Multiple Paternity (multiple + paternity)

Distribution by Scientific Domains


Selected Abstracts


Pair Bonding and Multiple Paternity in the Polygamous Common Quail Coturnix coturnix

ETHOLOGY, Issue 4 2003
J. D. Rodríguez-Teijeiro
The common quail (Coturnix coturnix) is one of the few species in which mate-switching (when different pair bonds are established within a single breeding attempt), has been recorded. In this study, we report the characteristics of pair bonds (description, number of males per female and duration) by monitoring a wild population of common quail (28 females and 49 males) by radiotracking. 57% of the females studied (n = 14) showed mate-switching, whereas 22% of the males were serially polygynous, successively forming pairs with a series of females. The fitness of females with mate-switching, measured in terms of clutch size and hatching success, did not differ from that of females bonded with one male. The analysis of paternity in three families by multilocus DNA fingerprinting revealed genetic polygamy in two of the nests studied. A male sired offspring with two females, and we obtained genetic evidence for intraspecific brood parasitism. We discuss how these behavioural and ecological observations may relate to the particular mating system of the common quail. [source]


Multiple Paternity and Similar Variance in Reproductive Success of Male and Female Wood Mice (Apodemus sylvaticus) Housed in an Enclosure

ETHOLOGY, Issue 10 2001
Susan Bartmann
The mating system and variance in individual reproductive success in wood mice (Apodemus sylvaticus) were analysed genetically and using observational studies within a large cage system in an outdoor enclosure. Four experimental groups contained four males and four females, each individually marked with a transponder (small computer chips injected under the skin) allowing individual detection of animals underground or within nest boxes without disturbance. The probability of paternity was analysed by comparing frequencies of cohabitation of males and females. In addition, DNA microsatellite analysis revealed reproductive success of each individual. Multiple paternity was found in 85% of all litters, which were sired by up to all four males. Males with a greater body mass, possibly indicative of a higher rank, sired more offspring than those with lower body mass. Interestingly, variance in the reproductive success of males and females did not differ. There was no indication that paternity could be assessed by the time males resided with a female shortly before she became pregnant. Our results indicate wood mice probably have a promiscuous mating system. [source]


Multiple paternity increases effective population size

MOLECULAR ECOLOGY, Issue 15 2009
DEVON E. PEARSE
[source]


Multiple paternity in reptiles: patterns and processes

MOLECULAR ECOLOGY, Issue 11 2008
TOBIAS ULLER
Abstract 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. [source]


Multiple paternity in a natural population of a wild tobacco fly, Bactrocera cacuminata (Diptera: Tephritidae), assessed by microsatellite DNA markers

MOLECULAR ECOLOGY, Issue 11 2007
SIMON D. SONG
Abstract Mating frequency has important implications for patterns of sexual selection and sexual conflict and hence for issues such as speciation and the maintenance of genetic diversity. Knowledge of natural mating patterns can also lead to more effective control of pest tephritid species, in which suppression programmes, such as the sterile insect technique (SIT) are employed. Multiple mating by females may compromise the success of SIT. We investigated the level of polyandry and sperm utilization in a Brisbane field population of the tropical fruit fly, Bactrocera cacuminata (Hering), using seven polymorphic microsatellite loci. The offspring of 22 wild-caught gravid females were genotyped to determine the number of males siring each brood and paternity skew, using the programs gerud and scare. Our data showed that 22.7% of females produced offspring sired by at least two males. The mean number of mates per female was 1.72. Paternal contributions of double-sired broods were skewed with the most successful male having sired between 76.9% and 87.5% of the offspring. These results have implications for SIT, because the level of remating we have identified would indicate that wild females could mate with one or more resident fertile males. [source]


Multiple paternity in a salamander with socially monogamous behaviour

MOLECULAR ECOLOGY, Issue 13 2006
ERIC B. LIEBGOLD
Abstract In the majority of birds and mammals, social monogamy is not congruent with genetic monogamy. No research to date has compared social and genetic monogamy in amphibians. We analysed paternity in clutches of red-backed salamanders (Plethodon cinereus), a species in which social monogamy has been demonstrated in the laboratory, and 28% of individuals in the forest are found in male-female pairs in the noncourtship season. We collected 16 clutches of eggs of P. cinereus in the southern Appalachian Mountains of Virginia and collected tail clippings from attending mothers. We genotyped embryos and adults at five microsatellite loci in order to analyse paternity of clutches. Most clutches (84.6%) had multiple sires, with two to three sires per clutch. In this study, 25% of clutches had males in addition to females attending eggs. None of the mothers of these clutches were genetically monogamous. All attending males sired some of the offspring in the clutch that they attended (between 9% and 50%) but never sired a majority in that clutch. We conclude that, at least in this population, social monogamy in P. cinereus is not concomitant with genetic monogamy. [source]


Early male reproductive advantage, multiple paternity and sperm storage in an amphibian aggregate breeder

MOLECULAR ECOLOGY, Issue 6 2003
J. A. Tennessen
Abstract We tested whether the order in which males encounter females affects reproductive fitness in spotted salamanders (Ambystoma maculatum). Using mating chambers in the field, we allowed one male access to a female before a second male. We then used four microsatellite markers in paternity analyses of the resulting larvae. First males sired a significantly larger number of offspring than second males, suggesting that male reproductive success is greatly enhanced by early arrival at breeding ponds. Multiple paternity was common among clutches, and frequently larvae were assigned to unidentified males that had not been in the chambers. Sperm from these males had either been stored by females for a year or obtained more recently at other breeding sites. [source]


Molecular determination of paternity in a natural population of the multiply mating polygynous lizard Eulamprus heatwolei

MOLECULAR ECOLOGY, Issue 3 2002
S. F. Morrison
Abstract We studied the mating system of the southern water skink, Eulamprus heatwolei, during spring and summer (encompassing the breeding season) in a population in southeastern Australia. We examined potential attributes that might influence the mating system and male reproductive success including home range size, physical proximity of adults and body size, and then genotyped all mothers, offspring and potential sires. Home range overlap of both sexes was extensive, with adult females sharing the greatest amount of space with each other and adult males the least amount of space with each other. However, not all adults hold home ranges. We classified approximately one quarter of adult males as home range holders and the rest as ,floaters'. Adult females occupy home ranges more than males, with approximately three-quarters classified as home range holders. Home range ownership is not correlated with body size for either sex, however, male body size is positively correlated with the number of adult female home ranges that his home range overlaps and adult male home ranges are larger than those of females. We used microsatellite genotyping to assign paternities to 55 offspring from 17 litters and then compared this data with our home range and behavioural observations. This species displays extreme levels of multiple paternity given the small mean clutch size of three. Multiple paternity was confirmed in 11 (64.7%) of 17 clutches but three other clutches (for a total of 82.4%) also may display multiple paternity. A total of 30 offspring from 12 litters were assigned to 10 of the 32 genotyped adult males from our study site. Of these 10 adult males, half were home range holders. Five complete clutches and a total of 25 out of the 55 offspring could not be positively assigned to any male surveyed as part of the study and were attributed to floater males or resident males adjacent to our study site that had not been genotyped. While sample sizes are small, neither male home range ownership nor body size is significantly correlated with the number of paternities a male obtained. Our study suggests a polygynous mating system for this species. [source]


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

MOLECULAR ECOLOGY, Issue 2 2002
M. K. Moore
Abstract 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. [source]


Variation in multiple paternity and sperm utilization patterns in natural populations of a simultaneous hermaphrodite land snail

BIOLOGICAL JOURNAL OF THE LINNEAN SOCIETY, Issue 2 2010
SANDRA KUPFERNAGEL
Mating frequency has important implications for patterns of sexual selection and sexual conflict, and hence for issues such as the maintenance of genetic diversity and speciation. We assessed the level of multiple paternity and sperm utilization patterns in four natural populations of the simultaneous hermaphrodite land snail Arianta arbustorum using four polymorphic microsatellite loci. A total of 1088 offspring from 26 wild-caught snails were genotyped to determine the number of fathers siring each brood and paternity skew in succeeding clutches. Multiple paternity was detected in the offspring of all 26 mother snails examined with the contribution of two to six fathers. The four populations examined differed in the level of multiple paternity. Snails in the population with the highest density of adults showed the highest level of multiple paternity, whereas snails in the population with the lowest density exhibited the lowest value of multiple paternity. Highly skewed paternity patterns were found in the progeny of 15 (57.7%) of the 26 mother snails. The number and identity of fathers siring the offspring of single mothers also varied among successive clutches. Furthermore, genetic analyses indicate a low level of self-fertilization in one of the four populations. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99, 350,361. [source]


Multiple paternity occurs with low frequency in the territorial roe deer, Capreolus capreolus

BIOLOGICAL JOURNAL OF THE LINNEAN SOCIETY, Issue 1 2009
C. VANPÉ
An explanation for female multiple mating when males offer no material benefits but sperm remains elusive, largely because of a lack of empirical support for the genetic benefits hypothesis. We used 21 microsatellite markers to test for multiple paternities among 88 litters of roe deer, Capreolus capreolus, and to investigate the inbreeding avoidance hypothesis as a potential mechanism for the evolution of female multiple mating. From paternity analyses, we found that 13.5% of polytocous litters were sired by more than one male. We also found that a half-sib relationship was more likely than a full-sib relationship for 20.5% of all litters. This is the first report of multiple paternities in a territorial ungulate species. In support of the inbreeding avoidance hypothesis, we found that parents who were strongly related produced offspring with lower individual heterozygosity that survived less well during their first summer than fawns with unrelated parents. In addition, fawns from multiple paternity litters survived their first summer better than fawns from single paternity litters. However, it remains unclear whether all female multiple paternity events in this species are provoked by an initial consanguineous mating. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society 2009, 97, 128,139. [source]


Male Mate Choice in the Guppy (Poecilia reticulata): Do Males Prefer Larger Females as Mates?

ETHOLOGY, Issue 2 2004
Emily J. E. Herdman
Although females are the choosier sex in most species, male mate choice is expected to occur under certain conditions. Theoretically, males should prefer larger females as mates in species where female fecundity increases with body size. However, any fecundity-related benefits accruing to a male that has mated with a large female may be offset by an associated fitness cost of shared paternity if large females are more likely to be multiply mated than smaller females in nature. We tested the above hypothesis and assumption using the Trinidadian guppy (Poecilia reticulata) by behaviourally testing for male mate choice in the laboratory and by ascertaining (with the use of microsatellite DNA genotyping) patterns of male paternity in wild-caught females. We observed significant positive relationships between female body length and fecundity (brood size) and between body length and level of multiple paternity in the broods of females collected in the Quaré River, Trinidad. In laboratory tests, a preference for the larger of two simultaneously-presented virgin females was clearly expressed only when males were exposed to the full range of natural stimuli from the females, but not when they were limited to visual stimuli alone. However, as suggested by our multiple paternity data, males that choose to mate with large females may incur a larger potential cost of sperm competition and shared paternity compared with males that mate with smaller females on average. Our results thus suggest that male guppies originating from the Quaré River possess mating preferences for relatively large females, but that such preferences are expressed only when males can accurately assess the mating status of encountered females that differ in body size. [source]


Geographic variation in sperm traits reflects predation risk and natural rates of multiple paternity in the guppy

JOURNAL OF EVOLUTIONARY BIOLOGY, Issue 6 2010
K. E. ELGEE
Abstract Guppies (Poecilia reticulata) are models for understanding the interplay between natural and sexual selection. In particular, predation has been implicated as a major force affecting female sexual preferences, male mating tactics and the level of sperm competition. When predation is high, females typically reduce their preferences for showy males and engage more in antipredator behaviours, whereas males exploit these changes by switching from sexual displays to forced matings. These patterns are thought to account for the relatively high levels of multiple paternity in high-predation populations compared to low-predation populations. Here, we assess the possible evolutionary consequences of these patterns by asking whether variation in sperm traits reflect differences in predation intensity among four pairs of Trinidadian populations: four that experience relatively low levels of predation from a gape-limited predator and four that experience relatively high levels of predation from a variety of piscivores. We found that males in high-predation populations had faster swimming sperm with longer midpieces compared to males in low-predation populations. However, we found no differences among males in high- and low-predation populations with respect to sperm number, sperm head length, flagellum length and total sperm length. [source]


Offspring-driven local dispersal in female sand lizards (Lacerta agilis)

JOURNAL OF EVOLUTIONARY BIOLOGY, Issue 6 2004
K. Ryberg
Abstract We report on a field study in which determinants of female breeding dispersal (i.e. the shift in the mean home range coordinates between successive breeding events) was investigated. Offspring were released in full sib groups (or half sib ones if there was within-clutch multiple paternity) at a separation distance from the females that varied between ,families'. This allowed for analysis of ,offspring nearness' effects on maternal dispersal. When a female's offspring were released more closely to her, she responded with greater dispersal. Furthermore, when the data set was truncated at 100 m maternal,offspring separation distance at offspring release (because perception at longer distances is likely to be unrealistic), maternal dispersal resulted in greater separation distance between female and offspring in the following year. A corresponding analysis for juveniles revealed no effect of maternal nearness on offspring dispersal but identified a significant effect of clutch size, to our surprise with dispersal declining with increasing clutch size. We discuss this result in a context of the ,public information hypothesis' (reinterpreted for juveniles in a nonsocial foraging species), suggesting that conspecific abundance perhaps acts as an indicator of local habitat quality. Thus, our analysis suggests a microgeographic structuring of the adult female population driven by genetic factors, either through inbreeding avoidance, or from simply avoiding individuals with a similar genotype regardless of their pedigree relatedness, while a nongenetic factor seems more important in their offspring. [source]


Multiple paternity in reptiles: patterns and processes

MOLECULAR ECOLOGY, Issue 11 2008
TOBIAS ULLER
Abstract 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. [source]


Patterns of relatedness and parentage in an asocial, polyandrous striped hyena population

MOLECULAR ECOLOGY, Issue 20 2007
AARON P. WAGNER
Abstract We investigated patterns of relatedness and reproduction in a population of striped hyenas in which individuals are behaviourally solitary but form polyandrous spatial groups consisting of one adult female and multiple adult males. Group-mate males were often close relatives, but were unrelated or distantly related in some cases, indicating that male coalitions are not strictly a result of philopatry or dispersal with cohorts of relatives. Most male,female pairs within spatial groups were unrelated or only distantly related. Considering patterns of relatedness between groups, relatedness was significantly higher among adult males living in non-neighbouring ranges than among neighbouring males. Mean relatedness among male,female dyads was highest for group-mates, but relatedness among non-neighbouring males and females was also significantly higher than among dyads of opposite-sex neighbours. Female,female relatedness also increased significantly with increasing geographic separation. These unusual and unexpected patterns may reflect selection to settle in a nonadjacent manner to reduce inbreeding and/or competition among relatives for resources (both sexes), or mates (males). Finally, resident males fathered the majority of the resident female's cubs, but extra-group paternity was likely in 31% of the cases examined, and multiple paternity was likely in half of the sampled litters. [source]


Early male reproductive advantage, multiple paternity and sperm storage in an amphibian aggregate breeder

MOLECULAR ECOLOGY, Issue 6 2003
J. A. Tennessen
Abstract We tested whether the order in which males encounter females affects reproductive fitness in spotted salamanders (Ambystoma maculatum). Using mating chambers in the field, we allowed one male access to a female before a second male. We then used four microsatellite markers in paternity analyses of the resulting larvae. First males sired a significantly larger number of offspring than second males, suggesting that male reproductive success is greatly enhanced by early arrival at breeding ponds. Multiple paternity was common among clutches, and frequently larvae were assigned to unidentified males that had not been in the chambers. Sperm from these males had either been stored by females for a year or obtained more recently at other breeding sites. [source]


Molecular determination of paternity in a natural population of the multiply mating polygynous lizard Eulamprus heatwolei

MOLECULAR ECOLOGY, Issue 3 2002
S. F. Morrison
Abstract We studied the mating system of the southern water skink, Eulamprus heatwolei, during spring and summer (encompassing the breeding season) in a population in southeastern Australia. We examined potential attributes that might influence the mating system and male reproductive success including home range size, physical proximity of adults and body size, and then genotyped all mothers, offspring and potential sires. Home range overlap of both sexes was extensive, with adult females sharing the greatest amount of space with each other and adult males the least amount of space with each other. However, not all adults hold home ranges. We classified approximately one quarter of adult males as home range holders and the rest as ,floaters'. Adult females occupy home ranges more than males, with approximately three-quarters classified as home range holders. Home range ownership is not correlated with body size for either sex, however, male body size is positively correlated with the number of adult female home ranges that his home range overlaps and adult male home ranges are larger than those of females. We used microsatellite genotyping to assign paternities to 55 offspring from 17 litters and then compared this data with our home range and behavioural observations. This species displays extreme levels of multiple paternity given the small mean clutch size of three. Multiple paternity was confirmed in 11 (64.7%) of 17 clutches but three other clutches (for a total of 82.4%) also may display multiple paternity. A total of 30 offspring from 12 litters were assigned to 10 of the 32 genotyped adult males from our study site. Of these 10 adult males, half were home range holders. Five complete clutches and a total of 25 out of the 55 offspring could not be positively assigned to any male surveyed as part of the study and were attributed to floater males or resident males adjacent to our study site that had not been genotyped. While sample sizes are small, neither male home range ownership nor body size is significantly correlated with the number of paternities a male obtained. Our study suggests a polygynous mating system for this species. [source]


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

MOLECULAR ECOLOGY, Issue 2 2002
M. K. Moore
Abstract 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. [source]


Variation in multiple paternity and sperm utilization patterns in natural populations of a simultaneous hermaphrodite land snail

BIOLOGICAL JOURNAL OF THE LINNEAN SOCIETY, Issue 2 2010
SANDRA KUPFERNAGEL
Mating frequency has important implications for patterns of sexual selection and sexual conflict, and hence for issues such as the maintenance of genetic diversity and speciation. We assessed the level of multiple paternity and sperm utilization patterns in four natural populations of the simultaneous hermaphrodite land snail Arianta arbustorum using four polymorphic microsatellite loci. A total of 1088 offspring from 26 wild-caught snails were genotyped to determine the number of fathers siring each brood and paternity skew in succeeding clutches. Multiple paternity was detected in the offspring of all 26 mother snails examined with the contribution of two to six fathers. The four populations examined differed in the level of multiple paternity. Snails in the population with the highest density of adults showed the highest level of multiple paternity, whereas snails in the population with the lowest density exhibited the lowest value of multiple paternity. Highly skewed paternity patterns were found in the progeny of 15 (57.7%) of the 26 mother snails. The number and identity of fathers siring the offspring of single mothers also varied among successive clutches. Furthermore, genetic analyses indicate a low level of self-fertilization in one of the four populations. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99, 350,361. [source]


Seasonal monogamy and multiple paternity in a wild population of a territorial reptile (tuatara)

BIOLOGICAL JOURNAL OF THE LINNEAN SOCIETY, Issue 1 2009
JENNIFER A. MOORE
Investigating the mating system of a population provides insight into the evolution of reproductive patterns, and can inform conservation management of threatened or endangered species. Combining behavioural and genetic data is necessary to fully understand the mating system and factors affecting male reproductive success, yet behavioural data are often difficult to collect for threatened species. In the present study, we use behavioural data and paternity analyses to characterize the mating system of a high density population of a long-lived, ancient reptile (tuatara, Sphenodon punctatus). We further investigate the phenotypic traits (including body size, body condition, tail length, and ectoparasite load) that affect male reproductive success. Our behavioural data reflect a seasonally monogamous system with low levels of polyandry and polygyny that are consistent with male mate guarding. Male reproduction is highly skewed (only 25,30% of males are successful), and body size is the primary predictor of male reproductive success. Based on the genetic data, multiple paternity was found in only 8% of clutches, and the results of the paternity analyses showed monandrous clutches from socially polyandrous females. Our behavioural and genetic results revealed complexities in female mating patterns that support the potential for cryptic female choice or sperm competition. This warrants further experimental investigation into the mechanisms underlying reptile fertilization and the disparities between social and genetic polyandry in wild populations. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 161,170. [source]