those from parentals due to their much smaller stripped ejaculate volumes (only about 19% that of parentals). Thus unless sneakers can compensate by releasing more sperm or gaining closer proximity to eggs at the time of spawning, they may be at a disadvantage with respect to sperm competition. We discuss these results in relation to models for the evolution of alternative reproductive behaviours in this species and suggest that the cuckolders may be making the best of a bad situation. Received: 18 February 2000 / Revised: 23 March 2000 / Accepted: 14 September 2000     

Sexual selection and reproductive careers in mandrills (Mandrillus sphinx)

In sexually dimorphic, polygynous species, where males provide little parental care and competition between males for access to fertile females is high, sexual selection theory predicts sex differences in age-specific reproductive output and mortality profiles, and greater variance in lifetime reproductive success in males than in females. We examined age-specific reproductive output, mortality patterns and the extent and causes of variation in reproductive success for a semi-free-ranging colony of mandrills (Mandrillus sphinx, Cercopithecidae) in Franceville, Gabon, using long-term (20 year) demographic records and microsatellite parentage analysis. Although differences in the demography and feeding ecology of this closed, provisioned colony, in comparison with wild mandrills, limit interpretation of our results, sex differences in reproductive output and mortality showed the patterns predicted by sexual selection theory. Mortality was higher in males than in females after sexual maturity, and lifespan was significantly shorter in males (mean 14 year) than in females (>22 year). Age at first reproduction was significantly earlier in females (mean 4.2 year) than in males (11.6 year), and male reproductive output declined earlier. All females of breeding age produced offspring; while only 17 of 53 sexually mature males (32%) sired. Males sired a maximum of 41 offspring, versus 17 in females, and variance in male reproductive output was significantly greater than in females at all ages. The most important influence on variation in lifetime reproductive output in both sexes was joint variation between length of the breeding period and reproductive rate, due to lower reproductive rates in younger animals. Finally, social rank significantly influenced reproductive output in both sexes: high-ranking females began their reproductive careers earlier and had a higher subsequent reproductive rate than low-ranking females, while males that achieved top rank during their career sired far more offspring than males that did not.Electronic Supplementary Material Supplementary material is available for this article at     

Determinants of male mating success in the red bishop (Euplectes orix)

We studied sexual selection in the red bishop, Euplectes orix, a colonial, polygynous weaverbird widely distributed over sub-Saharan Africa. Male reproductive success measured in terms of the number of nests accepted by females and the number of eggs and nestlings in all the nests on a male's territory varied considerably. The standardized variance (variance/mean²) in male reproductive success ranged from 0.505 to 1.737 in different years, indicating a high potential for sexual selection in this species. An analysis of genetic parentage for 432 nestlings by non-radioactive, multilocus DNA fingerprinting confirmed that male reproductive success (number of young sired on the territory) in this species can be reliably estimated by the measures introduced above. In all 4 study years there was a strong positive correlation between male mating success and the total number of nests that males built in their territories. The number of nests built can be partitioned into the number of weeks a male held a territory and his nest-building performance. Both factors exert a significant positive effect on male mating success and in combination explained between 53.3 and 86.3% of the variation in male reproductive success. Male morphological characters were found to be of no importance. Males that established a territory in the following season built more nests and held their territories for longer than males that did not establish a territory in the following season, suggesting that these measures might be indicators of male condition and quality. Male nest-building performance (number of nests built per week) seems to be unrelated to male condition or quality. Received: 8 January 1999 / Received in revised form: 7 June 1999 / Accepted: 13 June 1999     

Sperm competition or sperm selection: no evidence for female influence over paternity in yellow dung flies Scatophaga stercoraria

Recent studies of non-random paternity have suggested that sperm selection by females may influence male fertilization success. Here we argue that the problems originally encountered in partitioning variation in non-random mating between male competition and female choice are even more pertinent to interpreting patterns of non-random paternity because of intense sperm competition between males. We describe an experiment with the yellow dung fly, Scatophaga stercoraria, designed to partition variance in the proportion of offspring sired by the second male, P ₂, between males and females, and to control for sperm competition. Large males were shown to have a higher P ₂ than small males but P ₂ was independent of the size of the female’s first mate. This result might suggest an absolute female preference for large males via sperm selection. However, large males have a higher constant rate of sperm transfer and displacement. After controlling for this effect of sperm competition, large males did not achieve higher paternity than small males. We argue that a knowledge of the mechanism of sperm competition is essential so that male effects can be controlled before conclusions are made regarding the influence of sperm selection by females in generating non-random paternity. Received: 4 April 1995 / Accepted after revision: 17 October 1995     

Male crickets increase sperm number in relation to competition and female size

There is evidence to suggest that males of various species can respond to the threat of sperm competition by varying the amount of sperm transferred during copulation. We tested this in two species of cricket, Acheta domesticus and Gryllodes supplicans (Orthoptera: Gryllidae) by varying the apparent threat of intermale competition experimentally. The results showed that males of both species increased the amount of sperm transferred as apparent competition increased and that male A. domesticus transferred more sperm when encountering larger females. The results also showed that male G. supplicans produced a larger spermatophylax when a larger ampulla was transferred, a relationship consistent with a sperm protection function. Received: 5 May 1995/Accepted after revision: 27 January 1996     

Proximal traits and mechanisms for biasing paternity in the red flour beetle Tribolium castaneum (Coleoptera: Tenebrionidae)

A comprehensive understanding of sexual selection requires knowledge of the traits and mechanisms responsible for increasing a male’s paternity share (proportion of progeny sired) relative to that of other males mating with the same female. In this study we manipulated by starvation the expression of traits that might influence male paternity share in Tribolium castaneum. We then conducted experiments to examine how male starvation affects male performance during sequential episodes of sexual selection from mating to progeny production, and investigated female control over specific stages by using live vs dead females. Comparison of starved vs fed males revealed that T. castaneum females have control over spermatophore transfer during mating, as live females rejected inseminations by starved (“low quality”) males. None of the measured male copulatory behaviors (leg-rubbing frequency, asymmetry, and percent of time spent rubbing) affected the probability of successful insemination, but the last two were positively associated with male paternity share. Spermatophore positioning within the female reproductive tract was not affected by male treatment (starved/fed), by female treatment (live/dead), or by male copulatory behaviors. Starvation, however, had a dramatic effect on male reproductive physiology, decreasing both accessory gland size and total number of sperms transferred (but not sperm viability in seminal vesicles). In addition, females who mated to starved males stored fewer sperms in their spermathecae, which, together with decreased ejaculate size, may explain the reduced paternity share of starved males compared to fed males. This study elucidates some cryptic mechanisms influencing male reproductive success and aids our understanding of trait evolution through sexual selection.     

Socioecological influences on the reproductive success of female mountain gorillas (<Emphasis Type="Italic">Gorilla beringei beringei</Emphasis>)

Over the past few decades, socioecological models have been developed to explain the relationships between the ecological conditions, social systems, and reproductive success of primates. Feeding competition, predation pressures, and risk of infanticide are predicted to influence how female reproductive success (FRS) depends upon their dominance rank, group size, and mate choices. This paper examines how those factors affected the reproductive success of female mountain gorillas (Gorilla beringei beringei) of the Virunga Volcanoes, Rwanda from 1967–2004. Reproductive success was measured through analyses of interbirth intervals, infant survival, and surviving infant birth rates using data from 214 infants born to 67 females. Mountain gorillas were predicted to have “within-group scramble” feeding competition, but we found no evidence of lower FRS in larger groups, even as those groups became two to five times larger than the population average. The gorillas are considered to have negligible “within-group contest” competition, yet higher ranked mothers had shorter interbirth intervals. Infant survival was higher in multimale groups, which was expected because infanticide occurs when the male dies in a one-male group. The combination of those results led to higher surviving birth rates for higher ranking females in multimale groups. Overall, however, the socioecological factors accounted for a relatively small portion of the variance in FRS, as expected for a species that feeds on abundant, evenly distributed foliage.     

Philopatry and mother-daughter associations in bushy-tailed woodrats: space use and reproductive success

Social groups in mammals are often based on overlapping generations of philopatric females, yet few researchers have examined fitness consequences of associations between females and their daughters. We examined survival and reproductive consequences of sharing a natal site with one's mother or daughter in wild bushy-tailed woodrats (Neotoma cinerea). Bushy-tailed woodrats reside on discrete rocky outcrops, and females tend to spend their entire reproductive life on their natal outcrop. Mothers and daughters that co-existed on the natal outcrop were closely associated in space. Juvenile females were more likely to survive their first winter to become breeding yearlings at their natal site if their mother was also present at the natal site during the winter. Juveniles survived equally well with or without their mother where densities of adult females were experimentally reduced, suggesting that females enhance their daughter's survival by facilitating their access to limited resources. Yearling females exhibited no reproductive costs from association with their mothers at the natal site during the breeding season; in fact, yearlings that bred at the natal site simultaneously with their adult mothers tended (P = 0.07) to experience fewer reproductive failures than did those that bred in the absence of their mothers. Mothers did not experience any detectable costs when sharing a natal site with a daughter. We conclude that bushy-tailed woodrats exhibit stable, fitness-enhancing associations among mothers and their philopatric daughters.     

Copulation behavior and paternity in the chaffinch

Summary We investigated two aspects of sperm competition in a wild population of chaffinches Fringilla coelebs: copulation behavior and genetic parentage determined by DNA fingerprinting. Pairs copulated at a high rate before laying, peaking at 4.4 copulation attempts per hour on day –3 relative to laying, with an average of 207 copulation attempts (83 behaviorally successful) per clutch. Extra-pair copulation attempts (n = 20) made up 7.8% of all copulation attempts that females were involved in. The rate at which pairs copulated was lower during egg-laying, but there was no evidence that this was due to the male of the pair timing copulations to coincide with an insemination window; it was more likely due to the fact that females solicited copulations at a lower rate. Both sexes solicited copulations but males solicited mainly extra-pair copulations. DNA fingerprinting showed that 17.0% of chicks (n = 47) in 23% of broods (n = 13) were fathered by a male other than the one paired to their mother. There was no evidence of intraspecific brood parasitism. In three cases where we were able to identify the father of extra-pair offspring it proved to be a neighboring male.Correspondence to: B.C. Sheldon     

Biased parental investment and reproductive success in Gabbra pastoralists

Demographic data from 848 Gabbra households are used to examine the relationships between herd size and reproductive success in relation to sex, in a traditional, pastoralist population. The number of camels in the household herd has a significant positive effect on the reproductive success of both men and women, although the effect of wealth is greater for men, as predicted from evolutionary theory. The greater the number of elder brothers a man has, the lower his reproductive success, as a result of a smaller initial herd and a later age at marriage. This is not true for women –number of elder sisters does not have a measurable effect on a woman’s fertility, although it does have a small, negative effect on the size of her dowry. These results are interpreted as competition between same-sex siblings for parental investment, in the form of their father’s herd, which is more intense between sons than daughters as parental investments are greatest in males. Received: 30 June 1995/Accepted after revision: 23 October 1995     

Extra-pair paternity,sperm competition and the evolution of testis size in birds

Sperm competition should select for increased sperm production if the probability of fertilization by a specific male is proportional to the relative number of sperm inseminated. A review of the literature generally supports the predicted positive association between sperm production or allocation and various measures of the presumed intensity of sperm competition. However, it is not clear how increased sperm competition is related to extra-pair paternity, and it remains unknown whether certainty of paternity should be associated with relative testis size. Based on a large sample of bird species with information on extra-pair paternity gathered from the literature, we demonstrate that testis mass is related positively to the level of extra-pair paternity, after controlling for body size and phylogeny. Although large testes may be necessary to avoid sperm depletion in species in which males frequently engage in multi-pair copulations, we argue that selection has favoured increased testis mass in situations of more intense sperm competition in order to retaliate against copulations by rival males. The fact the males are not always successful in retaliating against rival ejaculates further suggests that females may largely control the allocation of paternity in birds and that increased sperm production by males may simply be a male strategy to make the best of a bad situation.