Patterns of male reproductive success in a highly promiscuous whale species: the endangered North Atlantic right whale

Parentage analyses of baleen whales are rare, and although mating systems have been hypothesized for some species, little data on realized male reproductive success are available and the patterns of male reproductive success have remained elusive for most species. Here we combine over 20 years of photo-identification data with high-resolution genetic data for the majority of individual North Atlantic right whales to assess paternity in this endangered species. There was significant skew in male reproductive success compared to what would be expected if mating was random (P < 0.001). The difference was due to an excess of males assigned zero paternities, a deficiency of males assigned one paternity, and an excess of males assigned as fathers for multiple calves. The variance in male reproductive success was high relative to other aquatically mating marine mammals, but was low relative to mammals where the mating system is based on resource- and/or mate-defence polygyny. These results are consistent with previous data suggesting that the right whale mating system represents one of the most intense examples of sperm competition in mammals, but that sperm competition on its own does not allow for the same degree of polygyny as systems where males can control access to resources and/or mates. The age distribution of assigned fathers was significantly biased towards older males (P < 0.05), with males not obtaining their first paternity until approximately 15 years of age, which is almost twice the average age of first fertilization in females (8 years), suggesting that mate competition is preventing younger males from reproducing. The uneven distribution of paternities results in a lower effective population size in this species that already has one of the lowest reported levels of genetic diversity, which may further inhibit reproductive success through mate incompatibility of genetically similar individuals.     

Male mating success in an aquatically mating pinniped, the harbour seal (Phoca vitulina), assessed by microsatellite DNA markers

Similar to many other pinniped species, harbour seals ( Phoca vitulina ) mate exclusively at sea. Here we present the first attempt to measure male mating success in an aquatically mating pinniped. Male mating success was estimated by paternity analysis in two cohorts of pups born at Sable Island, Nova Scotia, Canada, using microsatellite DNA markers. The genotypes of 275 pups born in 1994 and 1995 were compared to those of 90 candidate males at six microsatellite loci using a likelihood approach to resolve paternity. Paternity could be assigned for two, 22, 40 and 85 pups at confidence levels of 95, 80, 65 and 50%, respectively. Most successful males were assigned the paternity of a single offspring, suggesting a low variance in male mating success relative to most pinniped species. The proportion of paternal half sibs within cohorts and between maternally related sibs estimated by maximum likelihood were not significantly different from zero. It is thus unlikely that most offspring were sired by a small number of highly successful unsampled males, and that female harbour seals do not usually exhibit fidelity to the same male in sequential breeding seasons. A low level of polygyny in Sable Island harbour seals is consistent with predictions based on their breeding ecology, as females are highly mobile and widely dispersed in the aquatic mating environment at Sable Island.     

Breeding success of male brook trout (Salvelinus fontinalis) in the wild

Competition for females generally results in some males adopting alternative reproductive tactics to acquire matings. For fish, the ecological and evolutionary consequences of these tactics are not well understood because of an inability to link directly the interactions of individuals on the breeding grounds with genetic data. This study combines behavioural observations with genetic estimates of male reproductive success within an intensively studied wild population of lacustrine brook trout (Salvelinus fontinalis). Male brook trout exhibit a conditional reproductive strategy with small males adopting a peripheral position to that of larger dominant males in their proximity to spawning females. Parentage analysis of eggs collected from wild redds confirmed the reproductive success of individual males. Males relegated to peripheral positions during spawning participated frequently in spawning events, but in most cases the first male to spawn was the sole contributor, and no more than two males contributed successfully to a single brood. While behavioural observations of salmonines suggests that reproduction is partitioned among males in a manner dependent upon body size and proximity to spawning females, the genetic evidence from this study suggests a more limited distribution of reproductive success in the field. The genetic contributions of male brook trout are highly skewed towards larger males for this population. A review of the salmonine literature suggests little difference in individual reproductive success for males exhibiting size-related tactics within a conditional mating strategy vs. precocial maturation. Collectively, these genetic studies provide new insights on the evolution of alternative life histories among salmonines.     

Social mating system and reproductive success in house wrens

Current models explaining the establishment and maintenanceof social monogamy and polygyny within avian populations typicallyassume that the reproductive success of polygynous males exceedsthat of monogamous males. This assumption is almost always supportedwhen the number of fledglings or recruits to future breedingpopulations is used to measure adult reproductive success. However,recent studies using DNA markers indicate that simple countsof fledglings or recruits may be a poor estimator of the numberof nestlings sired by the social father. In this paper, we comparethe number of genetic offspring produced by socially monogamousand polygynous house wren (TrogiodyUs atdon) males in nestsat which they were the social father. Polygynous males did,in fact, sire more nestlings in their own nests than did monogamousmales. Moreover, although we have not identified the sires ofextrapair nestlings, we document that even when all extrapairnestlings in this population are hypotheticaOy assigned to monogamousmales, die total reproductive success of polygynous males exceedsthat of monogamous males. These results and those of severalother recent studies are consistent with the assumption thatpolygynous males produce more offspring than monogamous males.     

Voice pitch predicts reproductive success in male hunter-gatherers

The validity of evolutionary explanations of vocal sexual dimorphism hinges upon whether or not individuals with more sexually dimorphic voices have higher reproductive success than individuals with less dimorphic voices. However, due to modern birth control methods, these data are rarely described, and mating success is often used as a second-rate proxy. Here, we test whether voice pitch predicts reproductive success, number of children born and child mortality in an evolutionarily relevant population of hunter-gatherers. While we find that voice pitch is not related to reproductive outcomes in women, we find that men with low voice pitch have higher reproductive success and more children born to them. However, voice pitch in men does not predict child mortality. These findings suggest that the association between voice pitch and reproductive success in men is mediated by differential access to fecund women. Furthermore, they show that there is currently selection pressure for low-pitch voices in men.     

Familiarity breeds progeny: sociality increases reproductive success in adult male ring-tailed coatis (Nasua nasua)

The ring-tailed coati (Nasua nasua) is the only coati species in which social groups contain an adult male year round, although most males live solitarily. We compared reproductive success of group living and solitary adult male coatis to determine the degree to which sociality affects reproductive success. Coati mating is highly seasonal and groups of female coatis come into oestrus during the same 1-2 week period. During the mating season, solitary adult males followed groups and fought with the group living male. This aggression was presumably to gain access to receptive females. We expected that high reproductive synchrony would make it difficult or impossible for the one group living male to monopolize and defend the group of oestrous females. However, we found that group living males sired between 67-91% of the offspring in their groups. This reproductive monopolization is much higher than other species of mammals with comparably short mating seasons. Clearly, living in a group greatly enhanced a male's reproductive success. At the same time, at least 50% of coati litters contained offspring sired by extra-group males (usually only one offspring per litter); thus, resident males could not prevent extra-group matings. The resident male's reproductive advantage may reflect female preference for a resident male strong enough to fend off competing males.     

Multiple paternity in an aggregate breeding amphibian: the effect of reproductive skew on estimates of male reproductive success

Aggregate, or explosive, breeding is widespread among vertebrates and likely increases the probability of multiple paternity. We assessed paternity in seven field-collected clutches of the explosively breeding spotted salamander (Ambystoma maculatum) using 10 microsatellite loci to determine the frequency of multiple paternity and the number of males contributing to a female's clutch. Using the Minimum Method of allele counts, multiple paternity was evident in 70% of these egg masses. Simple allele counts underestimate the number of contributing males because this method cannot distinguish multiple fathers with common or similar alleles. Therefore, we used computer simulations to estimate from the offspring genotypes the most likely number of contributing fathers given the distributions of allele frequencies in this population. We determined that two to eight males may contribute to A. maculatum clutches; therefore, multiple paternity is a common strategy in this aggregate breeding species. In aggregate mating systems competition for mates can be intense, thus differential reproductive success (reproductive skew) among males contributing to a female's clutch could be a probable outcome. We use our data to evaluate the potential effect of reproductive skew on estimates of the number of contributing males. We simulated varying scenarios of differential male reproductive success, ranging from equal contribution to high reproductive skew among contributing sires in multiply sired clutches. Our data suggest that even intermediate levels of reproductive skew decrease confidence substantially in estimates of the number of contributing sires when parental genotypes are unknown.     

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 mating success, reproductive success and multiple paternity in a natural population of sand lizards: behavioural and molecular genetics data

Sand lizard Lacerta agilis females characteristically mate with several males which, in staged mating experiments, results in multiple paternity of the offspring. In order to investigate multiple paternity in a natural population and interpret male reproductive behaviours in terms of sired young, we sampled the blood of females, potential fathers and hatchlings, and determined paternity using multilocus DNA fingerprinting as well as the variation at a single locus detected by the probe (TC) _n . The paternity analyses were preceded by a laboratory experiment in which we established that the parental alleles identified by the single locus probe were inherited in a Mendelian way. Our molecular data demonstrated that 12 out of 13 males (92%) that sired offspring were correctly identified from the 56 sexually mature males in the population. Also smaller males were accepted as sexual partners by the females, but sired fewer young in competition with larger males and were less able to maintain prolonged post-copulatory mate guarding. This may result in that some sexually successful males are only observed inside a female's home range, but never in pair-association with the female.     

Determinants of reproductive success across sequential episodes of sexual selection in a firefly

Because females often mate with multiple males, it is critical to expand our view of sexual selection to encompass pre-, peri- and post-copulatory episodes to understand how selection drives trait evolution. In Photinus fireflies, females preferentially respond to males based on their bioluminescent courtship signals, but previous work has shown that male paternity success is negatively correlated with flash attractiveness. Here, we experimentally manipulated both the attractiveness of the courtship signal visible to female Photinus greeni fireflies before mating and male nuptial gift size to determine how these traits might each influence mate acceptance and paternity share. We also measured pericopulatory behaviours to examine their influence on male reproductive success. Firefly males with larger spermatophores experienced dual benefits in terms of both higher mate acceptance and increased paternity share. We found no effect of courtship signal attractiveness or pericopulatory behaviour on male reproductive success. Taken together with previous results, this suggests a possible trade-off for males between producing an attractive courtship signal and investing in nuptial gifts. By integrating multiple episodes of sexual selection, this study extends our understanding of sexual selection in Photinus fireflies and provides insight into the evolution of male traits in other polyandrous species.     

Extreme polygyny among southern elephant seals on Sea Lion Island, Falkland Islands

Elephant seals are known from long-term behavioral studies tobe highly polygynous and to show high variance in reproductivesuccess among males. However, genetic studies have determinedthat the level of polygyny varies between the closely relatednorthern and southern elephant seals. In the present study,we investigate paternal success at the Sea Lion Island southernelephant seal colony in the Falkland Islands by using both behavioralmeasures and genetic markers. We find that the average successof harem holding males at Sea Lion Island is significantly higherthan both the northern species and the nearby southern elephantseal population at Punta Delgada. We compare genetic paternitywith various behavioral indices of male mating success, andwe find that the behavioral measures provide a good estimateof the variance in male reproductive success. Only 28.2% ofmales achieved paternities, and among these, harem holders accountedfor 89.6%. We discuss the implications of our results in thecontext of the demographic and physical environment. Specifically,a comparatively high variance in resource holding potentialamong males, differences in male social behavior, and a smalltidal cycle limiting peripheral male access during female departurefrom the harem at this colony may be important factors leadingto the comparatively high variance in male reproductive successat Sea Lion Island.     

Movement and reproductive behavior of solitary male redtail guenons (Cercopithecus ascanius)

Adult male redtail guenons (Cercopithecus ascanius) live as resident males in heterosexual groups or as nonresident males outside groups. Data are reported here on movement and temporary intrusions by nonresident males in heterosexual groups. These data further elucidate the reproductive strategies of this class of individual. Observations of three radiocollared males provided data on the details of their movement relative to groups. Regular sampling of three heterosexual groups provided data on patterns of nonresident males' intrusions. During peak mating months, nonresident males formed loose affiliations with groups. The males affiliated with one group at a time, with each affiliation lasting several weeks. Nonresident male intrusions in groups were unevenly distributed and were not correlated with the number of potentially fertile females in each group. Estimates of male density indicate that there were about two nonresident males per group, which suggests an adult sex ratio of three females per male within the study area. Nonresident male redtail guenons apparently do not spread their reproductive efforts over several groups at once, but instead each male tends to direct his attention toward the group offering the best opportunity for reproductive payoffs. Factors that determine which groups they attempt to infiltrate may include the characteristics of resident males, female choice, or both, but the number of fertile females probably has no effect. The male low density and female-biased sex ratio among adults should facilitate resident males' attempts to monopolize fertilizations in groups; however, resident males were unable to prevent copulations by nonresident males even when only one nonresident was intruding in a group.     

Puddling in butterflies: sodium affects reproductive success in Thymelicus lineola*

ABSTRACT. Adults of many species of Lepidoptera, principally the males, frequent mud puddles, edges of streams, carrion and animal excreta where they imbibe moisture, an activity referred to as 'puddling' Sodium ions are the only known stimulus present which cause males of at least two lepidopteran species to drink for extended periods. In the European skipper Thymelicus lineola (Ochsenheimer) (Lepidoptera: Hesperiidae), only males puddle, even though they have concentrations of abdominal sodium 2–3 times that of females at emergence. During their first mating, males transfer 32% of their abdominal sodium to females. This could be of considerable importance given that an average egg complement contains >50% of the total body sodium of females at emergence. Virgin females, as well as having reduced fecundity, have reduced longevity. This is attributed to virgins not obtaining important nutrients which males transfer to females during mating. Access to sodium ions increases the total number of matings by c. 50% for males living >15 days. Access to sodium ions by once-mated males increases the percentage of males which re-mate on the day following first mating; the percentage of females, mated to the twice-mated males, which lay >50% fertile eggs; and the drought resistance of eggs laid by those females.     

Effects of fine‐scale genetic structure on male mating success in gynodioecious Beta vulgaris ssp. maritima

Plant mating systems are known to influence population genetic structure because pollen and seed dispersal are often spatially restricted. However, the reciprocal outcomes of population structure on the dynamics of polymorphic mating systems have received little attention. In gynodioecious sea beet (Beta vulgaris ssp. maritima), three sexual types co‐occur: females carrying a cytoplasmic male sterility (CMS) gene, hermaphrodites carrying a non‐CMS cytoplasm and restored hermaphrodites that carry CMS genes and nuclear restorer alleles. This study investigated the effects of fine‐scale genetic structure on male reproductive success of the two hermaphroditic forms. Our study population was strongly structured and characterized by contrasting local sex‐ratios. Pollen flow was constrained over short distances and depended on local plant density. Interestingly, restored hermaphrodites sired significantly more seedlings than non‐CMS hermaphrodites, despite the previous observation that the former produce pollen of lower quality than the latter. This result was explained by the higher frequency of females in the local vicinity of restored (CMS) hermaphrodites as compared to non‐CMS hermaphrodites. Population structure thus strongly influences individual fitness and may locally counteract the expected effects of selection, suggesting that understanding fine scale population processes is central to predicting the evolution of gender polymorphism in angiosperms.     

The association between rank and reproductive success of male rhesus monkeys

The paternity of 202 of 220 offspring of rhesus monkeys housed in six separate half-acre field cages at the California Primate Research Center was determined by genetic marker techniques. Reproductive success of the adult males was statistically significantly correlated (r = 0.76, P <0.0005) with rank. Marked systematic changes in reproductive success were, however, observed for two adult males during the three years covered by this study. Based upon these results and those of another study, it is argued that changes in rank position typically follow, rather than precede, changes in reproductive success.     

Pronounced reproductive skew in a natural population of green swordtails, Xiphophorus helleri

For many species in nature, a sire's progeny may be distributed among a few or many dams. This poses logistical challenges--typically much greater across males than across females--for assessing means and variances in mating success (number of mates) and reproductive success (number of progeny). Here we overcome these difficulties by exhaustively analyzing a population of green swordtail fish (Xiphophorus helleri) for genetic paternity (and maternity) using a suite of highly polymorphic microsatellite loci. Genetic analyses of 1476 progeny from 69 pregnant females and 158 candidate sires revealed pronounced skews in male reproductive success both within and among broods. These skews were statistically significant, greater than in females, and correlated in males but not in females with mating success. We also compare the standardized variances in swordtail reproductive success to the few such available estimates for other taxa, notably several mammal species with varied mating systems and degrees of sexual dimorphism. The comparison showed that the opportunity for selection on male X. helleri is among the highest yet reported in fishes, and it is intermediate compared to estimates available for mammals. This study is one of a few exhaustive genetic assessments of joint-sex parentage in a natural fish population, and results are relevant to the operation of sexual selection in this sexually dimorphic, high-fecundity species.     

Paternity analysis in Ophiopogon xylorrhizus Wang et Tai (Liliaceae s.l.): selfing assures reproductive success

We assessed the utility of codominant allozyme markers for paternity analysis in natural populations of Ophiopogon xylorrhizus (Liliaceae s. l.) by means of likelihood‐based approach. In the three independent natural stands of 46 individual plants with 354 seeds of O. xylorrhizus (Liliaceae s. l), we assigned 319 seeds to a single individual with the highest LOD score. Among these, 179 seeds had a significant D‐value. An individual (acting either as female or male) mateds with an average of one other individual on average to reproduce, except when it self‐pollinated. If an individual that neither donated pollen to other individuals nor selfed, being strictly a pollen acceptor, the number of offspring produced was half that produced by as many offspring as individuals which both provided and accepted pollen (4.1 vs. 9.5). Significant positive relationships were found in all the three stands between the number of self‐pollen an individual produced and the number of seeds that individual set. Male outcrossing reproductive success was unevenly varied, both in amount and spatial location. The individuals located in the centre of the stand and the individuals closest to each other had higher male outcrossing reproductive success than those at the edge of the stand. Male selfing reproductive success showed a similar pattern, with an even distribution of female reproductive output. Most mating events were took place within 20 m. The distance between mates mirrored the active ranges of pollinators, and shaped the fine‐scale population spatial genetic spatial structure. The results indicate that selfing assures reproductive success in O. xylorrhizus.     

Mating system variation and morph fluctuations in a polymorphic lizard

In polymorphic male painted dragon lizards (Ctenophorus pictus), red males win staged contests for females over yellow males, and yellow males have greater success in staged sperm competition trials than red males. This predicts different reproductive strategies in the wild with red males being more coercive or better mate guarders than yellow males. Yellow males would be expected to sire more offspring per copulation and have a greater proportion of offspring from clutches with mixed paternity. However, here we show using microsatellites that the frequency of mixed paternity in the wild is low (< 20% on average across years), that all morphs on average have the same number of offspring sired per year, and that mating system variation (polyandry vs. monandry) is strongly correlated with perch density on male territories. Furthermore, a logistic regression on male successful vs. unsuccessful mate acquisition showed that red males were under negative selection when they dominated the population, which suggests ongoing frequency dependent selection on male colouration.