Extra-pair paternity and the evolution of testis size in a behaviorally monogamous tropical mammal,the large treeshrew (<Emphasis Type="Italic">Tupaia tana</Emphasis>)

Monogamy is rare in mammals (<5% spp.) but occurs in greater frequency among primates (15%) and their close relatives, the treeshrews (100%; Order: Scandentia). Two genetic studies of parentage in monogamous primates revealed high rates of extra-pair paternity (EPP), but to date parentage has not been studied in a treeshrew species. I analyzed the genetic parentage of 22 offspring from two populations of large treeshrews in Sabah, Malaysia (NE Borneo), using seven autosomal microsatellite loci and one mitochondrial DNA marker. Half of these offspring were sired by males that were not the presumed partner of the mother (50% EPP), and three litters exhibited evidence of multiple paternity. However, comparative analysis indicated that the high rate of EPP in Tupaia tana is not associated with intense sperm competition. Relative testis size of treeshrews was similar to testis size in 22 primate species with uni-male mating systems but smaller than 44 primates with multi-male mating systems. After factoring out the effects of body size and phylogeny, I also found that the evolution of multi-male mating systems was significantly associated with the evolution of larger testis size. Male–female pairs of T. tana occupy joint territories but forage and sleep alone (“dispersed pair-living”), and I argue that this form of behavioral monogamy renders mate guarding ineffective. The adaptive advantages of behavioral monogamy likely differ from the advantages driving EPP in large treeshrews. However, small testis size suggests that behavioral monogamy is not masking a dispersed multi-male mating system in this species.     

Extra-pair paternity and the opportunity for sexual selection in a socially monogamous bird (Dendroica petechia)

We used multi-locus DNA fingerprinting to characterise the genetic mating system of the socially monogamous yellow warbler (Dendroica petechia). Over 2 years there were no instances of brood parasitism, but 59% of families (n = 90) contained extrapair sired young and 37% of offspring (n = 355) were of extra-pair paternity. Most hypotheses for extra-pair mating in monogamous species assume a paternity benefit to extra-pair sires, and focus on the benefit(s) to females. However, the assumption of male benefit has been little tested. Among yellow warblers, known extra-pair sires were just as likely to be cuckolded as any male in the population, and there was at least one reciprocal exchange of extra-pair paternity. Nevertheless, among known extra-pair sires, the paternity gains from extra-pair paternity were, on average, greater than the losses in their own families. These results show there is a paternity benefit to certain males. However, the benefit is not absolute but relative and therefore more difficult to measure. The results also suggest that patterns of extra-pair fertilisation are not determined by female choice alone. Most confirmed extra-pair mates were territorial neighbours, but some resided as far as three territories apart, and greater spatial separation was implied in other cases. Thus, the opportunity for extra-pair mating is great. We estimate that as a result of extra-pair fertilisations, variance in male mating success is increased somewhere between 3-fold and 15-fold over that which would result from within-pair reproduction alone. These findings affirm the potential importance of extra-pair reproduction for sexual selection in monogamous species and they support earlier suggestions that extra-territorial forays by male yellow warblers are for the purpose of extra-pair mating.     

Extra-pair paternity and male characteristics in the pied flycatcher

The pied flycatcher (Ficedula hypoleuca) is sexually dichromatic with extreme variation in male plumage coloration. The benefit for males of having black plumage is controversial, and few studies have found evidence for a sexual selection benefit of being black rather than brown. However, blacker males may be better able to achieve extra-pair fertilizations (EPFs), which may be an important component of sexual selection. We studied the role of EPFs in sexual selection in the pied flycatcher by establishing a set-up where two males with different back coloration (blacker vs browner) bred simultaneously near each other. DNA fingerprinting analysis revealed that 11% of offspring resulted from EPFs, and that 22% of broods included extra-pair young (EPY) among 36 nests containing 223 nestlings. We found no evidence that browner males suffered more often from EPFs than blacker males. There was no correlation of male or female morphology or age with EPF frequency. However, breeding pairs with low genetic similarity had EPY in their nests significantly more often. Thus we argue that females paired with genetically dissimilar males may try to avoid the effects of extreme outbreeding by seeking extra-pair copulations (EPCs). Alternatively, incompatibility between genetically dissimilar mates may simply expose females to more extra-pair copulations.     

Extra-pair paternity, offspring mortality and offspring sex ratio in the socially monogamous coal tit (Parus ater)

Females of many socially monogamous bird species commonly engage in extra-pair copulations. Assuming that extra-pair males are more attractive than the females’ social partners and that attractiveness has a heritable component, sex allocation theory predicts facultative overproduction of sons among extra-pair offspring (EPO) as sons benefit more than daughters from inheriting their father’s attractiveness traits. Here, we present a large-scale, three-year study on sex ratio variation in a passerine bird, the coal tit (Parus ater). Molecular sexing in combination with paternity analysis revealed no evidence for a male-bias in EPO sex ratios compared to their within-pair maternal half-siblings. Our main conclusion, therefore, is that facultative sex allocation to EPO is absent in the coal tit, in accordance with findings in several other species. Either there is no net selection for a deviation from random sex ratio variation (e.g. because extra-pair mating may serve goals different from striving for ‘attractiveness genes’) or evolutionary constraints preclude the evolution of precise maternal sex ratio adjustment. It is interesting to note that, however, we found broods without EPO as well as broods without mortality to be relatively female-biased compared to broods with EPO and mortality, respectively. We were unable to identify any environmental or parental variable to co-vary with brood sex ratios. There was no significant repeatability of sex ratios in consecutive broods of individual females that would hint at some idiosyncratic maternal sex ratio adjustment. Further research is needed to resolve the biological significance of the correlation between brood sex ratios and extra-pair paternity and mortality incidence, respectively.     

Extra-pair paternity in the monogamous alpine marmot (Marmota marmota): the roles of social setting and female mate choice

Extra-pair paternity (EPP) can be influenced by both social setting and female mate choice. If evidence suggests that females try to obtain extra-pair copulations (EPCs) in order to gain genetic benefits when mated to a homozygous and/or to a related male, females may not be able to choose freely among extra-pair mates (EPMs) as the social mate may constrain female access to EPMs. In this study, we investigated, first, how EPP depended on social setting and specifically on the number of subordinate males in the family group in a highly social and monogamous mammal, the alpine marmot. Second, we investigated how EPP depended on female mate choice for genetic benefits measured as male mate-heterozygosity and within-pair relatedness. Our results reveal, first, that EPP depended on the social setting, increasing with the number of subordinate males. Second, EPPs were related to relatedness between mates. Third, EPMs were found to be more heterozygous than within-pair males. Thus, social setting may constrain female choice by limiting opportunities for EPC. However, after accounting for social confounding factors, female choice for genetic benefits may be a mechanism driving EPP in monogamous species.     

Extra-pair paternity and tail ornamentation in the barn swallow Hirundo rustica

Females of socially monogamous species may copulate with attractive non-mates to obtain access to the genes of such males, and a preference for attractive copulation partners may result in sexual selection. Extra-pair copulations are common in the socially monogamous barn swallow Hirundorustica, and a 2-year study of paternity using multi-locus DNA fingerprinting demonstrated that 33% of 63 broods and 28% of 261 offspring were sired by extra-pair males. The frequency of extra-pair offspring within broods was highly skewed with the majority of all broods having either no extra-pair offspring or only extra-pair offspring. Individual pairs were consistent in their frequency of extra-pair paternity among broods, and the repeatability of extra-pair paternity of multiple broods of the same female was statistically significant. The proportion of extra-pair offspring was negatively related to the tail length of the male attending the nest. Behavioural observations showed that extra-pair fertilizations were more likely in broods raised by females that had been observed to engage in extra-pair copulations. The frequency of extra-pair offspring was unrelated to the intensity of two male paternity guards, mate guarding and the rate of intra-pair copulations. In an analysis of extra-pair paternity and male parental care in different broods of the same male, male barn swallows fed their offspring relatively less frequently if the brood contained more extra-pair offspring. Therefore, female barn swallows pursue extra-pair copulations with attractive males, which may result in sexual selection, even though extra-pair paternity is costly for females due to the reduction of paternal care by their social mates. Received: 24 January 1997 / Accepted after revision: 2 August 1997     

Extra-pair paternity,sperm competition and the evolution of testis size in birds

Sperm competition should select for increased sperm production if the probability of fertilization by a specific male is proportional to the relative number of sperm inseminated. A review of the literature generally supports the predicted positive association between sperm production or allocation and various measures of the presumed intensity of sperm competition. However, it is not clear how increased sperm competition is related to extra-pair paternity, and it remains unknown whether certainty of paternity should be associated with relative testis size. Based on a large sample of bird species with information on extra-pair paternity gathered from the literature, we demonstrate that testis mass is related positively to the level of extra-pair paternity, after controlling for body size and phylogeny. Although large testes may be necessary to avoid sperm depletion in species in which males frequently engage in multi-pair copulations, we argue that selection has favoured increased testis mass in situations of more intense sperm competition in order to retaliate against copulations by rival males. The fact the males are not always successful in retaliating against rival ejaculates further suggests that females may largely control the allocation of paternity in birds and that increased sperm production by males may simply be a male strategy to make the best of a bad situation.     

Extra-pair paternity and intraspecific brood parasitism in wild zebra finches Taeniopygia guttata,revealed by DNA fingerprinting

Summary The frequency of extra-pair parentage in a wild population of zebra finches Taeniopygia guttata was examined by DNA fingerprinting. A total of 25 families, comprising 16 pairs of parents and 92 offspring (in broods of 1 to 6) were examined. Ten cases of extra-pair parentage, presumed to constitute intraspecific brood parasitism, were detected (10.9% of offspring or 36% of broods), including one possible instance of quasi-parasitism (parasitism by a female fertilized by the male nest owner). The average number of parasitic eggs per clutch detected by fingerprinting was 1.10±0.32 SD, very similar to the one egg difference in average clutch size between parasitised (6.0±0.82) and unparasitised nests (5.0±0.95). Two cases of extra-pair paternity (EPP) were detected among 82 offspring whose maternity was confirmed: 2.4% of offspring, or 8% of broods. In both cases EPP accounted for only a single offspring within a brood. Behavioural observations show that EPP occurs through extra-pair copulation rather than rapid mate switching. The results are discussed in the light of what is known about the fertile period and sperm precedence patterns in this species. Offprint requests to: T.R. Birkhead     

Small testes size despite high extra-pair paternity in the pair-living nocturnal primate Phaner furcifer

Sperm competition will be the inevitable consequence of polyandrous mating behavior if two or more males inseminate a single female. It has been demonstrated for a wide variety of animals that males adapt to this situation behaviorally, physiologically and morphologically, e.g. by evolving relatively large testes size to produce more sperm. All pair-living primates investigated so far were found to have relatively small testes, suggesting a monandrous mating system. We investigated the relationship between extra-pair paternity (EPP) rate as a measure of sperm competition intensity and relative testes size in a pair-living primate, the fork-marked lemur (Phaner furcifer). Paternity exclusion analyses for seven offspring using six polymorphic DNA-microsatellite markers suggested a high EPP rate. Female nocturnal travel distances were longer during the mating season, suggesting that females take an active role in achieving extra-pair copulations (EPCs). Surprisingly, fork-marked lemur testes size was relatively small compared to 23 other lemuroid primates, a result that is in contrast to predictions of sperm competition theory. Neither possible behavioral and morphological adaptations to an alternative paternity guard (i.e. mate guarding), nor sampling biases, phylogenetic constraints, and population density effects explain the absence of large testes in a species with high EPP, a phenomenon also known from birds with moderate to low EPP rates. We conclude that more data are needed on the frequency of EPCs, the timing of in-pair and extra-pair copulations, as well as the role of female choice, to explain why males of some species apparently do not adapt to sperm competition.Communicated by S. Alberts     

Enhancement of reproductive success through mate choice in a social rock-wallaby, Petrogale assimilis (Macropodidae) as revealed by microsatellite markers

The reason why a female who is socially paired to one particular male seeks extra-pair copulations (EPCs) with others has important implications in life history models and to the study of behaviour. The Allied rock-wallaby, Petrogale assimilis, lives in spatially isolated colonies in tropical north Queensland, Australia. Extensive observations of a colony at Black Rock showed that intense behavioural bonding occurs between pairs of adult males and females; about two-thirds of males paired with one female, the remainder paired with two females simultaneously. Single-locus microsatellite profiling determined the paternity of 63 offspring from 21 females for which long-term behavioural data were available. One-third of the young were fathered by males which were not paired socially with the mother. The mating system was heterogeneous: (1) all offspring of 11 females were fathered by the mother's partner, (2) all young of 5 females were fathered by extra-pair males, and (3) only some of the young of 5 females were fathered by their regular consort. Analysis of individual longitudinal demographic records showed that females whose young were always fathered by their consort had higher reproductive success than those whose young were always fathered as a result of (EPCs). However, females with some offspring fathered by their regular consort and others via EPCs had the highest probability of raising young to independence. These females were significantly more likely to have an offspring fathered as a result of an EPC if their previous young had failed to survive to pouch emergence. These results are consistent with the hypothesis that females choose mates for their genetic quality. Comparison of the males with which these females sought EPCs and the regular consorts suggested that arm length rather than body weight or testes size was used as the index of genetic quality. Results from a second colony of rock-wallabies in which the reproductive rate was accelerated were also consistent with the genetic-quality hypothesis. These results imply that by choosing better-quality fathers irrespective of social pairing, females are able to maximise their overall lifetime reproductive success, and presumably, those of their offspring. Received: 8 June 1997 / Accepted after revision: 28 February 1998     

Mating patterns and reproductive success in the bushy-tailed woodrat (Neotoma cinerea), as revealed by DNA fingerprinting

The mating patterns and reproductive success of the bushy-tailed woodrat (Neotoma cinerea) were investigated over a 3-year period (1992–1994) using DNA fingerprinting. Paternity was determined by genetic analysis of 58 juveniles of known maternity from 35 litters. Analysis of DNA fingerprints revealed that all offspring within a litter were fathered by a single male; the statistical probability of detecting multiple males mating with a female was high, indicating that multiple paternity would have been detected had it occurred. However, individual males did not father more than one litter from a given female either within or between years. At least 75% of females and 57% of males successfully produced offspring each year. The finding that all littermates are first-order relatives may contribute to the high level of female cooperation in this species. Received: 28 May 1997 / Accepted after revision: 22 March 1998     

Low paternity in the hornet Vespa crabro indicates that multiple mating by queens is derived in vespine wasps

Queen mating frequency was studied in the European hornet, Vespa crabro, by analyzing four DNA microsatellite loci in 20 workers from each of 14 nests. Queens were found to be predominantly singly mated (9/14), although double (4/14) and triple mating (1/14) also occurred. For most multiply mated queens, paternity was significantly biased with the majority male fathering on average 80% of the female offspring. The population-wide effective mating frequency was therefore low (1.11), and sister-sister relatedness high (0.701 ± 0.023 SE). Low effective mating frequency in Vespa, in combination with data from other vespines, suggests that high paternity frequency is derived in the group. Some problems with the non-detection of fathers, where the queen was not sampled or shared alleles with males, are analyzed. Received: 16 November 1998 / Received in revised form: 29 March 1999 / Accepted: 12 April 1999     

Sexual selection in a socially monogamous bird: male color predicts paternity success in the mountain bluebird, <Emphasis Type="Italic">Sialia currucoides</Emphasis>

Ornamental traits are thought to evolve because they give individuals an advantage in securing multiple mates. Thus, the presence of ornamentation among males in many monogamous bird species presents something of a conundrum. Under certain conditions, extra-pair paternity can increase the variance in reproductive success among males, thus increasing the potential for sexual selection to act. We addressed this possibility in the mountain bluebird (Sialia currucoides), a socially monogamous songbird in which males possess brilliant ultraviolet (UV)-blue plumage. Specifically, we asked whether a male’s success at siring offspring within his own nest and within the nests of other males was related to his coloration. In pairwise comparisons, males that sired extra-pair offspring were not more colorful than the males that they cuckolded. However, males that sired at least one extra-pair offspring were, on average, brighter and more UV-blue than males that did not sire extra-pair offspring. Brighter, more UV-blue males sired more offspring both with their own mate and tended to sire more offspring with extra-pair mates and thus sired more offspring overall. Our results support the hypothesis that the brilliant UV-blue ornamental plumage of male mountain bluebirds evolved at least in part because it provides males with an advantage in fertilizing the eggs of multiple females.     

Mating system of the cooperatively breeding noisy miner Manorina melanocephala,as revealed by DNA profiling

In this study we examined parentage within broods of the cooperatively breeding noisy miner using multi-locus DNA profiling. Previous studies of noisy miners described them as highly promiscuous, leading to the suggestion that promiscuous mating behaviour was a tactic used by females to recruit males as provisioners to their nests (Dow 1978). At our study site in south-east Queensland, Australia, we found that both multiple and extra-group paternity (i.e. a female mating with a male outside the group of male provisioners at her nest) were rare. In nests where multiple paternity was possible (i.e. clutch size > 1) 97% of 31 broods were sired by only a single male. Overall, 96.5% of all nestlings (n = 85) were the result of monogamous matings. Also, at the vast majority of nests, the male that sired the nestlings was also the main provisioner among all male nest attendants. Our results show that the mating system of the noisy miner can no longer be considered cooperative polyandry (Brown 1987) but is clearly genetic monogamy. We discuss the implications of this finding for understanding the complex social system of this species.     

Alternative reproductive tactics in male common shrews: relationships between mate-searching behaviour,sperm production,and reproductive success as revealed by DNA fingerprinting

The common shrew (Sorex araneus) is a solitary small mammal with a promiscuous mating system. Previous studies of this species suggest that females typically mate multiply, and that males may adopt alternative mate-searching tactics. We studied two generations of common shrews in a population near Oxford, England. Males were found to adopt two different mate-searching tactics. Those classed as type A occupied relatively small exclusive ranges during March, and made repeated long-distance movements to visit female ranges around the time of first oestrus in April. Males classed as type B established large overlapping ranges in areas of relatively high female density during March, and maintained these ranges throughout April. Type B males were larger than type A males at an early stage of sexual maturation, but there was no difference in the adult body size of the two types of male. Type A males had significantly higher epididymal sperm counts than type B males. Paternity analyses of litters born during the first year of the study reveal that the mean number of offspring fathered by type B males was greater than the mean number fathered by type A males. It is concluded that different mate-searching tactics may be conditional upon the timing of sexual maturation. Differences in sperm production are discussed in relation to sperm competition theory.     

Cryptic hammerhead shark lineage occurrence in the western South Atlantic revealed by DNA analysis

A cryptic lineage of hammerhead shark closely related to but evolutionarily distinct from the scalloped hammerhead (Sphyrna lewini) was recently documented in the western North Atlantic Ocean. Here, we demonstrate using nuclear and mitochondrial DNA sequences that this cryptic lineage also occurs in the western South Atlantic Ocean, extending its distribution >7,000 km from its only previously reported location. Our results also further validate the existence of this evolutionarily distinct hammerhead shark lineage. The southern hemisphere cryptic individuals were 1.6 and 5.8% divergent from S. lewini (sensu stricto) for the nuclear internal transcribed spacer 2 (ITS2) and mitochondrial control region loci, respectively, and formed a strongly supported, reciprocally monophyletic sister group to sympatric S. lewini. Coalescent analysis (ITS2 locus) yielded a divergence estimate of ~4.5 million years between S. lewini and the cryptic lineage. Given expanding concerns about overfishing of the large-bodied hammerhead sharks, this cryptic lineage needs to be formally recognized and incorporated into shark management and conservation planning to avoid the inadvertent, potential extirpation of a unique hammerhead lineage.     

High relatedness and inbreeding in two species of haplodiploid eusocial thrips (Insecta: Thysanoptera) revealed by microsatellite analysis

Relatedness and inbreeding coefficients were estimated for Oncothrips tepperi and O. habrus, two species of eusocial gall-forming thrips, using data from two microsatellite loci. Relatedness between sets of individuals (sexes and castes) for O. tepperi ranged from 0.5 to 0.85 and for O. habrus estimates were centered around 0.5. Multiple mating in O. habrus was implicated in lowering relatedness within a gall. We estimated the inbreeding coefficient to be 0.38 for both species, the highest estimates known for eusocial insects. Our findings imply that high relatedness and inbreeding are important for the evolution and form of social behavior in Australian gall-forming Thysanoptera. Received: 14 November 1997 / Accepted after revision: 14 March 1998