Patterns Of Paternity Research Articles

A Genetic Analysis of the Virginia Opossum Mating System: Evidence of Multiple Paternity in a Highly Fragmented Landscape

Using molecular techniques, we examined patterns of paternity in Virginia opossums occupying a highly fragmented agricultural landscape in northern Indiana. During 2008, we collected tissue from 64 females and their pouch young in 34 forest patches distributed over a 1100-km(2) region. Using genotypes from 10 microsatellite loci, we determined the minimum number of fathers contributing to each litter using GERUD 1.0. Genotyped offspring with known mothers were then analyzed using CERVUS 3.0, incorporating genotypes from 317 males sampled from 2007-2008 to identify potential fathers. Our analyses revealed that promiscuity was common among females, with 26 (41%) litters having > or = 2 sires. Despite the fact that we intensively sampled forest patches for potential fathers, we only were able to identify 13 fathers contributing to 14 litters, with an average Euclidean distance of 18.7 km between father-offspring pairs found in disparate patches (N = 6). Our inability to identify most (85%) fathers of sampled litters, coupled with the extensive distances observed between putative father-offspring pairs, suggests that opossums may not maintain explicit home ranges in highly fragmented landscapes.

Épigénétique et pseudohypoparathyroïdies

Parental imprinting and the type of the genetic alteration play a determinant role in the phenotype expression of GNAS locus associated to pseudohypoparathyroidism (PHP). This imprint is tissue-specific, mainly localized in the kidney and the thyroid. Only the maternal allele is expressed at this level. An alteration in the coding sequence of the gene leads to an haplo-insufficiency and a dysmorphic phenotype (Albright's syndrome). If the alteration is on the maternal allele, there is a hormonal resistance to the PTH at the kidney level and to the TSH at the thyroid level. The phenotype is known as a PHP1a. If the alteration is on the paternal allele, there are few clinical signs with no hormonal resistance and the phenotype is known as pseudo-pseudo-hypoparathyroidism (PPHP). Methylation anomalies of GNAS locus, in particular of exon 1A, are responsible for a lack of expression of Gαs at kidney and thyroid levels only. If these anomalies concern the maternal allele (the only one expressed) with a paternal pattern, there is no haplo-insufficiency and no dysmorphic syndrome. The hormonal resistance is yet again limited to PTH and TSH. The phenotype is known as PHP1b. In the familial forms, these methylation anomalies are associated with a deletion of the syntaxine 16 gene in the maternal allele. This gene contains probably the imprinting center of the locus.

Experimental evidence that high levels of inbreeding depress sperm competitiveness

The effects of inbreeding on sperm quantity and quality are among the most dramatic examples of inbreeding depression. The extent to which inbreeding depression results in decreased fertilization success of a male's sperm, however, remains largely unknown. This task is made more difficult by the fact that other factors, such as cryptic female choice, male sperm allocation and mating order, can also drive patterns of paternity. Here, we use artificial insemination to eliminate these extraneous sources of variation and to measure the effects of inbreeding on the competitiveness of a male's sperm. We simultaneously inseminated female guppies (Poecilia reticulata) with equal amounts of sperm from an outbred (f = 0) male and either a highly (f = 0.59) or a moderately inbred (f = 0.25) male. Highly inbred males sired significantly fewer offspring than outbred males, but share of paternity did not differ between moderately inbred and outbred males. These findings therefore confirm that severe inbreeding can impair the competitiveness of sperm, but suggest that in the focal population inbreeding at order of a brother-sister mating does not reduce a male's sperm competitiveness.

Risk of Vertical HIV Transmission Combines the ‘B35-Cw4 Disadvantage’ and the ‘Pattern of Inheritance’ Theories of Progression

Mother-to-child transmission during pregnancy provides a unique system for studying the correlation between HLA phenotype and susceptibility to HIV infection. We studied this relationship in a Spanish cohort. We determined frequencies of HLA class I and II alleles in 120 infants born to HIV-infected mothers and 67 HIV-infected mothers. Although there was no statistical difference in the frequency of HLA-B35 between transmitting and non-transmitting mothers, the allele was more frequent in infected children than in uninfected children. HLA-B35 has been consistently reported as a risk factor in the progression to AIDS. In addition, it has been proposed that whether a given allele can confer susceptibility to, or protection against, progression depends on maternal versus paternal inheritance patterns, since the child inherits a virus that reflects the history of CTL encounters of the mother. Our results on vertical HIV transmission combine for the first time the 'HLA-B35 disadvantage' and the 'pattern of inheritance' theories.

Sperm precedence in monarch butterflies (Danaus plexippus)

We characterized sperm precedence in monarch butterflies (Danaus plexippus), using a series of experiments in which we manipulated male mating histories to vary spermatophore size and the number of sperm transferred. Several factors affected the outcome of sperm competition. There was a pattern of second-male sperm precedence, but second-male precedence was rarely complete, and several other factors had significant effects on paternity patterns. Larger males outcompeted smaller males when they were not matched for size. Phosphoglucose isomerase (PGI) genotype affected the outcome of sperm competition under very hot conditions. When sperm from the same pair of males competed in different females, males fared better when they transferred more sperm. These results demonstrate that sperm precedence within a species can be affected by many factors, including the circumstances under which it is measured. Key words: monarch butterflies, PGI genotype, sperm competition, sperm transfer. [Behav Ecol]

First male sperm precedence in multiply-mated females of the cooperative spider Anelosimus studiosus (Araneae, Theridiidae)

Patterns of sperm usage in multiply-mated females have profound fitness consequences for males, and create strong selective pressure on male behavior. In the cooperative theridiid spider Anelosimus studiosus Hentz 1850 adult males are tolerated in females' webs, and females have been observed to mate multiply with different males. In this experiment, virgin females were mated with two different males on consecutive days under controlled conditions to determine paternity patterns and behavioral responses of males to non-virgin females. The paternity of broods was analyzed using randomly amplified polymorphic DNA (RAPDs). Fifteen broods were analyzed and complete first male sperm precedence was found. Mating behavior differed between first and second males with the first males attempting fewer intromissions, but having a longer total time of intromission. This suggests that the second males are either prevented from normal copulation, or are reacting to the different condition of the females. The sperm precedence pattern is discussed with respect to its ramifications for male behavior, juvenile inclusive fitness, and the evolution of cooperative behavior.

Single paternity within broods of the brown crab Cancer pagurus: a highly fecund species with long-term sperm storage

Declining population sizes reported for a number of marine species have emphasised the need for information on mating systems to be incorporated into conservation and management strategies, particularly for exploited species. The brown crab Cancer pagurus L. supports a major fishery; however, many aspects of the species' mating system, such as paternity patterns, are unre- solved. In this study, 3 microsatellite loci conferring a high degree of statistical power were used to determine whether broods from 18 ovigerous females collected from the English Channel had been fertilised by multiple males. Despite the capacity of this species for long-term storage of sperm and the suspected potential for females to use sperm from multiple males simultaneously, no evidence of multiple paternity was detected. Hypotheses as to the predominant processes leading to single pater- nity are discussed. In systems where females exhibit genetic monogamy the effective population size is constrained by the number of females. Such systems may be particularly susceptible to declines if females are removed. This has important implications for management of C. pagurus populations, as fishery data indicate that females are more heavily harvested than males.

Functional assessment of centrosomes of spermatozoa and spermatids microinjected into rabbit oocytes

Although intracytoplasmic sperm injection (ICSI) is a widely used assisted reproductive technique, the fertilization rates and pregnancy rates of immature spermatids especially in round spermatid injection (ROSI) remain very low. During mammalian fertilization, the sperm typically introduces its own centrosome which then acts as a microtubule organizing center (MTOC) and is essential for the male and female genome union. In order to evaluate the function of immature germ cell centrosomes, we used the rabbit gamete model because rabbit fertilization follows paternal pattern of centrosome inheritance. First, rabbit spermatids and spermatozoa were injected into oocytes using a piezo-micromanipulator. Next, the centrosomal function to form a sperm aster was determined. Furthermore, two functional centrosome proteins (gamma-tubulin and centrin) of the rabbit spermatogenic cells were examined. Our results show that the oocyte activation rates by spermatozoa, elongated spermatids, and round spermatids were 86% (30/35), 30% (11/36), and 5% (1/22), respectively. Sperm aster formation rates after spermatozoa, elongated spermatids, and round spermatids injections were 47% (14/30), 27% (3/11), and 0% (0/1), respectively. The aster formation rate of the injected elongating/elongated spermatids was significantly lower than that of the mature spermatozoa (P = 0.0242). Moreover, sperm asters were not observed in round spermatid injection even after artificial activation. These data suggest that poor centrosomal function, as measured by diminished aster formation rates, is related to the poor fertilization rates when immature spermatogenic cells are injected.

Multiple paternity in the leafcutter ant Atta colombica- a microsatellite DNA study

An evolutionary understanding of the causes, correlates and consequences of multiple paternity in eusocial Hymenoptera (all ants, some bees and some wasps) relies on accurate estimation of this parameter at the species, population and colony level. We developed dinucleotide microsatellite DNA markers in order to study in detail the degree of multiple paternity in a population of the monogynous Panamanian leafcutter ant Atta colombica. These microsatellite markers were highly polymorphic such that nondetection caused by finite allelic diversity was very low (0.016). Hence, accurate information on the patterns of multiple paternity could be obtained. Genetic analysis revealed that in 33 out of 36 colonies two or more males had contributed genetically to the offspring. The mean number of fathers per colony was 2.6 and the mean effective paternity was 2.31. These are the highest values of effective paternity yet reported for any ant species. We examined the patterns of paternity frequency in young and old colonies to test if within-colony genetic diversity is related to colony survival, but found no support for any relationship. Our results confirm previous nongenetic studies showing high levels of multiple mating by queens of higher leafcutter ants. We discuss our findings in relation to known patterns of polyandry and paternity in other eusocial Hymenoptera.

Extra-pair paternity in the socially monogamous Sedge Warbler Actocephalus schoenobaenus as revealed by multilocus DNA fingerprinting

A marked population of Sedge Warblers Acrocephalus schoenobaenus was studied from 1993-95, the reproductive success of pairs was monitored and blood samples collected for DNA profiling. Measures of male physical and behavioural traits were also made, including song repertoire size, the amount of time spent singing and song-flighting, as well as territory quality. Although the Sedge Warbler is generally considered to be monogamous, social polygyny occurred in both 1994 and 1995, giving an overall rate for the two years of 7.7% of males. The overall rate of extra-pair paternity in the population was found to be 8.4% of offspring, with 34.4% of broods containing one or more extra-pair young. No incidences of intra-specific brood parasitism (egg dumping) were identified. Cuckolded males were compared with other males, but no significant differences were identified for any of the physical, behavioural or territorial measures. In particular, there was no evidence that previously detected mate choice cues are related d to patterns of paternity within the population, and hence no evidence that such cues indicate genetic benefits to females. It therefore seems likely that repertoire size reflects male phenotypic quality in this species.

Inter‐population variation in multiple paternity and reproductive skew in the guppy

We use microsatellite loci to detail the multiple paternity patterns in broods from 10 wild populations of the guppy (Poecilia reticulata) found in Northern Trinidad. The populations span two major drainages comprising the Caroni and the Oropouche, and include sites that are characterized by either high or low predation. Across the populations the frequency of multiple paternity is high with 95% (range: 70%-100%) of broods having multiple sires. Broods have an average of 3.5 sires (range: 1-9) and a mixed-model analysis suggests that broods from high predation sites have marginally more sires than do those from low predation sites, but this is true only in the Oropouche drainage. There is no difference in sire number between predation sites in the Caroni drainage. Brood size, but not female body length, is correlated with the number of sires and the correlation cannot be attributed solely to the stochastic process associated with sperm competition and a 'fair raffle'. Within broods there is significant skew in reproductive success among males, which may reflect variation in sperm competitiveness or female choice. There is, however, no difference in the skew among populations from different predation regimes or drainages. Finally, high predation populations were characterized by increased genetic variability at the microsatellite loci, suggesting a larger effective population size. We discuss explanations for the high degree of multiple paternity but the general lack of any major differences among broods from ecologically different populations.

The genetic similarity between pair members influences the frequency of extrapair paternity in alpine marmots

Extrapair paternity is widespread in birds and mammals. In particular, the alpine marmot, Marmota marmota, has a high frequency of extrapair paternity that seems to be explained by the genetic compatibility hypothesis. We investigated whether the number and proportion of extrapair young depend on the heterozygosity (individual genetic diversity) of the social male, or on the genetic similarity between the social male and his mate (relatedness). Both the number and the proportion of extrapair young increased with both high similarity and dissimilarity between the social pair. In combination with previous results, our study suggests that patterns of extrapair paternity in alpine marmots can best be explained by the genetic compatibility hypothesis, and more precisely its optimal outbreeding variant. Our results indeed suggest that extrapair paternity is a mechanism to avoid both in- and outbreeding depression. We discuss which proximal mechanisms may be involved in extrapair paternity in this species.

Multiple paternity in reptiles: patterns and processes

The evolution of female promiscuity poses an intriguing problem as benefits of mating with multiple males often have to arise via indirect, genetic, effects. Studies on birds have documented that multiple paternity is common in natural populations but strong evidence for selection via female benefits is lacking. In an attempt to evaluate the evidence more broadly, we review studies of multiple paternity in natural populations of all major groups of nonavian reptiles. Multiple paternity has been documented in all species investigated so far and commonly exists in over 50% of clutches, with particularly high levels in snakes and lizards. Marine turtles and lizards with prolonged pair-bonding have relatively low levels of multiple paternity but levels are nevertheless higher than in many vertebrates with parental care. There is no evidence that high levels of polyandry are driven by direct benefits to females and the evidence that multiple paternity arises from indirect genetic benefits is weak. Instead, we argue that the most parsimonious explanation for patterns of multiple paternity is that it represents the combined effect of mate-encounter frequency and conflict over mating rates between males and females driven by large male benefits and relatively small female costs, with only weak selection via indirect benefits. A crucial step for researchers is to move from correlative approaches to experimental tests of assumptions and predictions of theory under natural settings, using a combination of molecular techniques and behavioural observations.

Age‐related variation in primary sexual characters in a passerine with male age‐related fertilization success, the bluethroat Luscinia svecica

In passerine species with frequent extrapair mating, young (second calendar year) males often have a lower fertilization success than older (after second calendar year) males. This pattern might be explained by male‐ or female‐driven mechanisms, such as female preference for older males or higher competitive ability of older males. In this study we measured the size of the testes, the seminal glomera and the cloacal protuberance as well as the size and motility of the sperm, in individual bluethroats Luscinia svecica. In this species, nearly all extrapair fertilizations (EPFs) are obtained by older males. We found that the mass of the testes and the seminal glomera were highly positively correlated and that older males had significantly larger testes (38%), seminal glomera (15%) and cloacal protuberance (23%) than young males. In contrast, there was no difference between age groups in average sperm size or sperm motility. Our results are consistent with the idea that higher fertilization success by older males in this species is due to their higher rate of sperm production, allowing larger ejaculates and/or more frequent copulations. Unequal sperm production capacities by young and older males have important implications for the interpretation of paternity patterns in extrapair mating systems.

Faster male lizards are better defenders not sneakers

Locomotion is an important trait to individual fitness in numerous animal taxa for predator escape and prey acquisition. However, the role of locomotion in mating success has been largely unexplored. Even studies linking sprint speed with proxies of fitness (e.g. dominance) and actual measures of mating success (e.g. genetic reproductive success) have struggled to test explicit hypotheses as to how high-performance individuals attain higher fitness. We studied a free-ranging population of male collared lizards, Crotaphytus collaris , to determine why faster males sire more offspring. Specifically, we tested the alternative hypotheses that faster males are ‘fast defenders’ versus ‘fast sneakers’ by using molecular genetic techniques to examine patterns of maternity and paternity in the population. We found that females that were defended by faster males had a lower proportion of offspring sired by males that did not defend them (support for a fast defender hypothesis). In contrast, we found no relation between males' sprint speed and the proportion of their offspring that were produced by females other than those they defended (no support for a fast sneaker hypothesis). In species in which locomotor performance is important to male competition, these alternative hypotheses should be simultaneously tested and complemented with behavioural data to discriminate them from female choice.

Postcopulatory sexual selection favours intrinsically good sperm competitors

We used guppies to study repeatability in sperm competitiveness and postcopulatory sexual selection on male ornamentation. In a block design involving 25 pairs of males, artificial insemination was used to mate each pair (A and B) to four unrelated females—two that were mated with the combined ejaculates of both males (sperm-competition treatment) and two receiving sperm from each of the two males individually (single-male treatment). Our analysis revealed significantly repeatable patterns of paternity across females in the sperm-competition treatment, suggesting that certain males are intrinsically better sperm competitors than others, irrespective of female identity. Next, we compared mean brood success (number of offspring per brood) between sperm competition and single-male treatments. We found no significant effect of treatment on female fecundity, suggesting that the previously reported direct benefits of polyandry in this species may be due to factors such as differential maternal effects or differences in the number of inseminated sperm between treatments. Our artificial insemination assay was designed to control both factors. Finally, we determined whether variation in relative paternity was random with respect to male phenotype. Unlike previous work on Trinidadian populations, we found no significant relationship between male sexual ornamentation and sperm competitiveness in the focal population.

Fatherhood in different decades: Interactions between German fathers and their infants in 1977 and 2001

The present study about fatherhood in Germany addresses the issue of changing paternal behaviour in the German middle class between 1977 and 2001. Against the background of the ongoing phase of individualization in Germany, videotaped interactions between fathers and their 3-months-old infants are analysed. The results reveal a shift towards more autonomy and independence in the fathers' behaviour. This can be seen in increases and decreases of particular paternal behaviour patterns, which are related to either independence and autonomy or interdependence and relatedness. In sum, between the two points in time the fathers show an increase in the frequencies of object stimulation and contingent responses to infant signals in the face-to-face-context on the one hand and a decrease in the frequencies of body contact and interactional warmth on the other.

Male insemination decisions and sperm quality influence paternity in the golden orb-weaving spider

In polyandrous species, paternity may be influenced by the timing and frequency of mating. Female spiders possess 2 genital openings that lead to separate sperm-storage structures. Thus, even when mating with a previously mated female, a male may reduce direct sperm competition by inseminating the opposite opening to her first mate. Such morphology may provide females with greater control over paternity. We examined simultaneously whether males avoided already inseminated female genital openings and whether this behavior varied with the time between successive matings. To explore these questions, we mated female golden orb weaver spiders, Nephila edulis, each to 2 males and manipulated the timing of their second mating. We documented male insemination patterns and explored the influence of male mating decisions on paternity success using the irradiated male technique. We found that 60% of males avoided sperm competition by discriminating against inseminated genital openings. Moreover, male mating behavior had a dramatic impact on the paternity success of irradiated males. When males inseminated the same genital opening, the competitive ability of the irradiated male's sperm was dramatically reduced resulting in lower paternity success. In contrast, when the 2 males inseminated opposite genital openings both males sired equal proportions of offspring regardless of their radiation status. There was no evidence that the timing of the second mating affected patterns of paternity. Our data suggest that differences in sperm quality may influence paternity success of N. edulis males under a sperm-competitive scenario. In contrast, females appear to have limited postmating control over paternity. © The Author 2007. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved.

Patterns of paternity and group fission in wild multimale mountain gorilla groups

To understand variation among social systems, it is essential to know the relative reproductive success of individuals in group-living species. Particularly interesting for such studies are taxa such as mountain gorillas in which both one-male and multimale groups are common, because of the opportunity to estimate the costs and benefits to males of pursuing different reproductive strategies. We genotyped 68 individuals from two groups of multimale mountain gorilla groups in Bwindi Impenetrable National Park, Uganda to determine the distribution of paternity among the males. In both groups, the dominant male sired the majority of offspring. One group underwent a fission, and we found that the eight offspring assigned to the dominant silverback (and their mothers) remained with their father, while the two offspring of unknown paternity ended up in the small group headed by the formerly subordinate silverback. This is consistent with the proposal that the outcome of group fission in primates is not only influenced by maternal relationships among individuals, but also by patrilineal relationships. Results of this study show that subordinate males may gain reproductive benefits even while queuing for dominance status. Despite ecological differences between Bwindi and the Virunga Volcanoes, male mountain gorillas living in both populations benefit from remaining in multimale groups.

A cost of cryptic female choice in the yellow dung fly

Female dung flies Scathophaga stercoraria (L.) store sperm from several males in three or four spermathecae. Selection on the number of spermathecae was successful and the morphological intermediate stages in the evolution from three to four spermathecae are illustrated. The genetic quality of a male from a female's perspective depends on an interaction between their genotypes and the microhabitat in which the offspring will grow. Females influence the paternity pattern of their offspring, and do this differently in different microhabitats. Females with four spermathecae are better able to influence paternity than are those with three spermathecae. However, there must be a cost to building and maintaining an extra spermatheca. We estimate, using the animal model on pedigree data, that this cost is approximately five eggs per clutch, i.e. around 8% of the mean clutch size. This is a substantial cost and such costs should not be ignored in discussions of the benefits to females of assessing the genetic qualities of their mating partners. We suggest that the number of spermathecae in the study population is stable because the relative benefits in quality of offspring through cryptic female choice is balanced by the costs in total numbers of offspring.