Successful Sires Research Articles

Paternity success for resident and non-resident males and their influences on paternal sibling cohorts in Japanese macaques (Macaca fuscata) on Shodoshima Island

Reproductive success can be attributed to both resident and non-resident males in non-human primates. However, reproductive success of non-resident males has rarely been investigated at an individual level. As resident males achieve different degree of reproductive success with regard to various factors, such as male dominance relationships or female mate choice, the degree of reproductive success for non-resident males may vary between individuals. As male reproductive success is highly skewed towards specific individuals, the percentage of similar-aged paternal siblings within groups is expected to increase. However, the extent to which each male contributes to the production of cohorts of paternal siblings remains unclear. Here we examined the paternity of offspring born over five consecutive years in a free-ranging group of Japanese macaques Macaca fuscata on Shodoshima Island, Kagawa Prefecture. Genotypes of 87 individuals at 16 autosomal microsatellite loci were analyzed and paternity of 34 offspring was successfully assigned to a single candidate father. We quantitatively assessed paternity success for resident and a few non-resident males whose genetic samples were successfully collected. We quantitatively assessed the percentages of paternal siblings in the same age cohorts produced by those males. Non-resident males sired similar percentage of offspring compared to resident males. A large prime-aged non-resident male was the most successful sire among males in two of the five years. These results provide new insights that male reproductive success could be highly skewed toward a specific non-resident male. Subadult males had a lower percentage of paternity success, which may be because females may prefer physically mature males. Various males, including non-resident males, contributed to the creation of paternal sibling in the same age cohort. The overall results highlighted that not only resident but also non-resident males play an important role in shaping within-group kin structures.

Reproductive success of Bornean orangutan males: scattered in time but clustered in space

The social and mating systems of orangutans, one of our closest relatives, remain poorly understood. Orangutans (Pongo spp.) are highly sexually dimorphic and females are philopatric and maintain individual, but overlapping home ranges, whereas males disperse, are non-territorial and wide-ranging, and show bimaturism, with many years between reaching sexual maturity and attaining full secondary sexual characteristics (including cheek pads (flanges) and emitting long calls). We report on 21 assigned paternities, among 35 flanged and 15 unflanged, genotyped male Bornean orangutans (Pongo pygmaeus wurmbii), studied from 2003 to 2018 in Tuanan (Central Kalimantan, Indonesia). All 10 infants born since mid-2003 with an already identified sire were sired by flanged males. All adult males ranged well beyond the study area (c. 1000 ha), and their dominance relations fluctuated even within short periods. However, 5 of the 10 identified sires had multiple offspring within the monitored area. Several sired over a period of c. 10 years, which overlapped with siring periods of other males. The long-calling behavior of sires indicated they were not consistently dominant over other males in the area around the time of known conceptions. Instead, when they were seen in the area, the known sires spent most of their time within the home ranges of the females whose offspring they sired. Overall, successful sires were older and more often resident than others.Significance statementIt is difficult to assess reproductive success for individuals of long-lived species, especially for dispersing males, who cannot be monitored throughout their lives. Due to extremely long interbirth intervals, orangutans have highly male-skewed operational sex ratios and thus intensive male-male competition for every conception. Paternity analyses matched 21 immature Bornean orangutans with their most likely sire (only 10 of 50 genotyped males) in a natural population. Half of these identified sires had multiple offspring in the study area spread over periods of at least 10 years, despite frequently ranging outside this area. Dominance was a poor predictor of success, but, consistent with female mating tactics to reduce the risk of infanticide, known “sires” tended to have relatively high local presence, which seems to contribute to the males’ siring success. The results highlight the importance of large protected areas to enable a natural pattern of dispersal and ranging.

Paternal reproductive success drives sex allocation in a wild mammal.

Parents should bias sex allocation toward offspring of the sex most likely to provide higher fitness returns. Trivers and Willard proposed that for polygynous mammals, females should adjust sex-ratio at conception or bias allocation of resources toward the most profitable sex, according to their own body condition. However, the possibility that mammalian fathers may influence sex allocation has seldom been considered. Here, we show that the probability of having a son increased from 0.31 to 0.60 with sire reproductive success in wild bighorn sheep (Ovis canadensis). Furthermore, our results suggest that females fertilized by relatively unsuccessful sires allocated more energy during lactation to daughters than to sons, while the opposite occurred for females fertilized by successful sires. The pattern of sex-biased offspring production appears adaptive because paternal reproductive success reduced the fitness of daughters and increased the average annual weaning success of sons, independently of maternal allocation to the offspring. Our results illustrate that sex allocation can be driven by paternal phenotype, with profound influences on the strength of sexual selection and on conflicts of interest between parents.

Multiple mating and offspring quality in Lasius ants

Genetic diversity benefits for social insect colonies headed by polyandrous queens have received intense attention, whereas sexual selection remains little explored. Yet mates of the same queen may engage in sperm competition over the siring of offspring, and this could confer benefits on queens if the most successful sire in each colony (the majority sire) produces gynes (daughter queens) of higher quality. These benefits could be increased if high-quality sires make queens increase the percentage of eggs that they fertilize (unfertilized eggs develop into sons in social hymenopterans), or if daughters of better genetic quality are over-represented in the gyne versus worker class. Such effects would lead to female-biased sex ratios in colonies with high-quality majority gynes. I tested these ideas in field colonies of Lasius niger black garden ants, using body mass of gynes as a fitness trait as it is known to correlate with future fecundity. Also, I established the paternity of gynes through microsatellite DNA offspring analyses. Majority sires did not always produce heavier gynes in L. niger, but whenever they did do so colonies produced more females, numerically and in terms of the energetic investment in female versus male production. Better quality sires may be able to induce queens to fertilize more eggs or so-called caste shunting may occur wherever the daughters of better males are preferentially shunted to into the gyne caste. My study supports that integrating sexual selection and social evolutionary studies may bring a deeper understanding of mating system evolution in social insects.

Testing the priority-of-access model in a seasonally breeding primate species

In mammals, when females are clumped in space, male access to receptive females is usually determined by a dominance hierarchy based on fighting ability. In polygynandrous primates, as opposed to most mammalian species, the strength of the relationship between male social status and reproductive success varies greatly. It has been proposed that the degree to which paternity is determined by male rank decreases with increasing female reproductive synchrony. The priority-of-access model (PoA) predicts male reproductive success based on female synchrony and male dominance rank. To date, most tests of the PoA using paternity data involved nonseasonally breeding species. Here, we examine whether the PoA explains the relatively low reproductive skew in relation to dominance rank reported in the rhesus macaque, a strictly seasonal species. We collected behavioral, genetic, and hormonal data on one group of the free-ranging population on Cayo Santiago (Puerto Rico) for 2 years. The PoA correctly predicted the steepness of male reproductive skew, but not its relationship to male dominance: the most successful sire, fathering one third of the infants, was high but not top ranking. In contrast, mating success was not significantly skewed, suggesting that other mechanisms than social status contributed to male reproductive success. Dominance may be less important for paternity in rhesus macaques than in other primate species because it is reached through queuing rather than contest, leading to alpha males not necessarily being the strongest or most attractive male. More work is needed to fully elucidate the mechanisms determining paternity in rhesus macaques.

Female mouthbrooders in control of pre- and postmating sexual selection

The fertilization mode determines which sex has greater control over the offspring’s sires. With internal fertilization, females can strongly influence the chances of different males’ ejaculates to fertilize their eggs by the postmating sexual selection process referred to as cryptic female choice. In contrast, when fertilization is external and multiple males compete in this process, the outcome of pre- and postmating sexual selection is largely determined by the competitive quality of males and their sperm. Intermediate modes of fertilization as found in mouthbrooding fishes might allow for a greater maternal influence on her offspring’s sire. Here, we show that in the maternal mouthbrooder Ophthalmotilapia ventralis, females collect sperm from different males in their mouth, and males can successfully fertilize eggs even if the female did not lay eggs with them. In the field, 25 of 30 clutches had multiple sires, and the fertilization success was significantly biased toward particular males in most clutches. A mate choice experiment revealed that females prefer to spawn with males possessing strongly elongated pelvic fins, a conspicuous secondary sexual character of males in this cichlid. Additionally, the body length of males partly explained their success in sperm competition within the females’ mouth, a factor without apparent influence on female choice of partners with which to lay eggs. Hence, successful sires are determined by a 2-step process that is largely under female control; females select which males to spawn with and from which males they collect additional ejaculates for the subsequent sperm competition in their mouth.

Mating system in a gopher tortoise population established through multiple translocations: Apparent advantage of prior residence

Population manipulations such as translocation are becoming increasingly important tools in the management of rare and declining species. Evaluating the effectiveness of such manipulations requires comprehensive monitoring of population processes, including dispersal, survivorship, and reproduction. We investigated the mating system of a translocated population of gopher tortoises ( Gopherus polyphemus) established through multiple releases, which occurred primarily during 1987–1994. During 2006–2007, we sampled and genotyped 27 candidate males (candidate sires), 34 candidate females (candidate dams), and 121 offspring from 19 clutches at five polymorphic microsatellite loci to determine the relative frequency of multiple paternity and to estimate individual reproductive success. Multiple paternity was detected in 57% of clutches genotyped, and females of single-sire clutches and females of multiple-sire clutches were of similar size. Reproductive success varied among male tortoises, and successful sires were significantly larger than males to which no offspring were attributed. Among successful sires, previously established males sired a disproportionate number of the offspring sampled, despite being significantly smaller than subsequently released males. The high variance in individual reproductive success and the apparent reproductive advantage associated with prior residence observed in this gopher tortoise population has important implications for the design of future translocation projects.

Paternity and social rank in wild chimpanzees (Pan troglodytes) from the Budongo Forest, Uganda

We analyzed patterns of paternity and male dominance rank in the Sonso community of wild East African chimpanzees (Pan troglodytes schweinfurthii) in the Budongo Forest, Uganda. Our major objective was to determine whether and how social rank influenced paternity success. We successfully genotyped 52 individuals at up to nine microsatellite loci, using DNA extracted from fecal samples. Of 24 offspring analyzed, we identified sires for 21. Paternity success was significantly correlated with social rank, with alpha males siring a disproportionate number of offspring. However, both middle- and low-ranking males also fathered offspring, and the priority-of-access model provided a relatively poor prediction of which males would be successful and under what circumstances. The concentration of paternities among only seven males and the tendency for high-ranking males to sire offspring of multiparous females suggest that both individual variation in male quality and the resource value of particular females may be mediating factors. In comparison with other chimpanzee studies, our results support the hypothesis that larger male cohort size reduces the ability of the alpha male to monopolize females, though within our study, male number did not affect the success of the alpha. Successful sires were not necessarily those who achieved the highest mating success with the females whose offspring they sired, but were those who demonstrated higher investment by spending significantly more time in association with these females. Finally, we estimate extra-group paternity at 0-5%, supporting other evidence that the community serves as the primary reproductive unit in chimpanzees.

Age- and tactic-related paternity success in male African elephants

Information on age- and tactic-related paternity success is essential for understanding the lifetime reproductive strategy of males and constitutes an important component of the fitness trade-offs that shape the life-history traits of a species. The degree of reproductive skew impacts the genetic structure of a population and should be considered when developing conservation strategies for threatened species. The behavior and genetic structure of species with large reproductive skew may be disproportionately impacted by anthropogenic actions affecting reproductively dominant individuals. Our results on age- and tactic-specific paternity success in male African elephants are the first from a free-ranging population and demonstrate that paternity success increases dramatically with age, with the small number of older bulls in the competitive state of musth being the most successful sires. However, nonmusth males sired 20% of genotyped calves, and 60% of mature bulls (.20 years old) were estimated to have sired offspring during the 5-year study period. The 3 most successful males sired less than 20% of the genotyped offspring. Hence, contrary to prediction from behavior and life-history traits, reproduction was not heavily skewed compared with many other mammalian systems with a similar breeding system. Nevertheless, these results indicate that trophy hunting and ivory poaching, both of which target older bulls, may have substantial behavioral and genetic effects on elephant populations. In addition, these results are critical to the current debate on methods for managing and controlling increasing populations of this species. Key words: Eelephants, musth, paternity, reproductive strategy, skew, tactic. [Behav Ecol]

Genetic relatedness of mates does not predict patterns of parentage in North American red squirrels

Previously limited to laboratory studies, the deleterious effects of inbreeding are now being revealed in a number of wild systems. Female North American red squirrels, Tamiasciurus hudsonicus, show high levels of multimale mating and little to no overt precopulatory mate selection. We hypothesized that the negative repercussions of inbreeding should select for a female's ability to select sperm from more distantly related males. Consequently, successful sires should be less genetically related to the female than are unsuccessful males. We tested this hypothesis using both an analysis of absolute success among all copulating males and also relative success of sires within multiply sired litters. Pairwise genetic relatedness and paternity were determined through molecular analysis of tissue samples collected from reproductive females, copulating males and resultant offspring. In contrast to other systems, we found no evidence that the genetic similarity of mates predicts patterns of parentage in red squirrels. Genetic relatedness did not predict whether a copulating male would sire any offspring, and relative success of sires within multiply sired litters was unrelated to their relatedness to the dam of the litter. Furthermore, selection for inbreeding avoidance mechanisms may be minimal, as there were no observable negative fitness repercussions to inbreeding. We detected no relationship between the genetic relatedness of an offspring's parents and its neonatal mass, growth rate or survival to reproductive age. In red squirrels, we found no evidence of parentage patterns based on genetic similarity of mates, and this phenomenon may be less universal than previously thought.

Extra–pair mating, male plumage coloration and sexual selection in yellow warblers (Dendroica petechia)

Extra-pair mating has been proposed as a source of sexual selection responsible for secondary sexual traits that are common among socially monogamous birds, although supporting evidence is scant. In the socially monogamous yellow warbler, males are larger than females, and unlike females, have extensive reddish streaking on their breasts. Using DNA fingerprinting we show that within-pair parentage was positively related to male size, and that extra-pair mating success was positively related to the amount of streaking on the breast. To our knowledge, this is the first intraspecific evidence of an association between a male plumage ornament and gains of extra-pair paternity that is apparently independent of age. This study confirms that extra-pair mating can be an important mechanism of sexual selection even when the most successful sires are commonly cuckolded, and refutes a previous hypothesis that the variation in plumage and behaviour among male yellow warblers is an example of alternative, equally successful, evolutionarily stable strategies (ESS). More generally, the demonstrated independence of within-pair and extra-pair success and their associated traits indicates that where animals have multiple secondary sexual traits, different traits may be selected by different mechanisms that contribute to total reproductive success.