Why babies look like their daddies: paternity uncertainty and the evolution of self-deception in evaluating family resemblance

It has been suggested that in a socially monogamous system where fathers invest in their mate's offspring but paternity is far from certain, it will be adaptive on the part of infants to conceal their father's identity; but the opposite claim has also been made that this is against the genetic interests of the fathers, and a high frequency of adulterine births will select instead for paternal resemblance. In this article, I present a simple theoretical model that suggests that neonatal anonymity benefits fathers, mothers, and children. Once anonymity becomes established, however, all babies start paying the cost of paternity uncertainty, that is, the reduction in paternal care due to fathers not knowing whether they have truly sired their mate's offspring. By diminishing the fitness of babies, such a cost bounces back as lowered fitness for parents as well. We should then expect the evolution of maternal strategies directed to decrease paternity uncertainty, in the form of instinctive and unsolicited comments on babies' resemblance to their putative fathers. In contradiction to the widespread belief that it would be in fathers' interest to be skeptical of these allegations, the model suggests that, under conditions of infant anonymity, fathers will actually promote their own fitness by believing their spouses. Received in revised form: 5 September 2001 Electronic Publication     

A retrospective assessment of the accuracy of the paternity inference program CERVUS

CERVUS is a Windows-based software package written to infer paternity in natural populations. It offers advantages over exclusionary-based methods of paternity inference in that multiple nonexcluded males can be statistically distinguished, laboratory typing error is considered and statistical confidence is determined for assigned paternities through simulation. In this study we use a panel of 84 microsatellite markers to retrospectively determine the accuracy of statistical confidence when CERVUS was used to infer paternity in a population of red deer (Cervus elaphus). The actual confidence of CERVUS-assigned paternities was not significantly different from that predicted by simulation.     

Multiple paternity in loggerhead turtle (Caretta caretta) nests on Melbourne Beach, Florida: a microsatellite analysis

Many aspects of sea turtle biology are difficult to measure in these enigmatic migratory species, and this lack of knowledge continues to hamper conservation efforts. The first study of paternity in a sea turtle species used allozyme analysis to suggest multiple paternity in loggerhead turtle (Caretta caretta) clutches in Australia. Subsequent studies indicated that the frequency of multiple paternity varies from species to species and perhaps location to location. This study examined fine-scale population structure and paternal contribution to loggerhead clutches on Melbourne Beach, FL, USA using microsatellite markers. Mothers and offspring from 70 nests collected at two locations were analysed using two to four polymorphic microsatellite loci. Fine-scale population differentiation was not evident between the sampled locations, separated by 8 km. Multiple paternity was common in loggerhead nests on Melbourne Beach; 22 of 70 clutches had more than one father, and six had more than two fathers. This is the first time that more than two fathers have been detected for offspring in individual sea turtle nests. Paternal genotypes could not be assigned with confidence in clutches with more than two fathers, leaving the question of male philopatry unanswered. Given the high incidence of multiple paternity, we conclude that males are not a limiting resource for this central Florida nesting aggregate.     

Exclusions and attributions of paternity: practical experiences of forensic genetics and statistics.

The Swedish State Institute for Blood Group Serology is a central government laboratory handling all blood typing in paternity cases in Sweden, each year testing 1,500-2,000 cases using about 13 polymorphisms. Of the accused men, 35%-40% are nonfathers, but in one-man cases (about 78% of all cases), approximately 75% are the true fathers. Exclusions appear to be distributed as expected from allele frequencies, and the paternity probability of nonexcluded men is assessed with a Bayesian approach. Some cases are retested in extended investigations which raise theoretical exclusion capability from about 87% to about 99%. Both the results of extended investigations and the theoretical consideration of the distribution of paternity probabilities support the use of such positive statistical evidence for the attribution of paternity.     

Some fallacies in the computation of paternity probabilities.

Legal identification of fathers by means of a "paternity probability" has been used in European courts for decades, and has recently been introduced into American courts and accepted by some of them. The voluminous literature on this topic contains virtually no fundamental criticism of the logical basis for the probabilistic computations. Here I suggest that the "paternity probability" suffers from three basic fallacies: (1) contrary to claims, the figure is not, in fact, the probability that the alleged father is the true father, (2) the denominator of the likelihood ratio used in the computation is driven by (sometimes self-contradictory) assumptions and is not based on facts, and (3) post-inclusionary computations are based on speculation about genotypes that does not constitute scientific evidence. It is recommended that pending the resolution of these difficulties "paternity probabilities" should not be computed or introduced as positive evidence of paternity.     

Statistical approaches to paternity analysis in natural populations and applications to the North Atlantic humpback whale

We present a new method for paternity analysis in natural populations that is based on genotypic data that can take the sampling fraction of putative parents into account. The method allows paternity assignment to be performed in a decision theoretic framework. Simulations are performed to evaluate the utility and robustness of the method and to assess how many loci are necessary for reliable paternity inference. In addition we present a method for testing hypotheses regarding relative reproductive success of different ecologically or behaviorally defined groups as well as a new method for estimating the current population size of males from genotypic data. This method is an extension of the fractional paternity method to the case where only a proportion of all putative fathers have been sampled. It can also be applied to provide abundance estimates of the number of breeding males from genetic data. Throughout, the methods were applied to genotypic data collected from North Atlantic humpback whales (Megaptera novaeangliae) to test if the males that appear dominant during the mating season have a higher reproductive success than the subdominant males.     

Empirical validation of the Essen-Möller probability of paternity.

The validity of the Essen-Möller formulation probability of paternity is supported by demonstrating its correctness in a model genetic system--the ABO system. An analysis was made of 1,393 paternity cases typed uniformly for HLA-A and -B, ABO, Rh, and MNSs, in which the mother named one man only as the child''s father and in which both mother and putative father identified themselves as Caucasian. For purposes of analysis, putative fathers not excluded from paternity by the four systems tested were regarded as actual fathers. The joint distribution of observed triplets of ABO phenotypes is shown to be statistically consistent with expected values, and the fractions of "true" fathers for a given triplet closely approximated the probability of paternity calculated using a realistic prior probability. Recent allegations of fallaciousness of the method by Li and Chakravarty and Aickin are discussed in terms of the results presented.     

Pollen flow in the wildservice tree, Sorbus torminalis (L.) Crantz. I. Evaluating the paternity analysis procedure in continuous populations

The joint development of polymorphic molecular markers and paternity analysis methods provides new approaches to investigate ongoing patterns of pollen flow in natural plant populations. However, paternity studies are hindered by false paternity assignment and the nondetection of true fathers. To gauge the risk of these two types of errors, we performed a simulation study to investigate the impact on paternity analysis of: (i) the assumed values for the size of the breeding male population (NBMP), and (ii) the rate of scoring error in genotype assessment. Our simulations were based on microsatellite data obtained from a natural population of the entomophilous wild service tree, Sorbus torminalis (L.) Crantz. We show that an accurate estimate of NBMP is required to minimize both types of errors, and we assess the reliability of a technique used to estimate NBMP based on parent-offspring genetic data. We then show that scoring errors in genotype assessment only slightly affect the assessment of paternity relationships, and conclude that it is generally better to neglect the scoring error rate in paternity analyses within a nonisolated population.     

Social relations between fathers and offspring in a captive group of rhesus monkeys (Macaca mulatta)

Analysis of social relations between adult males and immatures of known paternity in a captive group of rhesus monkeys (Macaca mulatta) revealed that fathers and offspring associated significantly more than other male-immature dyads. This association was highly variable, however, and there was no evidence of active preference for or investment in offspring by fathers. The tendency of offspring to approach fathers more often than other males appeared to account for the pattern of selective association. Preferential father-offspring association occurred whether or not mothers were in proximity to fathers, but mothers' associations with males did predict their offspring's, especially for the younger juveniles and the infants. It is possible that long-term social relationships between mothers and fathers lead to father-offspring association, but a year-to-year pattern of shifting mating preferences in the group weakens this hypothesis.     

Extrapair paternity in the great tit (Parus major): a test of the "good genes" hypothesis

In 1993 and 1994 we determined the frequency of extrapair paternityin broods of great tits, Parus major using multilocus DNA fingerprinting.We found no instances of intraspecific brood parasitism, but40% of broods (31/78) contained extrapair-fathered young and83% of offspring (58/681) were xtrapair We identified the geneticfathers of 60% of the extrapair nestlings (35/ 58). Males withfull and lost paternity did not differ significantly in traitsthat have been suggested to indicate male quality, nor did thegenetic and social fathers of extrapair offspring. In 1993,cuckolded males sired more offspring that recruited to the subsequentbreeding season than males with full paternity. Moreover, eventhough genetic fathers of extrapair young (EPY) sired more fledglingsthan the males they cuckolded, genetic and social fathers ofEPY did not differ in the number of recruits sired. Also, theEPY of a brood did not survive better than their half sibs.Thus, our results do not supportthe hypothesis that femaleschoose better quality males for extrapair matings ("good genes"hypothesis). Further, the level of extrapair paternity differedmarkedly between the two years. Our data show that females areconstrained in their extrapair activities by the availabilityof extrapair mates. This is at least partly due to yearly differencesin breeding synchrony.     

The efficiency of multilocus DNA fingerprint probes for individualization and establishment of family relationships, determined from extensive casework.

The properties of human DNA fingerprints detected by multilocus minisatellite probes 33.6 and 33.15 have been investigated in 36 large sibships and in 1,702 Caucasian paternity cases involving the analysis of over 180,000 DNA fingerprint bands. The degree of overlap of minisatellite loci detected by these two probes is shown to be negligible (approximately 1%), and the resulting DNA fingerprints are therefore derived from independent sets of hypervariable loci. The level of allelism and linkage between different hypervariable DNA fragments scored with these probes is also low, implying substantial statistical independence of DNA fragments. Variation between the DNA fingerprints of different individuals indicates that the probability of chance identity is very low (much less than 10(-7) per probe). Empirical observations and theoretical considerations both indicate that genetic heterogeneity between subpopulations is unlikely to affect substantially the statistical evaluation of DNA fingerprints, at least among Caucasians. In paternity analysis, the proportion of nonmaternal DNA fragments in a child which cannot be attributed to the alleged father is shown to be an efficient statistic for distinguishing fathers from nonfathers, even in the presence of minisatellite mutation. Band-sharing estimates between a claimed parent and a child can also distinguish paternity from nonpaternity, though with less efficiency than comparison of a trio of mother, child, and alleged father.     

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.     

Sexual behaviour and paternity in three captive groups of rhesus monkeys (Macaca mulatta)

Each offspring born into three captive groups of rhesus monkeys (Macaca mulatta) during the spring of 1981 was assigned (1) a most probable behavioural father and (2) a subset of all possible behavioural fathers, on the basis of intensive observations of sexual activity during the 1980 fall breeding season. These predictions were then compared with true paternity determined by electrophoretic and serological analyses of polymorphic blood proteins of mothers, infants, and all adult and subadult males. Coincidence between the assignments of paternity based upon behavioural and biochemical data occurred no more frequently than chance would allow. Furthermore, there were no significant relationships between biochemical and behavioural rankings of overall reproductive success. It was concluded that conventional estimates of sexual activity during the breeding season are not a reliable indicator of true paternity and relative reproductive success in rhesus macaques.     

CORRELATED MATINGS IN THE PARTIAL SELFER MIMULUS GUTTATUS

In partially selfing populations, siblings may be correlated for both selling and paternity. A model of the mating system based upon sampling pairs of progeny from a maternal parent is described. The model separates the correlation of selfing from the correlation of outcrossed paternal alleles and is an approach to paternity analysis suited for larger populations with fewer marker loci. Its parameters determine the components of genetic covariance between sibs and provide information about the average number of fathers in a maternal sibship. Electrophoretic markers were used to obtain estimates of correlated matings for two Mimulus guttatus populations. In both populations, about 50% selfing was observed. For two sibs randomly selected from the same capsule, the correlations of selfing between these sibs were 17% and 12% in the two populations, and the correlations of paternity (the proportion of full-sibs among outcrossed sib-pairs) were 37% and 44%. Sibs from different capsules were not correlated for selfing, and the paternity correlation dropped to near 20% in both populations. However, estimates of correlated matings have high variance, lack statistical independence, and can be difficult to obtain. The use of marker loci with many alleles can alleviate these problems.     

Who's your daddy? Paternity testing reveals promiscuity and multiple paternity in the carnivorous marsupial Dasyurus maculatus (Marsupialia: Dasyuridae)

Female promiscuity is common among mammals but its advantages, particularly for marsupials, remain unclear. Using microsatellite DNA from pouch young of known mothers, we identified the most likely fathers of 25 wild spotted-tailed quolls ( Dasyurus maculatus ) from six litters. We aimed to determine whether young within the same litter had different fathers, and whether breeding success of males was associated with large body mass (consistent with inter-male competition) or scrotal width (consistent with sperm competition). We also explored the possible influence of promiscuity on relatedness within litters. Finally, we used data on paternity and relatedness to make inferences regarding movement and dispersal.
Four litters were sired by more than one male, and three males sired offspring in more than one litter. Known fathers had higher body mass, but not scrotal width, than males of unknown paternity status, suggesting that males may compete for access to females. Sires were less related to dams than expected by chance, and litters with multiple paternity had lower relatedness than litters sired by a single male.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 1–7.     

Microsatellite assessment of multiple paternity in natural populations of a live-bearing fish,Gambusia holbrooki

Three polymorphic microsatellite loci were isolated and employed to examine paternity patterns in two natural populations of live-bearing mosquitofish, Gambusia holbrooki. Each locus displayed four to five alleles per population in samples of presumably unrelated adults. Nearly 900 embryos from a total of 50 pregnant females were assayed individually, and paternal alleles in each embryo were identified. Counts of paternal alleles, Mendelian segregation patterns, multilocus allelic associations and genetic relatedness coefficients were employed to estimate the minimum and effective numbers of fathers per brood. At least 90% of the assayed broods were shown to have been fathered by multiple males, a figure substantially higher than previous estimates based on less polymorphic genetic loci. However, the genetic data yield a face-value estimate of only about 2.2 fathers per brood, a number that seems perhaps surprisingly low based on frequencies of attempted copulations by males. Both biological and sampling factors that might bias mean sire counts downward are considered. Although higher sire counts per brood might be obtained from loci with even greater numbers of alleles, little statistical room remains for higher frequency estimates of multiple paternity in Gambusia.     

When ‘blood speaks’: naming the father and the mystics of kinship in Dominica,Eastern Caribbean

This article explores the mystical implication of fathers in reproduction in Dominica, Eastern Caribbean. It traces naming acts that assign paternity at various points in the filial life course, each attempting to disambiguate paternity. Confronting a recurring anthropological problematic – the problem of paternity (paternity's inherent putativity) – the article argues that Dominicans contest uncertain physical fatherhood through the proverb ‘blood speaks’. The article elaborates how relatedness reveals itself in the subtle bodies of kin at three moments: through a local version of the couvade (‘sympathetic pregnancy’); in elders’ post-partum ritual scrutiny of children's bodies for familial resemblances; and during serendipitous encounters in later life. The article highlights how physical fatherhood is disclosed in fathers’ and children's symptoms, appearances, and sensations, revealing their kinship in transpersonal terms. Therefore, blood ‘speaks’ to counter broad-brushed narratives of Caribbean fatherly absence by revealing the physical and spiritual significance of fatherhood. Herein, the article revives classic anthropological debates on legitimacy, the couvade, and Caribbean kinship, whilst contributing to contemporary theorizations of blood and naming.     

Implications of Advancing Paternal Age: Does It Affect Offspring School Performance?

Average paternal age is increasing in many high income countries, but the implications of this demographic shift for child health and welfare are poorly understood. There is equivocal evidence that children of older fathers are at increased risk of neurodevelopmental disorders and reduced IQ. We therefore report here on the relationship between paternal age and a composite indicator of scholastic achievement during adolescence, i.e. compulsory school leaving grades, among recent birth cohorts in Stockholm County where delayed paternity is notably common. We performed a record-linkage study comprising all individuals in Stockholm County who finished 9 years of compulsory school from 2000 through 2007 (n = 155,875). Data on school leaving grades and parental characteristics were retrieved from administrative and health service registers and analyzed using multiple linear regression. Advancing paternal age at birth was not associated with a decrease in school leaving grades in adolescent offspring. After adjustment for year of graduation, maternal age and parental education, country of birth and parental mental health service use, offspring of fathers aged 50 years or older had on average 0.3 (95% CI −3.8, 4.4) points higher grades than those of fathers aged 30–34 years. In conclusion, advancing paternal age is not associated with poorer school performance in adolescence. Adverse effects of delayed paternity on offspring cognitive function, if any, may be counterbalanced by other potential advantages for children born to older fathers.     

Paternity cues and mating opportunities: what makes fathers good?

Human males provide facultative paternal investment to their offspring; that is, the male care is not necessary for the survival of his offspring. It is expected that the degree of male investment (1) increases with growing paternity certainty, (2) increases when investment increases the survival and later reproductive prospect of offspring and (3) declines when there are opportunities to mate with multiple females. Using a large sample of adult offspring and their fathers (n = 245), we first investigated the role of two factors possibly involved in the assessment of paternity and subsequently regulating the level of paternal investment: (a) father–child facial resemblance and (b) assortative mating for eye colour. Second, because mating opportunities are inversely related to paternal investment, we also investigated how male facial attractiveness (a cue of mate opportunities) correlates with paternal investment. In line with paternal investment theory, male investment positively correlated with offspring facial resemblance. However, paternal investment were neither higher among blue-eyed couples, nor there were preferences of blue-eyed men to marry with blue-eyed women. Moreover, father facial attractiveness was unrelated to paternal investment. These results indicate that resemblance between offspring and their fathers still plays an important role in paternal investment decision later in offspring’s life.