Low Paternity Research Articles

Low extrapair paternity observed in a tropical bird despite ample opportunities for extrapair mating

Abstract. The occurrence of extrapair paternity (EPP) in socially monogamous species varies greatly among species and across latitudes. Recent work suggests that birds residing in less seasonal, tropical environments will have lower levels of EPP than seasonal tropical and temperate species. Less seasonal tropical birds are predicted to have the lowest rates of EPP because their presumed low breeding densities and low breeding synchrony may reduce the opportunities for extrapair mating, and their potentially higher adult survival and longer-term pair bonds may increase the costs of retaliation by males, resulting in reduced paternal care. Nevertheless, the limited number of studies in tropical regions impedes our understanding of whether EPP varies across environments and why. We report on rates of EPP and the potential underlying mechanisms for the observed rate in the Black-crowned Antshrike (Thamnophilus atrinucha, previously known as the Western Slaty Antshrike), a Neotropical and socially monogamous ...

The impact of paternity on male–infant association in a primate with low paternity certainty

In multimale groups where females mate promiscuously, male-infant associations have rarely been studied. However, recent studies have shown that males selectively support their offspring during agonistic conflicts with other juveniles and that father's presence accelerates offspring maturation. Furthermore, it was shown that males invest in unrelated infants to enhance future mating success with the infant's mother. Hence, infant care might provide fitness gain for males. Here, we investigate male-infant associations in rhesus macaques (Macaca mulatta), a primate with low paternity certainty as females mate with multiple partners and males ensure paternity less efficiently through mate-guarding. We combined behavioural data with genetic paternity analyses of one cohort of the semi-free-ranging population of Cayo Santiago (Puerto Rico) and recorded affiliative and aggressive interactions between focal subjects and adult males from birth to sexual maturation (0-4years) of focal subjects. Our results revealed that 9.6% of all interactions of focal subjects involved an adult male and 94% of all male-infant interactions were affiliative, indicating the rareness of male-infant aggression. Second and most interestingly, sires were more likely to affiliate with their offspring than nonsires with unrelated infants. This preference was independent of mother's proximity and emphasized during early infancy. Male-infant affiliation rose with infant age and was pronounced between adult males and male rather than female focal subjects. Overall, our results suggest that male-infant affiliation is also an important component in structuring primate societies and affiliation directed towards own offspring presumably represent low-cost paternal care.

Divergence in genital morphology may contribute to mechanical reproductive isolation in a millipede

Genitalia appear to evolve rapidly and divergently in taxa with internal fertilization. The current consensus is that intense directional sexual selection drives the rapid evolution of genitalia. Recent research on the millipede Antichiropus variabilis suggests that the male genitalia are currently experiencing stabilizing selection – a pattern of selection expected for lock-and-key structures that enforce mate recognition and reproductive isolation. Here, we investigate how divergence in genital morphology affects reproductive compatibility among isolated populations of A. variabilis. Females from a focal population were mated first to a male from their own population and, second, to a male from one of two populations with divergent genital morphology. We observed variation in mating behavior that might indicate the emergence of precopulatory reproductive barriers: males from one divergent population took significantly longer to recognize females and exhibited mechanical difficulty in genital insertion. Moreover, we observed very low paternity success for extra-population males who were successful in copulating. Our data suggest that divergence in genital shape may be contributing to reproductive isolation, and incipient speciation among isolated populations of A. variabilis.

Promiscuity and elongated sperm storage organs work cooperatively as a cryptic female choice mechanism in an earwig

Female genitalia often show complex morphologies that cannot be explained by sperm reception and storage functions. However, our understanding of the forces underlying genital exaggeration in females is limited. Female earwigs, Euborellia plebeja , are promiscuous and their highly elongated sperm storage organs allow only partial removal and displacement of stored sperm by shorter male genitalia, resulting in only a 20% gain in paternity per copulation with a sperm-saturated female. This study examined the significance and optimality of restricted sperm displacement for females. A staged mating experiment with a paternity success analysis revealed that large males dominated male–male competition for burrows housing females, resulting in repeated copulations with the same female. Despite the low paternity gain per copulation, such repeated copulations resulted in a significant increase in paternity for larger males with higher resource-holding potential. A numerical simulation based on the relationship between male body size and copulation frequency showed that restricted sperm displacement (about 20% per copulation) is optimal for promiscuous females to accumulate sperm effectively from larger males. Because male body size is heritable in this species, females were estimated to benefit from a 1.4% increase in their sons' mating success. This genetic benefit disappeared when only a single copulation per male–female encounter was assumed. Since no measurable costs of mating for females have been detected in this species, the combination of promiscuity and restricted sperm displacement is best explained by the cryptic female choice hypothesis.

High degree of paternity loss in a species with alternative reproductive tactics

In many mating systems, males adopt alternative reproductive tactics (ARTs) to maximize reproductive success. In fishes, guarding males often invest more energy into courtship, defense, and paternal care, whereas cuckolding males forego such costs and steal fertilizations by releasing their sperm in the nest of a guarding male. These two tactics have been documented in the plainfin midshipman fish (Porichthys notatus), yet the relative reproductive success of the guarding and cuckolding male tactics remains unknown. In this study, we used microsatellite markers to determine the level of paternity of the guarding type I males. We explored how paternity varied with male phenotype and across the breeding season. Our results revealed the lowest documented levels of paternity in a species with obligate paternal care. Although paternity remained consistently low, it did increase as the breeding season progressed. Male body size did not significantly predict paternity. The low paternity in this species may be explained, in part, by aspects of their reproductive ecology including the duration of parental care period, limited nest availability and competition for nests, as well as the occurrence of nest takeovers. Overall, our findings contribute to the understanding of the ultimate factors underlying ARTs in this species and highlight the importance of investigating reproductive success across the entire breeding season.

Paternal effects on access to resources in a promiscuous primate society

The evolution of paternal care is rare in promiscuous mammals, where it is hampered by low paternity confidence. However, recent evidence indicates that juveniles whose fathers are present experience accelerated maturation in promiscuous baboon societies. The mechanisms mediating these paternal effects remain unclear. Here, we investigated whether father–offspring associations might facilitate offspring access to resources in wild desert baboons (Papio ursinus). We combined paternity analyses and behavioral observations of juveniles that had started feeding autonomously to show that (1) offspring associate more often with their genetic father than with any other male, and actively manage such associations, (2) offspring associate more closely with their father when another adult male is in sight, and when their mother is out of sight, (3) father–offspring associations are more frequent when juveniles are feeding (relative to other activities), and these associations enable juveniles to access richer food patches, and (4) father–offspring associations are stronger among subordinate males and their offspring. Taken together, these findings indicate that fathers may buffer the social and ecological environment faced by their offspring. In addition to mitigating risks of attacks by predators or conspecifics, paternal presence improves offspring access to food in wild baboons, highlighting a new mechanism through which fathers may impact offspring fitness in promiscuous primate societies. Key wor ds: baboons, foraging success, paternal care, primates, promiscuity , reproductive strategies, sex roles. [Behav Ecol]

Exclusive male care despite extreme female promiscuity and low paternity in a marine snail

Males exhibit striking variation in the degree to which they invest in offspring, from merely provisioning females with sperm, to providing exclusive post-zygotic care. Paternity assurance is often invoked to explain this variation: the greater a male's confidence of paternity, the more he should be willing to provide care. Here, we report a striking exception to expectations based on paternity assurance: despite high levels of female promiscuity, males of a marine snail provide exclusive, and costly, care of offspring. Remarkably, genetic paternity analyses reveal cuckoldry in all broods, with fewer than 25% of offspring being sired by the caring male, although caring males sired proportionally more offspring in a given clutch than any other fathers did individually. This system presents the most extreme example of the coexistence of high levels of female promiscuity, low paternity, and costly male care, and emphasises the still unresolved roles of natural and sexual selection in the evolution of male parental care.

PATTERNS OF PATERNITY SKEW AMONG POLYANDROUS SOCIAL INSECTS: WHAT CAN THEY TELL US ABOUT THE POTENTIAL FOR SEXUAL SELECTION?

Monogamy results in high genetic relatedness among offspring and thus it is generally assumed to be favored by kin selection. Female multiple mating (polyandry) has nevertheless evolved several times in the social Hymenoptera (ants, bees, and wasps), and a substantial amount of work has been conducted to understand its costs and benefits. Relatedness and inclusive fitness benefits are, however, not only influenced by queen mating frequency but also by paternity skew, which is a quantitative measure of paternity biases among the offspring of polyandrous females. We performed a large-scale phylogenetic analysis of paternity skew across polyandrous social Hymenoptera. We found a general and significant negative association between paternity frequency and paternity skew. High paternity skew, which increases relatedness among colony members and thus maximizes inclusive fitness gains, characterized species with low paternity frequency. However, species with highly polyandrous queens had low paternity skew, with paternity equalized among potential sires. Equal paternity shares among fathers are expected to maximize fitness benefits derived from genetic diversity among offspring. We discuss the potential for postcopulatory sexual selection to influence patterns of paternity in social insects, and suggest that sexual selection may have played a key, yet overlooked role in social evolution.

Low paternity skew and the influence of maternal kin in an egalitarian, patrilocal primate

Levels of reproductive skew vary in wild primates living in multimale groups depending on the degree to which high-ranking males monopolize access to females. Still, the factors affecting paternity in egalitarian societies remain unexplored. We combine unique behavioral, life history, and genetic data to evaluate the distribution of paternity in the northern muriqui (Brachyteles hypoxanthus), a species known for its affiliative, nonhierarchical relationships. We genotyped 67 individuals (22 infants born over a 3-y period, their 21 mothers, and all 24 possible sires) at 17 microsatellite marker loci and assigned paternity to all infants. None of the 13 fathers were close maternal relatives of females with which they sired infants, and the most successful male sired a much lower percentage of infants (18%) than reported for the most successful males in other species. Our findings of inbreeding avoidance and low male reproductive skew are consistent with the muriqui's observed social and sexual behavior, but the long delay (≥2.08 y) between the onset of male sexual behavior and the age at which males first sire young is unexpected. The allocation of paternity implicates individual male life histories and access to maternal kin as key factors influencing variation in paternal--and grandmaternal--fitness. The apparent importance of lifelong maternal investment in coresident sons resonates with other recent examinations of maternal influences on offspring reproduction. This importance also extends the implications of the "grandmother hypothesis" in human evolution to include the possible influence of mothers and other maternal kin on male reproductive success in patrilocal societies.

Mating opportunities, paternity, and sexual conflict: paternal care in northern and southern temperate house wrens

Males are generally predicted to care less for their young when they have more additional mating opportunities, lower paternity, or when their mates care more. We tested these predictions using male provisioning as a proxy for paternal care in two temperate populations of house wrens (Troglodytes aedon) with divergent life histories. Males in the migratory, occasionally socially polygynous New York, USA (northern) population provisioned less when more local females were fertile. A similar relationship was only weakly supported in the resident, socially monogamous Buenos Aires Province, Argentina (southern) population, possibly due to the higher density of house wrens there. A relationship between male provisioning and level of paternity within the brood was supported in both populations, but in opposite directions: while males in the southern population provisioned less at broods containing more extra-pair young, males in the northern population provisioned such broods more, contradicting predictions. Males provisioned less when their mates provisioned more in both populations, in agreement with sexual conflict theory. Additionally, the populations both exhibited a positive relationship between male provisioning and nestling age, but differed in the direction of the relationships of male provisioning with date and brood size. Our results suggest that even within a species, life history differences may be accompanied by differences in the determinants of behavior such as paternal care.

Breaking the rules: sex roles and genetic mating system of the pheasant coucal

Generally in birds, the classic sex roles of male competition and female choice result in females providing most offspring care while males face uncertain parentage. In less than 5% of species, however, reversed courtship sex roles lead to predominantly male care and low extra-pair paternity. These role-reversed species usually have reversed sexual size dimorphism and polyandry, confirming that sexual selection acts most strongly on the sex with the smaller parental investment and accordingly higher potential reproductive rate. We used parentage analyses and observations from three field seasons to establish the social and genetic mating system of pheasant coucals, Centropus phasianinus, a tropical nesting cuckoo, where males are much smaller than females and provide most parental care. Pheasant coucals are socially monogamous and in this study males produced about 80% of calls in the dawn chorus, implying greater male sexual competition. Despite the substantial male investments, extra-pair paternity was unusually high for a socially monogamous, duetting species. Using two or more mismatches to determine extra-pair parentage, we found that 11 of 59 young (18.6%) in 10 of 21 broods (47.6%) were not sired by their putative father. Male incubation, starting early in the laying sequence, may give the female opportunity and reason to seek these extra-pair copulations. Monogamy, rather than the polyandry and sex-role reversal typical of its congener, C. grillii, may be the result of the large territory size, which could prevent females from monopolising multiple males. The pheasant coucal's exceptional combination of classic sex-roles and male-biased care for extra-pair young is hard to reconcile with current sexual selection theory, but may represent an intermediate stage in the evolution of polyandry or an evolutionary remnant of polyandry.

Is multiple mating beneficial or unavoidable? Low multiple paternity and genetic diversity in the shortspine spurdog Squalus mitsukurii

Proposed benefits of multiple paternity include increased reproductive output, elevated fitness of progeny, and maintenance of population genetic diversity. However, another consideration is whether multiple paternity is simply an unavoidable byproduct of sexual conflict, with males seek- ing to maximize mating encounters while females seek to minimize the stress of copulation. Here we examined the polyandrous mating system in sharks, with a focus on the reproductive genetics of the shortspine spurdog Squalus mitsukurii. Members of the genus Squalus are long-lived, slow-growing, and employ among the longest gestation periods of any vertebrate. To evaluate multiple paternity and genetic diversity in S. mitsukurii, we genotyped 27 litters plus 96 individuals with 8 microsatel- lite loci. Further, 670 bp of the mtDNA control region were sequenced in 112 individuals to examine population structure. S. mitsukurii in Hawaii showed low genetic diversity relative to other sharks (π = 0.0010 ± 0.0008) and no significant population structure in the Hawaiian Archipelago. Direct allele counts and Bayesian approximations returned concordant estimates of 11% multiple paternity, the lowest observed in sharks to date. Considering the protracted reproductive interval of S. mitsu- kurii, sexual conflict that results from differential male and female reproductive strategies may favor the development of female mating avoidance behavior to minimize trauma. In S. mitsukurii this behavior includes segregation of sexes and an asynchronous reproductive cycle.

More than friends? Behavioural and genetic aspects of heterosexual associations in wild chacma baboons

In mammals, fathers are facultative caretakers, and male care is expected to evolve only if it is directed towards related young. Yet, in several promiscuous primate societies, males seem to care for infants despite a presumably low paternity confidence. In cercopithecines, cohesive associations (‘friendships’) between a lactating female and an adult male are frequent and provide the female and her infant with protection against various sources of aggression, including infanticide. However, the benefits gained by males through such relationships remain unclear, in part, because the relatedness between males and their protected infants has rarely been examined. Moreover, little is known about the nature of the cues underlying kin discrimination by males in societies where females mate polyandrously. In this study, we combine behavioural and genetic data from wild chacma baboons (Papio ursinus) in Namibia to investigate (1) whether males are related to their friend’s infant and (2) whether similarity between the major histocompatibility complex (MHC) genotype of males and infants (potentially perceived through odour phenotype) favours the establishment of friendships. We first show that males share close genetic ties with their friend’s infants, most often by having sired the infant. Secondly, we find that male–infant MHC (Class II–DRB) similarity, in contrast to paternity, does not predict male–infant associations. Overall, our results clarify the nature of the evolutionary benefits gained by males in these heterosexual associations, which can be considered as true paternal care. However, the proximate mechanisms underlying paternity recognition remain to be identified.

Comparison of contemporary mating patterns in continuous and fragmented Eucalyptus globulus native forests

While habitat fragmentation is a central issue in forest conservation studies in the face of broad-scale anthropogenic changes to the environment, its effects on contemporary mating patterns remain controversial. This is partly because of the inherent variation in mating patterns which may exist within species and the fact that few studies have replication at the landscape level. To study the effect of forest fragmentation on contemporary mating patterns, including effective pollen dispersal, we compared four native populations of the Australian forest tree, Eucalyptus globulus. We used six microsatellite markers to genotype 1289 open-pollinated offspring from paired fragmented and continuous populations on the island of Tasmania and in Victoria on mainland Australia. The mating patterns in the two continuous populations were similar, despite large differences in population density. In contrast, the two fragmented populations were variable and idiosyncratic in their mating patterns, particularly in their pollen dispersal kernels. The continuous populations showed relatively high outcrossing rates (86-89%) and low correlated paternity (0.03-0.06) compared with the fragmented populations (65-79% and 0.12-0.20 respectively). A greater proportion of trees contributed to reproduction in the fragmented (de/d>or= 0.5) compared with the continuous populations (de/d = 0.03-0.04). Despite significant inbreeding in the offspring of the fragmented populations, there was little evidence of loss of genetic diversity. It is argued that enhanced medium- and long-distance dispersal in fragmented landscapes may act to partly buffer the remnant populations from the negative effects of inbreeding and drift.

Queen condition, mating frequency, queen loss, and levels of worker reproduction in the hornets Vespa affinis and V. simillima

Abstract 1. Mature queens of the hornet Vespa affinis are unusual in that they lose all their body hair and wings. This has been used as evidence for matricide in hornets. Factors favouring matricide such as low paternity and long annual lifecycle are present in most hornets.2. We determined paternity in V. affinis and compared queen condition, levels of queen loss, and worker reproduction in 163 V. affinis and 63 V. simillima colonies. These two species have very similar lifecycles and colony sizes, but different paternities (1.3 vs 2.4). Furthermore, in queen‐right V. affinis colonies small proportions (4%) of reproductive workers were present, whereas in queen‐right V. simillima colonies no reproductive workers were detected.3. Despite these differences, queen damage in both species was influenced predominantly by her age and in V. affinis was not influenced by presence of reproductive workers.4. The number of queen‐less V. simillima (9/63 = 14%) and V. affinis (28/163 = 17%) colonies were also not significantly different (P = 0.8). Therefore, queen damage and proportions of queen‐less colonies were not linked making it a poor indicator of matricide.5. It is proposed that graded control of sexual and worker production in wasps and hornets prevents a situation where kin‐selected matricide is ever favoured.

Do male paternity guards ensure female fidelity in a duetting fairy-wren?

Most socially monogamous bird species engage in extra-pair mating, and consequently males may adopt various behavioral strategies to guard paternity. However, the relationship between mate guarding and extra-pair paternity is unclear: low levels of extra-pair paternity can be associated either with no mate guarding or with intense mate guarding. We investigate paternity guards in the purple-crowned fairy-wren (Malurus coronatus), a duetting species where extra-pair paternity is rare. This species is unusual in a genus known for extremely high levels of extra-pair mating. We examine the behavioral interactions between the sexes underlying these low rates of extra-pair paternity and show that male purple-crowned fairy-wrens do not use frequent copulation or courtship feeding to assure paternity or guard females acoustically by duetting. Males maintain close proximity to females both when they are fertile and when they are not breeding and do not invest in courtship displays to extra-pair females. Consistent with predictions of theoretical models, low extra-pair paternity in this species may be related to female fidelity rather than male paternity assurance strategies, but short-term removal of males would be necessary to test this experimentally.

A scientific note on the levels of polyandry in the black dwarf honeybeeApis andreniformisfrom Malaysia

A majority of social Hymenoptera species such as ants, bees and wasps are monandrous or exhibit extremely low paternity frequency. Multiple mating by queens has independently evolved in some species of advanced social Hymenoptera (Boomsma and Ratnieks, 1996). The honeybee belongs to the genus Apis; they display extremely high levels of polyandry, resulting in very low genetic relatedness among workers and decreased potential inclusive fitness. Several researchers have attempted to explain the evolution and maintenance of extreme polyandry in honeybees by several plausible hypotheses such as sperm need, task specialization, sperm selection, reproductive conflict, resistance to parasites and diseases, and curious promiscuity of queens (reviewed by Palmer and Oldroyd, 2000; Tarpy and Page, 2001; Oldroyd and

Use of X‐linked short tandem repeat loci in routine parentage casework

Dealing with genetic inconsistencies in parentage testing, especially in motherless cases, remains a continual difficulty. Four difficult cases, comprising two trios and two duos, were selected from routine parentage testing casework. In these, relatively low combined paternity indices were observed as a result of few discrepant loci that were treated as being due to paternal mutations. An additional eight short tandem repeat (STR) loci along the X chromosome were studied in the alleged father and female child to try and help resolve these cases. In all four cases, the X chromosome haplotypes in the alleged father were different from those in the child, showing decisively that the alleged father could be excluded from being the biologic father of the child. In recent times the study of X chromosome haplotypes has been shown to be useful in parentage testing where the alleged father is absent and where only his close relatives are available for testing. This work demonstrates that such studies can also prove valuable in the testing of standard trios and duos in cases where there only a few genetic inconsistencies amongst the loci tested, making it difficult to distinguish between paternal mutations and a close relative of the alleged father being the biologic father.

Confidence of paternity, divorce, and investment in children by Albuquerque men

Using a sample of men living in Albuquerque, NM, we examined the relationship between paternity confidence and men's investment in children. In humans, men may reduce their investment in a child in two ways: indirectly, by ending their relationship with the child's mother and ceasing to cohabit with the child (e.g., divorce), and directly, by allocating less time and fewer resources to the child. In this article, we tested two hypotheses regarding the effect of paternity confidence on investment in children: (1) men will be more likely to divorce women if they suspect or are sure that they are not the father of their wife's child, and (2) controlling for divorce, men will reduce direct investments in low paternity confidence children relative to high paternity confidence children. The first hypothesis was supported by the data. The second hypothesis was supported for two out of three measures of paternal investment we examined; low paternity confidence reduces the time men spend with a child in a group with other children or adults, and it reduces extensive involvement with the child's educational progress; there was no effect of paternity confidence on the amount of time men spend with children in one-on-one interactions. We also examined the effects of unstated paternity confidence (e.g., when men decline to answer the question) on divorce and paternal investment. Overall, the results suggested that paternity confidence plays an important role in shaping men's relationships with women and with their putative genetic children.

Demographic correlates of paternity confidence and pregnancy outcomes among Albuquerque men

We examine the demographic correlates of paternity confidence, or men's assessment of the likelihood that they are the genetic father of a particular child. Evolutionary theory predicts that men will provide less parental investment for putative genetic offspring who are unlikely to be their actual offspring, but confidence of paternity has not been as extensively examined as its importance would merit. Using self-reported data on paternity confidence in 3,360 pregnancies reported by men living in Albuquerque, New Mexico, we find that low paternity confidence is more common among unmarried couples and for unplanned pregnancies. We also find that men are more likely not to state paternity confidence (i.e., they refuse to answer the question) if a pregnancy is unplanned. We additionally examine the pregnancy outcomes associated with confidence of paternity. We find that low paternity confidence pregnancies are significantly more likely to be aborted, and pregnancies for which paternity confidence is unstated are more likely to be aborted or to miscarry. Both abortion and miscarriage are associated with unmarried couples, with unplanned pregnancies, and with couples who have fewer children together.