Genetic relationships within colonies suggest genetic monogamy in the Eurasian beaver (<Emphasis Type="Italic">Castor fiber</Emphasis>)

Social monogamy, considered rare in mammals, has been described in two species of beaver, the Eurasion beaver (Castor fiber), and the North American beaver (Castor Canadensis). Social monogamy, however, does not necessarily imply genetic monogamy. For example, in group living mammals, females may engage in extra-pair copulations as a result of increased female mate choice opportunities. Recently, following genetic analysis, a wide range of genetic relationships among colony members have been documented in the North American beaver, including extra-pair paternity. Here, we used microsatellite loci to provide parentage estimates from colonies of the Eurasian beaver in the Kirov region, Russia. No evidence for the presence of any extra-pair young was detected. However, in two cases, we found a pair of unrelated males inhabiting a single colony. Our results suggest that while colonies may comprise both related and unrelated individuals, the genetic mating system appears to match that of the previously inferred social monogamy.     

High frequency of extrapair copulation with low level of extrapair fertilization in the Lanyu scops owl Otus elegans botelensis

The genetic mating system is known for only a few species of owls. Most of them are genetically monogamous. The Lanyu scops owl Otus elegans botelensis breeds in high density in the forests of Lanyu (Orchid Island), southeast of Taiwan. Because extra-pair copulations (EPCs) have frequently been observed, we suspected a high degree of extra-pair fertilizations (EPFs). Through intensive field observations we quantified both within-pair and extra-pair copulations of this owl, and used a set of microsatellite loci to assign the parentage of 200 offspring from 108 families collected between 1999 and 2004. Among copulations for which we could identify both participants, 19.77% were EPC. However, no EPC was observed in the period just before egg laying. We found only two cases of parentage mismatch among 108 broods. The first case was most likely a case of brood usurpation, which would be the first case reported in the Strigidae. The second case was an EPF resulting in one offspring. Our study found that parentage mismatch in the Lanyu scops owls to be extremely low, therefore reproductive success can be estimated accurately by simply counting chicks in nests.     

Genetic and Social Monogamy – Does It Occur Without Mate Guarding in the Ringed Plover?

Among birds, waders (suborder Charadrii) show a remarkable variation in social mating systems. Their genetic mating systems are, however, less well known, especially in socially monogamous species. Here, we use DNA fingerprinting and behavioral studies to examine genetic parentage and male mate guarding in the ringed plover Charadrius hiaticula , a monogamous wader with biparental care. None of the putative parents was excluded as a genetic parent of the chicks attended (57 young from 21 families). Statistical resampling supported that extra-pair parentage occurs only rarely, if ever, in the ringed plover. We found no evidence for male mate guarding by close following as a paternity assurance strategy. Lack of extra-pair paternity in the ringed plover is therefore probably not a consequence of male mate guarding, but of high costs and/or low benefits from extra-pair copulations for females.     

Extra-pair paternity in monogamous and polygynous Savannah sparrows,Passerculus sandwichensis

Extra-pair paternity can influence mating systems by affecting the fitness costs associated with polygyny. Polygyny is disadvantageous to males when the time and energetic demands of multiple pairings decrease either a male's success at gaining extra-pair fertilizations or his ability to ensure paternity among harem members. In Savannah sparrows,Passerculus sandwichensison Kent Island, New Brunswick, Canada, multilocus DNA fingerprinting of 136 adults and young revealed substantial female infidelity: overall, 31 of 92 young (33.7%) in 15 of 24 nests (62.5%) were the product of extra-pair fertilizations. Male mating status was a strong predictor of paternity. Each of seven monogamous females produced at least one extra-pair offspring, but only six of 11 primary females (54.5%) and two of six secondary females (33.3%) were unfaithful. As a result, nearly 80% of the young in nests of polygynous males resulted from within-pair fertilizations, compared with only 40% of the young in nests of monogamous males. Kent Island Savannah sparrows are simultaneously polygynous, and the absence of paternity costs associated with polygyny is surprising. The observed pattern of paternity suggests the operation of female choice, although male control of parentage cannot be excluded.     

Steller Sex: Infidelity and Sexual Selection in a Social Corvid (Cyanocitta stelleri)

Genetic analysis of avian mating systems has revealed that more than 70% of monogamous species show incidence of offspring parentage that does not match the social partner. Extra-pair parentage (EPP) has been linked to a variety of factors, including size and symmetry of ornamental traits, coloration, resource availability, and local conspecific density. We examined how ornamental plumage traits of individual Steller''s jays (Cyanocitta stelleri) and territory characteristics influence genetic fidelity of socially monogamous pairs. We used seven highly polymorphic microsatellite markers to assign paternity to 79 offspring, and identified 12 (15.2%) as extra-pair young (EPY). Steller''s jays with extra-pair young had significantly lower values of feather brightness and hue, indicating more ultraviolet-blue shifted coloration, and nested in closer proximity to the forest edge than Steller''s jays with no detected EPY. Body size, crest height, asymmetry of ornamental crest stripes, as well as vegetative composition of territories and their proximity to supplemental feeders appeared to have little relationship to EPP. These results indicate that extra-pair parentage plays a role in the evolution of secondary sexual characteristics in both sexes, and suggest local density and availability of resources may influence Steller''s jay mating dynamics.     

Using probability modelling and genetic parentage assignment to test the role of local mate availability in mating system variation

The formal testing of mating system theories with empirical data is important for evaluating the relative importance of different processes in shaping mating systems in wild populations. Here, we present a generally applicable probability modelling framework to test the role of local mate availability in determining a population's level of genetic monogamy. We provide a significance test for detecting departures in observed mating patterns from model expectations based on mate availability alone, allowing the presence and direction of behavioural effects to be inferred. The assessment of mate availability can be flexible and in this study it was based on population density, sex ratio and spatial arrangement. This approach provides a useful tool for (1) isolating the effect of mate availability in variable mating systems and (2) in combination with genetic parentage analyses, gaining insights into the nature of mating behaviours in elusive species. To illustrate this modelling approach, we have applied it to investigate the variable mating system of the mountain brushtail possum (Trichosurus cunninghami) and compared the model expectations with the outcomes of genetic parentage analysis over an 18-year study. The observed level of monogamy was higher than predicted under the model. Thus, behavioural traits, such as mate guarding or selective mate choice, may increase the population level of monogamy. We show that combining genetic parentage data with probability modelling can facilitate an improved understanding of the complex interactions between behavioural adaptations and demographic dynamics in driving mating system variation.     

Correlates of genetic monogamy in socially monogamous mammals: insights from Azara's owl monkeys

Understanding the evolution of mating systems, a central topic in evolutionary biology for more than 50 years, requires examining the genetic consequences of mating and the relationships between social systems and mating systems. Among pair-living mammals, where genetic monogamy is extremely rare, the extent of extra-group paternity rates has been associated with male participation in infant care, strength of the pair bond and length of the breeding season. This study evaluated the relationship between two of those factors and the genetic mating system of socially monogamous mammals, testing predictions that male care and strength of pair bond would be negatively correlated with rates of extra-pair paternity (EPP). Autosomal microsatellite analyses provide evidence for genetic monogamy in a pair-living primate with bi-parental care, the Azara''s owl monkey (Aotus azarae). A phylogenetically corrected generalized least square analysis was used to relate male care and strength of the pair bond to their genetic mating system (i.e. proportions of EPP) in 15 socially monogamous mammalian species. The intensity of male care was correlated with EPP rates in mammals, while strength of pair bond failed to reach statistical significance. Our analyses show that, once social monogamy has evolved, paternal care, and potentially also close bonds, may facilitate the evolution of genetic monogamy.     

Sequential mating patterns suggest extra-pair mating is not part of a mixed reproductive strategy by female red-winged blackbirds

Studies aimed at determining why female birds often produce offspring sired by males other than their social mates generally compare traits of social and genetic mates. Here I examine paternity patterns in nests of the same female red-winged blackbirds (Agelaius phoeniceus) in successive breeding seasons. Returning females preferentially selected their former social mates as their new social mates when those males were present. However, paternity patterns were much less consistent. A female''s behaviour (faithful versus unfaithful) in one year did not predict her behaviour the following year. Females unfaithful in successive years did not prefer the same extra-pair males. Females unfaithful in one year that switched social mates the next year did not preferentially choose their former extra-pair mates as their new social mates. By switching genetic mates, females did not generally improve the quality of their mates. These results, together with previous analyses, suggest that female blackbirds in this population have little control over extra-pair mating. Although females may benefit from extra-pair mating because extra-pair males are generally longer lived, paternity patterns in this population are not consistent with extra-pair mating being part of a finely tuned female reproductive strategy.     

High levels of genetic monogamy in the group-living Australian lizard Egernia stokesii

The Australian lizard Egernia stokesii lives in spatially and temporally stable groups of up to 17 individuals. We have recently shown that these groups are comprised of breeding partners, their offspring and, in some cases, highly related adults, providing the first genetic evidence of a family structure in any lizard species. Here we investigated the mating system of E. stokesii using data from up to eight polymorphic microsatellite loci and tested the hypothesis that breeding partners are monogamous both within and between mating seasons. Among 16 laboratory-born litters from field collected gravid females from two sites in South Australia, 75% had a single male parent and no male contributed to more than one litter, indicating a high level of genetic monogamy within a season. Additional analyses of field caught individuals, captured between 1994 and 1998, enabled assignment of parentage for 70 juveniles and subadults. These data showed that most young (88.6%) had both parents from within the same group and that high proportions of males (88.9%) and females (63.6%) have multiple cohorts of offspring only with the same partner. Our results suggest that monogamy both within and between seasons is a common mating strategy of E. stokesii and that breeding partners maintain stable associations together and with multiple cohorts of their offspring over periods of up to at least 5 years.     

No evidence of immediate fitness benefits of within-season divorce in monogamous birds

Individuals of socially monogamous species can correct for suboptimal partnerships via two secondary mating strategies: divorce and extra-pair mating, with the former potentially providing both genetic and social benefits. Divorcing between breeding seasons has been shown to be generally adaptive behaviour across monogamous birds. Interestingly, some pairs also divorce during the breeding season, when constraints on finding a new partner are stronger. Despite being important for a comprehensive understanding of the evolution of social monogamy, whether within-season divorce is adaptive and how it relates to extra-pair mating remains unknown. Here, we meta-analysed 90 effect sizes on within-season divorce and breeding success, extracted from 31 studies on 24 species. We found no evidence that within-season divorce is adaptive for breeding success. However, the large heterogeneity of effect sizes and strong phylogenetic signal suggest social and environmental factors—which have rarely been considered in empirical studies—may play an important role in explaining variation among populations and species. Furthermore, we found no evidence that within-season divorce and extra-pair mating are complementary strategies. We discuss our findings within the current evidence of the adaptiveness of secondary mating strategies and their interplay that ultimately shapes the evolution of social monogamy.     

Mixed reproductive strategies of the Common moorhen on a microscale as revealed by genetic data

External factors shaping reproductive strategies within a population are still poorly understood. How individuals use space and where they decide to build a nest may influence reproductive strategies, as individuals that are close in space may more frequently interact socially. Here, we investigated a population (n = 58 from 15 nests) of the Common moorhen in the Loir river (Western France) using microsatellite data (54 alleles). We found a surprisingly low level of genetic monogamy, a low relatedness among offspring in some nests and a low relatedness between the social parents and the offspring. Nest heterozygosity was highest close to the geographic center of the population. The mating strategies of the Common moorhen were highly variable, despite the social monogamy of the species, and were, to some extent, influenced by the microspatial structure. We discuss how our results contribute to the understanding of parent–offspring and offspring–offspring relationships.     

Monogamy in black vultures: genetic evidence from DNA fingerprinting

Recent research has indicated that avian mating systems maycommonly deviate from monogamy due to extrapair fertilizations(EPFs). Because the majority of avian species have long beenconsidered monogamous, accurate measurement of the frequencyof EPFs in a variety of species is important to enhance understandingof the evolution of avian mating systems. We used DNA fingerprintingto investigate the apparently monogamous mating system of blackvultures (Coragyps airaius) by assaying parentage within severalnuclear families. Monogamy is suggested in black vultures becausemated pairs exhibit long-term pair bonding and year-round association,and share incubation and nestling feeding duties equally. Thirtytwobreeders and 36 nestlings representing 16 complete nuclear familieswere tagged for individual identification and sampled for DNAanalysis using 2 restriction enzymes and 3 probes for hypervariableregions. Putative parents were assigned parentage in all cases.We empirically examined the probability of detecting EPFs bycomparing nestlings' fingerprints to those of a putative parentand another randomly chosen adult. All putative parents couldbe assigned with 95%confidence and all outside adults couldbe similarly excluded. There is therefore no evidence for successfulEPFs in this population, indicating a mating system that doesnot deviate from strict monogamy. The complex social behaviorof black vultures may eliminate the opportunity for EPFs dueto the prohibition of copulations in the presence of relatives.     

Agricultural management affects evolutionary processes in a migratory songbird

Hay harvests have detrimental ecological effects on breeding songbirds, as harvesting results in nest failure. Importantly, whether harvesting also affects evolutionary processes is not known. We explored how hay harvest affected social and genetic mating patterns, and thus, the overall opportunity for sexual selection and evolutionary processes for a ground-nesting songbird, the Savannah sparrow ( Passerculus sandwichensis ). On an unharvested field, 55% of females were in polygynous associations, and social polygyny was associated with greater rates of extra-pair paternity (EPP). In this treatment, synchrony explained variation in EPP rates, as broods by more synchronous females had more EPP than broods by asynchronous females. In contrast, on a harvested field, simultaneous nest failure caused by haying dramatically decreased the overall incidence of EPP by increasing the occurrence of social monogamy and, apparently, the ability of polygynous males to maintain paternity in their own nests. Despite increased social and genetic monogamy, these haying-mediated changes in mating systems resulted in greater than twofold increase in the opportunity for sexual selection. This effect arose, in part, from a 30% increase in the variance associated with within-pair fertilization success, relative to the unharvested field. This effect was caused by a notable increase (+110%) in variance associated with the quality of social mates following simultaneous nest failure. Because up to 40% of regional habitat is harvested by early June, these data may demonstrate a strong population-level effect on mating systems, sexual selection, and consequently, evolutionary processes.     

Genetic and behavioural evidence of monogamy in a mammal,Kirk's dik-dik (Madoqua kirkii).

Little is known about the mating behaviour of monogamous mammals. Here, we present behavioural and genetic evidence of fidelity in a socially monogamous dwarf antelope, Kirk''s dik-dik. DNA microsatellite analysis revealed no evidence of extra-pair paternity (EPP) in dik-diks: mothers'' partners matched the paternal genotype in all 12 juveniles tested. One likely reason for the absence of EPP is that males guard their mates closely during oestrus and over-mark all female scent, thereby reducing the likelihood of other males attempting to mate. In addition, males may be limited in their ability to search for extra-pair populations (EPCs) by activities associated with pair-bond maintenance. Year-round, males maintained proximity within pairs, followed their females'' activity patterns, and spent approximately 64% of their time with their partners. However, males did attempt to obtain EPCs when the opportunity arose, and genetic monogamy in dik-diks is probably best explained by the behaviour of females: in contrast to many monogamous female birds, female dik-diks do not appear to seek EPC partners. We propose that females avoid extra-pair males because they are unable to mate with them without instigating a potentially dangerous conflict.     

Comparison of the mating systems and breeding behavior of a resident and a migratory tropical flycatcher

ABSTRACT.   Little is known about the genetic mating systems of tropical passerines and how they vary among species. We studied the Lesser Elaenia ( Elaenia chiriquensis ) and the Yellow-bellied Elaenia ( E. flavogaster ) near Gamboa, Panama. These species breed in the same habitat, but Lesser Elaenias are intratropical migrants with seasonal territories and Yellow-bellied Elaenias are permanent residents that remain paired and defend territories throughout the year. Lesser Elaenias exhibited greater breeding synchrony (15–18 %) than Yellow-bellied Elaenias (9–10%). For Lesser Elaenias, 10 of 15 (67%) nests contained extra-pair young and 14 of 38 (37%) young resulted from extra-pair fertilizations (EPFs). In contrast, only one extra-pair nestling (4%, N = 24 nestlings) was found in 13 Yellow-bellied Elaenia nests. Neither species exhibited strong mate guarding. The higher rate of EPFs in Lesser Elaenias is consistent with the hypothesis that year-round territorial tropical passerines with low breeding synchrony have little or no extra-pair behavior compared with species that breed seasonally. Although the low singing rates of Lesser Elaenias (7 songs/h) suggest that this not an important cue for female extra-pair mate choice, the role of conspicuous male dawn song remains to be investigated. Further studies of tropical passerines are needed to help disentangle the effects of synchrony, density, and other ecological and behavioral factors that have influenced the evolution of extra-pair mating systems in passerines.     

Extra-pair paternity does not result in differential sexual selection in the mutually ornamented black swan (Cygnus atratus)

We studied patterns of parentage in 85 broods (332 cygnets) of black swans during three breeding seasons, using a set of eight polymorphic microsatellite markers. We detected both intraspecific brood parasitism (IBP; < 5% of cygnets per year) and extra-pair paternity (EPP). In these years, 10-17% (mean = 15.1%) of cygnets resulted from EPP, and 27-40% (mean 37.6%) of broods contained at least one extra-pair cygnet. Compared with levels of EPP in closely related species with similar life histories, these values are unexpectedly high. EPP in black swans appears unrelated to ecological factors (breeding density and synchrony) or genetic factors (genetic similarity between pair members or genetic quality of the offspring). We found no evidence that a mutual sexual feather ornament known to play a role in social mate choice in black swans (curled wing feathers) is involved in extra-pair mate choice. EPP does not lead to greater variance in reproductive success in males, relative to females in this species. We therefore suggest that EPP does not result in differential sexual selection on males and females, explaining why they are ornamented to the same degree.     

Multiple mating and a low incidence of cuckoldry for nest-holding males in the two-spotted goby, Gobiusculus flavescens

Background  

A major question in behavioural ecology concerns the relationship between genetic mating systems and the strength of sexual selection. In this study, we investigated the genetic mating system of the two-spotted goby (Gobiusculus flavescens), a useful fish model for the study of sexual selection whose genetic mating system remains uncharacterized. We developed four polymorphic microsatellite markers and used them to conduct parentage analyses on 21 nests collected during the breeding season to examine the rates of multiple mating by males and to test for evidence of alternative mating strategies.     

Social common mole-rats enhance outbreeding via extra-pair mating

Females in many species engage in matings with males that are not their social mates. These matings are predicted to increase offspring heterozygosity and fitness, and thereby prevent the deleterious effects of inbreeding. We tested this hypothesis in a cooperative breeding mammal, the common mole-rat Cryptomys hottentotus hottentotus. Laboratory-based studies suggested a system of strict social monogamy, while recent molecular studies indicate extensive extra-pair paternity despite colonies being founded by an outbred pair. Our data show that extra-pair and within-colony breeding males differed significantly in relatedness to breeding females, suggesting that females may gain genetic benefits from breeding with non-resident males. Extra-colony male mating success was not based on heterozygosity criteria at microsatellite loci; however, litters sired by extra-colony males exhibited increased heterozygosity. While we do not have the data that refute a relationship between individual levels of inbreeding (Hs) and fitness, we propose that a combination of both male and female factors most likely explain the adaptive significance of extra-pair mating whereby common mole-rats maximize offspring fitness by detecting genetic compatibility with extra-pair mates at other key loci, but it is not known which sex controls these matings.     

Contrasting levels of extra-pair paternity in mainland and island populations of the house sparrow (Passer domesticus): is there an 'island effect'?

Despite the many studies that have investigated the genetic mating system of socially monogamous birds, very little is known about the underlying causes of extra-pair paternity and few studies have attempted to test those hypotheses which have been suggested. This study describes die analysis of die genetic mating system of two populations of the house sparrow [Passer domesticus) , and uses the results from four other populations to test existing hypodieses using an intra-specific comparative approach. The parentage analysis was conducted using a combination of published and newly presented microsatellite loci isolated from the house sparrow. One population in Kentucky, U.S.A. was found to contain what may be considered to be a typical level of extra-pair paternity for mis species (10.5%, 19/185 offspring). The second, a population on the island of Lundy, UK, exhibited a very low level (1.3%, 4/305 offspring), significandy lower dian that in all the other populations studied so far. The finding of such diverse rates of extra-pair paternity, along with the existing estimates from ofher populations, has allowed us to test the effects of breeding density and genetic variation on die level of extra-pair paternity. We found no effect of either factor on the frequency of extra-pair paternity in the house sparrow, leaving the cause of this variation open to fresh ideas.     

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.