Breeding synchrony and extra-pair mating in red-winged blackbirds

Using data from a 6-year paternity study of red-winged blackbirds, I tested the hypotheses that increased nesting synchrony should either promote extra-pair mating by increasing the advantage of extra-pair mating to females, or decrease extra-pair mating by constraining males from seeking extra-pair copulations. Contrary to these hypotheses, the occurrence of extra-pair paternity did not vary with nesting synchrony over the breeding season, or vary with the number of synchronous nests within territories or within marshes, or with nesting order on territories. However, for nearly all nests with extra-pair young, there were fewer females synchronous with that nest on the cuckolder's territory than on the territory of the cuckolded male. This “advantage” of a synchrony difference was less pronounced for older males that cuckolded younger males, particularly when the two males were not neighbors. Collectively, these results suggest that breeding synchrony affects extra-pair mating by affecting mate guarding, but that breeding synchrony alone can not be used to predict which females are more likely to engage in extra-pair mating, nor with which extra-pair males they will mate. Understanding why extra-pair mating by older males is less affected by breeding synchrony may explain much about both the proximate and ultimate causes of extra-pair mating in red-winged blackbirds. Received: 7 June 1996 / Accepted after revision: 25 November 1996     

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.     

Condition-dependent control of paternity by female purple martins: implications for coloniality

Proposed causal links between extra-pair copulation (EPC) and colony formation in socially monogamous birds hinge on the question of which sex controls fertilizations. We examined in colonial purple martins Progne subis (1) whether EPCs were forced or accepted by females, and (2) the degree to which apparently receptive females were able to obtain EPCs against their mates’ paternity defenses. Paternity analyses of multilocus DNA fingerprinting confirmed previous findings of a marked relationship between age class and extra-pair fertilizations (EPFs), with young males losing paternity of 43% (n = 53) of their putative offspring compared to 4% (n = 85) by old males. All assignable extra-pair offspring were sired by old males, with one male obtaining most EPFs each year. Contrary to the hypothesis that EPCs are forced, EPF frequency within age class did not increase with seasonal increases in the number of males per fertile female. Whereas the male control hypothesis predicted that the male age class that mate-guarded more would be cuckolded less, the reverse was true: young males guarded significantly more intensely. The male age class difference in cuckoldry could not be explained by the possibility that young and inexperienced females (which are usually paired to young males) were more vulnerable to forced copulation because EPFs were unrelated to female age. These findings suggest that females (1) pair with old males and avoid EPCs, or (2) pursue a mixed mating strategy of pairing with young males and accepting EPCs from old males. The receptivity to EPCs by females paired to young males put them in conflict with their mates. Two factors determined the paternity achieved by young males: (1) the relative size of the male to the female, with young males achieving much higher paternity when they were larger than their mates, and (2) the intensity of mate-guarding. Both variables together explained 77% of the variance in paternity and are each aspects of male-female conflict. Given female receptivity to EPCs, mate-guarding can be viewed as male interference with female mating strategies. We conclude that EPCs are rarely or never forced, but the opportunity for females paired to young males to obtain EPCs is relative to the ability of their mates to prevent them from encountering other males. Evidence of mixed mating strategies by females, combined with other features of the martin mating system, is consistent with the female-driven “hidden lek hypothesis” of colony formation which predicts that males are drawn to colonies when females seek extra-pair copulations. Received: 23 March 1995/Accepted after revision: 14 January 1996     

Song rates of dark-eyed juncos do not increase when females are fertile

Frequency of singing by birds may vary with reproductive stage in ways that reflect variation in the functions of song in intersexual and intrasexual communication. In dark-eyed juncos (Junco hyemalis) high-amplitude song is produced only by males. To investigate the function of this song, we tested whether fertility of females affected singing by their mates or by neighboring males. Using focal observations, song censuses, and radiotracking data, we determined whether song production varied between and among periods when females were fertile and non-fertile. Our findings show that males do not increase song production when their mates are fertile, nor do they increase song production when neighboring females are fertile. These results suggest that male juncos do not signal their intent to defend territories (or mates) more when females are fertile and that they do not use song to advertise to specific potential participants in extra-pair fertilizations. Received: 13 February 1997 / Accepted after revison: 2 May 1997     

Ornamentation predicts reproductive success in female pipefish

In the sex-role reversed pipefish Syngnathus typhle females compete for access to males and males are choosy. Females develop a temporary ornament when competing over mates with other females and when performing nuptial dances with males. This ornament is an amplification of the normal striped pattern in these fishes. We here show experimentally that (1) the contrast of this normal pattern forecasts the extent to which the ornament is shown, (2) contrast and ornamentation honestly signal female quality (egg numbers), (3) contrast and ornamentation accurately predict female mating success, (4) contrast is a phenotypically plastic trait specifically exaggerated under situations of female – female competition, and (5) neither contrast nor ornament are energetically expensive to the females (i.e., they are independent of short-term nutritional status). Hence, as predicted in sex-role reversed species, ornament design is constrained by costs to female fecundity: an energetically demanding ornament would impair on a female's ability to produce eggs. The type of ornament described here is the expected one, costly for reasons other than being energetically expensive to produce. Received: 4 April 1996 / Accepted after revision: 27 October 1996     

Common goldeneyes adjust maternal effort in relation to prior brood success and not current brood size

Parental investment theory predicts that parental effort should be related to the reproductive value of the current brood. This depends on both the number of young and the survival prospects of each of them. Thus parents may provide more care to larger broods either because of (1) the direct effect of brood size per se on reproductive value (the “brood size” hypothesis) or because (2) past mortality, reflected in current brood size, predicts future mortality of the brood and hence its reproductive value (the “brood success” hypothesis). Earlier studies have not attempted to distinguish between these alternatives. We tested the hypotheses in the precocial, nidifugous common goldeneye Bucephala clangula, a species with uniparental female care. Maternal effort was measured as the time spent by the female in rearing the brood. We found that brood size itself is not associated with maternal effort, but that females modify their maternal effort according to the mortality already experienced by the brood, supporting the prediction of the brood success hypothesis. We also found that brood mortality varied considerably between broods and that previous mortality predicts future mortality within broods, basic assumptions of the brood success hypothesis. Received: 30 January 1996 / Accepted after revision: 27 October 1996     

Sexual cohabitation as mate-guarding in the leaf-curling spider Phonognatha graeffei Keyserling (Araneoidea, Araneae)

The leaf-curling spider Phonognatha graeffei incorporates a twisted leaf into the central hub of its orb-web that is used as a retreat. This species is unusual among orb-weaving spiders because males cohabit in the leaf retreat with both immature and mature females, mating with the former shortly after the female molts. Cohabitation appears to be a form of mate-guarding because cohabiting males respond agonistically to rival males that venture onto the web, and their behaviour depends upon the reproductive status of the female; males defending immature females are more aggressive than those defending virgin, adult females. Males copulate with previously mated females for significantly longer than with virgin females. Females may cannibalise cohabiting males, which occurs independently of whether the female has been deprived of food. Females that cannibalise a single male do not have a higher fecundity than non-cannibalistic females. Received: 2 February 1996 / Accepted after revision: 27 October 1996     

Female mate choice in the non-territorial lizard Ameiva plei (Teiidae)

Mate choice by females has been documented in a variety of taxa. Female mate choice in species lacking male resource control or paternal care might occur if preferred males provide protection from harassment. Female mate choice was investigated in a natural population of the non-territorial lizard Ameiva plei (Teiidae). Consort pairs were allowed to form naturally. Consort males were significantly larger than non-consort males. After removal of consort males, the “abandoned” female's reaction to the first male who approached her was recorded. Females rejected all small males. Female preference for large males was significantly higher than preference for small males. Large males may be better equipped to guard the females from harassment and behavior of large males is less harassing than behavior of small males, thereby affording the female increased foraging time. Received: 21 June 1996 / Accepted after revision: 28 December 1996     

Mate choice games, context-dependent good genes, and genetic cycles in the side-blotched lizard, Uta stansburiana

According to mate choice models, a female should prefer males with traits that are reliable indicators of genetic quality which the sire can pass on to their progeny. However, good genes may depend on the social environment, and female choice for good genes should be context dependent. The side-blotched lizard, Uta stansburiana, exhibits genetically based throat colors (orange, blue, or yellow) that could be used as a sexually selected signal since they reliably predict the genetic quality of mates. The frequencies of male and female morphs cycle between years, and both male and female morphs have an advantage when rare; thus genetic quality will depend on morph frequency. A female should choose a sire that maximizes the reproductive success of both male and female progeny. We examine a game theoretical model that predicts female mate choice as a function of morph frequency and population density. The model predicts the following flexible mate choice rule: both female morphs should prefer rare males in ’boom years’ of the female cycle (e.g., ’rarest-of-N rule’), but prefer orange males in ’crash years’ of the female cycle (’orange-male rule’). Cues from the current social environment should be used by females to choose a mate that maximizes the future reproductive success of progeny, given the social environment of the next generation. We predict that the cue is the density of aggressive orange females. In the side-blotched lizard, cycling mate choice games and context-dependent mate choice are predicted to maintain genetic variation in the presence of choice for good genes. Received: 8 March 2000 / Revised: 26 August 2000 / Accepted: 4 September 2000     

Parentage and paternal care: consequences of intersexual selection in Savannah sparrows?

Empirical relationships between parentage and male parental care are commonly interpreted in the context of life-history models that consider increased offspring survivorship as the only benefit of paternal effort. However, indirect benefits associated with male care can also influence a male's response to cuckoldry: if females allocate paternity according to their prior experience with male parental care, it may pay for males to provision extra-pair young in early broods. Here, I assess the relationship between first-brood parentage and paternal care in a population of Savannah sparrows (Passerculussandwichensis) where a male's fertilization success in the second brood appears to be influenced by his prior parental performance. Based on the multi-locus DNA fingerprinting of 17 first broods, male feeding effort was influenced by parentage (percent of brood resulting from within-pair fertilizations) but not by brood size, male mating status (monogamous versus polygynous), timing of breeding (hatching date), structural size (wing length) or condition (mass). Males provided more care to broods that contained few within-pair young. This result supports the idea that males provision young to increase their future mating success, but alternative hypotheses involving male quality and timing of breeding cannot be excluded. Received: 13 August 1996 / Accepted after revision: 22 February 1997     

Social monogamy and extra-pair fertilization in an Australian lizard, Tiliqua rugosa

This study investigates social monogamy in the Australian sleepy lizard, Tiliqua rugosa. At a 70-ha site near Mount Mary, South Australia, we radio tracked 55 adult female and 39 adult male lizards during their spring activity periods. Each lizard was observed in 1–5 years. Females were observed with a single male partner on an average of 10.8 days per year, although in 17.3% of cases, females were observed on 2 or fewer days with a male. The most intense pairing period each year was 15 September–15 November when females were with male partners on an average of 36% of observation days. Partnerships lasted an average of 43.3 days each year. After mating in early November, the pairs separated. Observations of females pairing with other males were rare. Most males (82%) were also consistently monogamous, although 7 were observed pairing with 2 females within one season. To investigate paternity, we allowed 21 gravid females to give birth to 42 offspring in the laboratory. We determined genotypes at five polymorphic microsatellite DNA loci for the females, their male partners and their offspring. Four litters (19%) and 6 of the offspring from those litters (14.3%) showed evidence of extra-pair fertilization (EPF). Although the sample sizes are small, females of polygynous males were more likely to experience EPF. Received: 22 February 1998 / Accepted after revision: 23 May 1998     

Infanticide in seasonally breeding multimale groups of Hanuman langurs (Presbytis entellus) in Ramnagar (South Nepal)

In the seasonally breeding langur (Presbytis entellus) population of Ramnagar, South Nepal, where multimale groups prevail, 25 attacks on 11 infants (including one actual killing) by seven adult males were witnessed in five groups by six observers between 1990 and 1996. Circumstantial evidence also indicates three additional attempts at infanticide and in seven additional cases infanticide was presumed or likely. Infanticide presumably accounted for 30.8–62.5% of infant mortality in the first 2 years of life. Most attackers (91.4%) were residents of the infants' group and had immigrated after the infants had been born (75.0%) or conceived (25.0%). Thus, they were not related to the victims. The interbirth interval was shortened if an infant died either prior to September of its 1st year of life (mean = 1.2 years), or its 2nd year (mean = 2.0) and even its 3rd year (mean = 2.4). All attackers remained in the group at least until the next mating season; high-ranking males maintained their dominance rank and lower-ranking males rose in rank. Since rank and mating success were correlated and rank and reproductive success might be correlated, all attackers had a good chance of siring the next infant of the victims' mothers and could thus have benefited by their action. Infanticide seems to be a male reproductive strategy at Ramnagar. Infanticide has never before been reported among seasonally breeding langurs living at such low densities. This is also the first detailed report of infanticide as a male reproductive strategy in a seasonally breeding primate population. Received: 19 December 1996 / Accepted after revision: 7 June 1997     

Relatedness, polyandry and extra-group paternity in the cooperatively-breeding white-browed scrubwren (Sericornis frontalis )

We used DNA fingerprinting to examine the genetic parentage and mating system of the cooperatively breeding white-browed scrubwren, Sericornis frontalis, in Canberra, Australia. Our analyses revealed a remarkable variety of mating tactics and social organization. Scrubwrens bred in pairs or multi-male groups that consisted of a female and two or more males. Females were always unrelated to the pair male or alpha (dominant) male. Among multi-male groups we found three different mating tactics. Firstly, when alpha and beta (subordinate) males were unrelated, they usually shared paternity in the brood. This resulted in both males gaining reproductive benefits directly. Secondly, when beta males were not related to the female but were related to the alpha males, beta males sired offspring in some broods. In this situation, beta males gained reproductive benefits both directly and potentially indirectly (through the related alpha male). Thirdly, when beta males were related to the female or both the female and alpha male, they remained on their natal territory and did not sire any offspring. Thus beta males gained only indirect reproductive benefits. Overall, when group members were related closely, the dominant male monopolized reproductive success, whereas when the members were not related closely the two males shared paternity equally. This positive association between monopolization of reproduction and relatedness is predicted by models of reproductive skew, but has not been reported previously within a single population of birds. Other cooperatively breeding birds with both closely related and unrelated helpers may show a similar variety of mating tactics. Finally, we found that extra-group paternity was more common in pairs (24% of young) than in multi-male groups (6%), and we discuss three possible reasons for this difference. Received: 21 May 1996 / Accepted after revision: 14 December 1996     

The relative roles of predation and sperm competition on the duration of the post-copulatory association between the sexes in the blue crab, Callinectes sapidus

In many species, post-copulatory mate guarding prevents other males from mating with the guarded female. In crabs, males stay with their mates to protect the female from predators because, in some species, mating occurs when she is soft and vulnerable after molting. I tested the relative roles of sperm competition and predation on the duration of the post-copulatory association in the blue crab, Callinectes sapidus. Unpaired females suffered greater predation mortality than paired females and males stayed with the female longer in the presence of predators than in their absence, suggesting that the post-copulatory association protects females during their vulnerable period. However, the association may also occur in blue crabs because of sperm competition since spermathecal contents of females in the field indicate that 12.4% mated twice. Females experimentally mated with two males contained both males ejaculates and each ejaculate had access to the unfertilized eggs, suggesting that the size of a male's ejaculate influences his fertilization rate in a multiply-mated female. Males stayed longest in response to a high risk of sperm competition. Longer post-copulatory associations allowed the first male's ejaculate to harden into a type of sperm plug, which limited the size of a second inseminator's ejaculate in a non-virgin female as compared with a virgin. Males passed larger ejaculates in the presence of rivals and when previous ejaculates were in the female spermathecae, another response to sperm competition. Larger ejaculates may need longer post-copulatory associations before a more effective sperm plug forms. Large males stayed with the female longer, which is consistent with their ability to pass larger ejaculates than small males and suggests that there may be costs to minimizing the duration of the post-copulatory association. In the field, associations last long enough to protect the female during her vulnerable phase and may ensure that the guarding male fertilizes the most eggs in the female, even if she remates. Thus, the post-copulatory association protects female blue crabs from additional inseminators as well as from predators. Received: 23 January 1996 / Accepted after revision: 9 November 1996     

Female mallard mating preferences for multiple male ornaments

Mating preferences were studied in captive wild-stock female mallards. Independent observers scored ornament brightness for the bill and eight plumage areas of male mallards on a scale of 1 to 6. Ornament scores were generally positively correlated with each other as indicated by univariate correlations and principal component analysis. Males with higher bill scores were significantly more likely to obtain pairings. None of eight individual plumage ornaments were significant predictors of pairing success, but males with higher average plumage scores had significantly higher pairing success. Males that completed the molt first were also significantly more likely to be paired. Thus females may have paid some attention to plumage brightness. Stepwise multiple regression produced a model that included only bill and molt, both of which contributed a similar degree (r ² = 0.39); plumage ornaments and size measurements did not enter the model. These results are interpreted in light of hypotheses for the evolution of multiple ornaments, and phylogenetic plumage patterns in dabbling ducks. Received: 18 December 1995 / Accepted after revision: 22 September 1996     

A molecular genetic analysis of social structure, dispersal, and interpack relationships of the African wild dog (Lycaon pictus )

The African wild dog is a highly social, pack-living predator of the African woodland and savannah. The archetypal wild dog pack consists of a single dominant breeding pair, their offspring, and non-breeding adults who are either offspring or siblings of one of the breeding pair. Non-breeding adults cooperate in hunting, provisioning and the protection of young. From these observations follows the prediction that the genetic structure of wild dogs packs should resemble that of a multigenerational family, with all same-sexed adults and offspring within a pack related as sibs or half-sibs. Additionally, a higher kinship between females from neighboring packs should be evident if females tend to have small dispersal distances relative to males. We test these predictions through analysis of mitochondrial DNA control region sequences and 14 microsatellite loci in nine wild dog packs from Kruger National Park, Republic of South Africa. We show that as predicted, African wild dog packs generally consist of an unrelated alpha male and female, subdominant close relatives, and offspring of the breeding pair. Sub-dominant wild dogs occasionally reproduce but their offspring rarely survive to 1 year of age. Relatedness influences the timing and location of dispersal events as dispersal events frequently coincide with a change in pack dominance hierarchy and dispersers often move to areas with a high proportion of close relatives. Received: 22 February 1996 / Accepted after revision: 16 November 1996     

Female control of offspring paternity in a western population of red-winged blackbirds (Agelaius phoeniceus)

Extra-pair copulations, which occur when individuals that have formed social relationships to breed copulate outside their pairbond, now are recognized as an important component of reproductive success in many species. In situations where both males and females benefit from extra-pair copulations without incurring much risk, an inevitable conflict arises between pairbonded mates. In this study I investigated the conflict of interest between male and female reproductive strategies in a western population of red-winged blackbirds (Agelaius phoeniceus). Female red wings in this population initiate extra-pair copulations, which resulted in a 35% rate of extra-pair fertilization. Females initiated the majority (78%) of extra-pair copulations away from their nesting territory where pairbonded individuals typically copulate, and females that engaged in extra-pair copulations spent a significantly greater amount of time off the marsh during peak fertilization compared to females that did not. In addition, females that nested in areas with a large number of potential extra-pair partners produced significantly more extra-pair fertilized young compared to females that nested on marshes with few male neighbors. Males’ strategies to protect paternity were limited primarily to patrolling territory boundaries and to opportunistically preventing extra-pair copulations off the marsh when they were visible. In this population females appear to use behavioral means to control nestling paternity, which in turn directly affected their mate’s reproductive success, and males were restricted to using strategies that were largely ineffective at preventing the threat of extra-pair paternity. Received: 23 December 1994/Accepted after revision: 17 December 1995     

Do female black-capped chickadees prefer high-ranking males as extra-pair partners?

Previous studies have shown that some female black-capped chickadees (Poecile atricapillus) solicit copulations from males that rank higher in winter flocks than their social mates, and extra-pair paternity in nests occurs commonly enough to be considered a potential female mating tactic. This study uses blood samples collected in 1992–1995 from 58 families of black-capped chickadees to test whether females with extra-pair offspring have chosen extra-pair sires higher in social rank than their mates. Paternity was assessed with multilocus DNA fingerprinting in 1992–1994 nests and with microsatellite and single-locus minisatellite DNA typing in 1995 nests. Seventeen of 58 nests (29.3%) contained young genetically mismatched with their social father. In 11 of 15 cases where the identity of the extra-pair male was known, the extra-pair male was dominant to the social father. Using data from 29 nests located in 1994 and 1995 for which we had the most data on relative ranks of males, high-ranking males had greater realized reproductive success than low-ranking males as a result of extra-pair fertilizations. There was no significant difference between the number of nests containing extra-pair young of females mated to low-ranked versus high-ranked males. Two nests in 1995 contained young either genetically mismatched with both social parents (intraspecific brood parasitism) or, in one nest, genetically mismatched with the social mother but not the social father (quasi-parasitism). The implications of female strategies acquiring genetic benefits through extra-pair copulations are discussed. Received: 7 July 1997 / Accepted after revision: 14 March 1998     

Positive association between social and extra-pair mating in a polygynous songbird, the dickcissel (Spiza americana)

In polygynous species, males appear to gain additional offspring by pairing with multiple females simultaneously. However, this may not be true if some females copulate outside of the social pair bond. Polygynous males could experience lower paternity because of trade-offs among gaining multiple social mates, guarding fertility with these mates, and pursuing extra-pair matings. Alternatively, polygynous males could simultaneously gain extra social mates and have high paternity, either because of female preferences or because of male competitive attributes. We tested four predictions stemming from these hypotheses in a facultatively polygynous songbird, the dickcissel (Spiza americana). Unlike most previous studies, we found that males with higher social mating success (harem size) also tended to have higher within-pair paternity and that the number of extra-pair young a male sired increased significantly with his social mating success. Females that paired with mated males were not more likely to produce extra-pair young. In contrast, extra-pair paternity was significantly lower in the nests of females whose nesting activity overlapped that of another female on the same territory. This pattern of mating was robust to differences in breeding density. Indeed, breeding density had no effect on either extra-pair mating or on the association between polygyny and paternity. Finally, nest survival increased with harem size. This result, combined with the positive association between polygyny and paternity, contributed to significantly higher realized reproductive success by polygynous male dickcissels.     

Extra-pair paternity in tree swallows: why do females mate with more than one male?

Recent studies of monogamous tree swallows (Tachycineta bicolor) suggest that females may receive some type of genetic benefit from extra-pair fertilizations. In this study we attempted to determine what type of genetic benefits might be gained by females. We compared numerous morphological and behavioral traits (Table 1) of every male nesting on one grid of nest-boxes (n = 23) to determine what male traits were correlated with male success at gaining extra-pair fertilizations. DNA fingerprinting revealed an increase in the level of extra-pair paternity from the previous year (50% of broods contained extra-pair young in 1990 vs. 87% of broods in 1991), but no significant correlates of paternity. We found six extra-pair fathers at seven nests (20 nests had extra-pair young). The traits of these extra-pair males did not differ from those of the males they cuckolded. We discuss several reasons for this lack of difference, but argue that our results are not inconsistent with females choosing extra-pair males to enhance the genotypic quality of their offspring. Despite a complete search of the nest-box grid for extra-pair fathers, we were able to explain the paternity of just 21% (13/63) of all extra-pair young. This suggests that extra-pair fathers were either residents off our study grid or non-territorial floaters. Tree swallows are quite mobile and spend only part of the day at their nest prior to laying. In addition, we rarely see swallows visiting other grids of nest-boxes. Therefore, we suggest that most extra-pair copulations occur at some unknown location, possibly at a feeding or roosting area where females may be able to choose from many more potential extra-pair fathers than at their nest-site.