Promiscuity: an inbreeding avoidance mechanism in a socially monogamous species?

Summary Paternity likelihood was tested in a population of splendid fairy-wrens Malurus splendens by allozyme electrophoresis. A total of 91 offspring of 24 dams and 37 putative sires were typed at 10 polymorphic loci. All young were compatible with their dams but at least 65% were not fathered by any of the males in their group. A long-term study of this wren population has shown that the males are sedentary, show little evidence of dispersal and help care for the nestlings and fledglings in their group. Had the senior male sired all the offspring in his group, there would have been a high incidence of close inbreeding. The promiscuous mating system demonstrated here would reduce the level of inbreeding in the population but still allow individuals the security of group-living in a stable year-round territory. Offprint requests to: M.G. Brooker     

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.     

The importance of biparental care in a precocial,monogamous bird,the bar-headed goose (Anser indicus)

Summary This study presents the first direct evidence of benefit derived from the male's parental effort during rearing of young in a monogamous, precocial bird species. We compared mothers accompanied by a mate (paired mothers) with single mothers, some of which were artificial widows, in a semicaptive flock of bar-headed geese (Anser indicus). Paired mothers were less often displaced by other birds and suffered fewer interruptions of brooding. Their goslings spent more time grazing and survived with a higher probability. Although one beneficial result of the male's parental effort may be the continued availability and survival of his mate, a more direct benefit arises from higher offspring survival between hatching and fledging.     

Experimentally manipulated brood sex ratios: growth and survival in the black-headed gull (Larus ridibundus), a sexually dimorphic species

In sexually size dimorphic species, individuals of the larger sex often suffer from enhanced mortality during the nestling period. This has been attributed to higher nutritional requirements of the larger sex, which may render this sex more vulnerable to adverse food conditions. However, sex-biased mortality might not exclusively depend on the differences in food demand but also on other phenotypic differences, e.g., in competitiveness. Interference competition between the sexes and position in the laying sequence in particular may be essential components contributing to biased mortality.By creating synchronously-hatched unisex broods in the sexually size dimorphic black-headed gull, we specifically tested the effect of sex-specific food demand by excluding interference competition between the sexes as well as hatching asynchrony. To test the effect of egg quality, which varies with the position in the laying sequence, we composed each nest of chicks from eggs of all different positions in the laying sequence.All-male nests showed significantly enhanced mortality compared to all-female nests from the beginning of the development of the sexual size dimorphism onwards. This underlines the role of a higher food demand in biased mortality of the larger sex.In males but not females, asymptotic body mass and skeletal size were negatively associated with position in the laying sequence, while survival was not affected by position. As a consequence, sexual size dimorphism at the end of the nestling period was less pronounced compared to the natural situation. These data show that, although male growth is more sensitive to a decrease in egg quality, the higher mortality of last hatched chicks in natural nests is mainly due to hatching asynchrony and egg size but not egg content.     

Females alter their song when challenged in a sex-role reversed bird species

Birdsong serves to attract mates and to deter territorial rivals. Even though song is not restricted to males, this dual function has almost exclusively been demonstrated for male song. To test the generality of hypotheses on birdsong, we investigated female song in the sex-role reversed, classically polyandrous African black coucal (Centropus grillii) in the context of female–female competition. We compared spontaneously vocalizing females with females vocally responding to a playback simulating a conspecific intruder. Females changed vocal parameters in response to playbacks: They lowered the pitch of their vocalizations and enhanced the duration of song elements when being challenged. Also, the composition of the vocalizations was altered. There was no significant correlation between pitch and body size parameters in spontaneous song, but there was for response songs, with larger females having a lower pitch. These changes in vocal properties suggest that the vocalizations are important for mutual assessment of competitive abilities in females. Our findings confirm the general role of intrasexual competition in vocal communication of birds.     

Extra-pair copulations in a lek: the secondary mating system of monogamous razorbills

Summary I studied the mating strategies of razorbills Alca torda, a monogamous colonial seabird, during 1987–1989 in Wales, U.K. The outstanding feature of the study population's mating system was the performance of most copulations in mating arenas outside the colony. Females visited the arenas and sometimes accepted extra-pair copulations (EPCs), and males aggressively competed for EPCs. During the fertilizable period of most females, the arenas resembled leks because they contained no resources except mates, and males contributed only sperm to extra-pair females. Typical of leks, the operational sex ratio was strongly male-biased, and male mating success was highly skewed. To examine the potential for sexual selection to operate in this system, I correlated male EPC success with variables that could be associated with male-male competition and/or female choice. The frequencies of three behaviors (interference of copulation attempts, fights won against other males, and EPC attempts), accounted for 62% of the variance in EPC success and were strongly intercorrelated, with interference explaining most of the variance in a multivariate test. EPC success was not correlated with body size, age, paired status or either of two estimates of the time spent in the arena. The hypothesis that male EPC success was determined by active female choice was tested by examining the relative success (EPCs per attempt) of males. Relative success was not correlated with any of the three behaviors associated with absolute success, or with age, body size or attendance, suggesting that male-male competition, mainly in the form of copulation interference, is the principal correlate of EPC success. These findings in a monogamous species illustrate that EPC is a secondary mating system of razorbills in which sexual selection operates. The existence of this system outside the colony raises the possibility that lekking for EPCs may also occur within the nesting territories of other monogamous, colonial species but is hidden by competition for nests and breeding partners.     

Major histocompatibility complex and mate choice in a monogamous rodent

A growing number of studies indicate that females can increase the viability of their offspring by gaining direct benefits such as parental care or genetic advantages through selective mating with certain males. Among the best candidates for the genetic basis of mate choice in vertebrates are the genes of the major histocompatibility complex (MHC) because these highly polymorphic genes may increase offspring viability and provide direct cues for mate choice. A free-ranging, pair-living rodent was used as an example to investigate MHC-dependent mate choice in an obligate monogamous species, the Malagasy giant jumping rat Hypogeomys antimena. Two possible mechanisms of mate choice were tested. First, mate choice may occur to increase the heterozygosity of MHC genes in the progeny and, second, mates might choose each other according to the degree of dissimilarity of their functional MHC DRB (exon 2) proteins in order to maximise the allelic divergence in their offspring. Analyses of 65 Hypogeomys couples failed to confirm associations of mating patterns with the MHC genotype to increase heterozygosity or MHC allelic divergence in the progeny. Also, no evidence for mechanisms to increase the allelic divergence was found in sex-specific analyses where a male or female, respectively, migrated to and was accepted by a territory and burrow holder of the opposite sex. However, the frequency distribution of 0, 1 or 2 new alleles potentially available for the progeny differed significantly when a new male was chosen by a territory-holding female. In contrast to current models, genetically similar instead of dissimilar mates seem to be the preferred choice. This is the first study investigating the role of the MHC in mate selection in an obligate monogamous rodent.Communicated by G. Wilkinson     

Colony foundation and polygyny in the ant Formica podzolica

We document the variation in number of queens occurring naturally in founding, immature and mature nests of the ant Formica podzolica, and compare development of colonies and survivorship of queens in experimental nests started with 1–16 foundresses. Number of queens per nest was associated with stage of colony development. Most nests were monogynous, but 20% of immature nests (n = 66) and 25% of mature nests (n = 92) were oligogynous or polygynous. Colonies were usually established by single queens (i.e., haplometrosis), but colony establishment by multiple queens (i.e., pleometrotis) was also common, occurring in 27% of founding nests (n = 492). Foundress groups in the field were small ( = 1.47 ± 0.04 queens/nest), and large groups experienced high mortality and low productivity in artificial nests. Therefore, the many queens (up to 140) in some immature and mature colonies were probably secondarily pleometrotic. Experimental nests started with 1–4 queens were more successful than those initiated by 8 or 16 queens. Small groups (2–4 queens) produced more pupae before the first nests reared workers than single foundresses or larger groups (8 or 16 queens). Although single foundresses were less productive than queens in small groups, they experienced greater survivorship and less weight loss than queens in pleometrotic associations. Besides low productivity, queen mortality and weight loss were greatest in large groups.     

Inheritance of migratory direction in a bird species: a cross-breeding experiment with SE- and SW-migrating blackcaps (Sylvia atricapilla)

Summary Young avian migrants of many species are able to find their species- or population-specific wintering area without the help of conspecifics. In orientation tests hand-raised birds have been demonstrated to choose appropriate population-specific migratory directions, suggesting a genetic basis to this behaviour. I here report results of a cross-breeding experiment between individuals of two blackcap (Sylvia atricapilla) populations with widely different migratory directions. The orientation of the F1 offspring was intermediate between and significantly different from that of both parental populations (Fig. 2). The variance of individual mean directions in the F1 generation did not increase compared with the parental groups, and the inheritance of migratory directions was not sex-linked. The data provide direct evidence for a genetic basis of migratory directions in birds and demonstrate a phenotypically intermediate mode of inheritance.     

Sexual selection and cuckoldry in a monogamous songbird: implications for sexual selection theory

Sexual selection is generally assumed to be weaker in monogamous than in polygynous animals. Recently, though, extra-pair fertilizations have been hailed as an important force in generating variance in reproductive success among males in socially monogamous species, thereby increasing the intensity of sexual selection. To see if extra-pair copulations contribute to variance in male reproductive success in the house finch (Carpodacus mexicanus), we used DNA fingerprinting to determine the paternity of chicks from 35 nests. This species is a socially monogamous passerine in which plumage brightness serves as a sexually selected indicator of male quality. Out of 119, nestlings 10 (8.3%) were fathered by a male other than the attending male, but cuckoldry occurred randomly with respect to the plumage colouration, size, or age of the attending male. Thus extra-pair fertilizations do not generate variance in male reproductive success with respect to plumage colour. On the other hand, a strongly male-biased sex ratio and asynchronous breeding by females may generate substantial variance in male reproductive success and could explain the evolution of ornamental colouration.     

Intrasexual selection in Mirza coquereli : evidence for scramble competition polygyny in a solitary primate

The primates of Madagascar (Lemuriformes) deviate from fundamental predictions of sexual selection theory in that polygynous species lack sexual dimorphism, have even adult sex ratios and often live in female-dominated societies. It has been hypothesized that intrasexual selection in these species is either reduced or primarily focused on traits related to scramble competition. The goal of this study was to examine these hypotheses by studying the mating system of a solitary nocturnal species, Mirzacoquereli. During a 4-year field study in western Madagascar, I captured and followed 88 individually marked animals. I found that adult males were significantly larger than females, providing the first evidence for sexual size dimorphism in lemurs. In addition, the adult sex ratio was biased in favour of females in 3 out of 4 years. There was no significant sex difference in canine size, however. Males showed pronounced seasonal variation in testis size with a 5-fold increase before and during the short annual mating season. During the mating season, males had more injuries than females and more than quadrupled their home ranges, overlapping with those of more than ten females, but also with about the same number of rivals. Only about one social interaction per 10 h of observation was recorded, but none of them were matings. Together, these results indicate that these solitary lemurs are clearly subject to intrasexual selection and that male-male competition is primarily, but not exclusively, of the scramble type. In addition, they suggest that the above-mentioned idiosyncracies may be limited to group-living lemurs, that social systems of solitary primates are more diverse than previously thought, and that the temporal distribution of receptive females is responsible for this particular male mating strategy. Received: 11 January 1997 / Accepted after revision: 18 April 1997     

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.     

Male mate guarding in a socially monogamous mammal,the round-eared sengi: on costs and trade-offs

Mate guarding is predicted to be one of the driving forces for the evolution of monogamy, but supporting evidence in free-living mammals is rare. The goals of our study were three-pronged. First, we tested if mate guarding, measured as intrapair distance, occurs as a behavioral tactic in round-eared sengis (Macroscelides proboscideus), a socially monogamous species lacking paternal care and in which females breed asynchronously, producing 2–3 litters during an 8-month long breeding season. Second, we determined if mate guarding involves costs which we identified as changes in male body mass. Third, we investigated whether variation in individual investment in mate guarding depended on the males’ body mass and the number of neighboring males. Field data were collected in a semidesert in South Africa using radio-tracking, trapping, and direct observations during three successive breeding seasons. Mate guarding strongly depended on the females’ reproductive state, and all males started to guard their mates prior to and during estrus, as exemplified by reduced intrapair distance. Mate guarding incurred costs: overall, males lost about 5% of body mass. Male body mass loss and initial body mass were negatively related to the intensity of precopulatory mate guarding. Furthermore, during estrus intrapair distance was inversely correlated with the number of neighboring males. The results show that mate guarding is the predominant male tactic in round-eared sengis. However, since mate guarding imposed costs, males may balance benefits and costs associated with guarding by varying their effort in relation to their physical capabilities and the competitive environment.     

Nest site limitation and facultative polygyny in the ant Leptothorax longispinosus

Summary The ant L. longispinosus displays geographic variation in its pattern of facultative polygyny (Fig. 2). In nature, nest density and frequency of multiple queening are positively associated over three sites. A putative causal relation between availability of vacant nest sites and polygyny was examined in New York, where a plot was seeded with additional nest sites and monitored for 24 months. Both queen number and worker number per nest on the experimental plot were reduced relative to controls (Fig. 4, Fig. 5), indicating that scarcity of available nest sites influences the pattern of polygyny in this species. The observed demographic changes resulted from fractionation of existing colonies; adding nest sites induced polydomy. Although numbers of adult ants changed with addition of nest sites, the numbers of immatures were no different after 2 years (Table 1), suggesting that the population was undergoing growth to expand into the additional sites. These results are the first direct experimental evidence linking polygyny to an ecological parameter for any ant species.     

Optimal divorce and re-mating strategies for monogamous female birds: a simulation model

Although the extensive variation in divorce rates among monogamous bird species has stimulated several theoretical accounts, the mechanisms underlying divorce strategies remain poorly understood. Here, we use an individual-based simulation model to investigate the adaptiveness of mechanisms of mate choice in the context of remating. Our model compares the fitness of females that choose a mate during each breeding season using one of two different decision rules; best-of-n females sample n potential partners and then select the male with the highest quality, whereas better option females choose a mate whose quality is maximal among the non-mated individuals they sampled the season before. It is assumed in the model that best-of-n females have no a priori information about the quality of potential partners and systematically decide to divorce at the beginning of each breeding season before searching for a new mate. Conversely, better option females use the information they gained the season before, and may retain their previous partner if they have no opportunity to mate with an individual of better quality. Results from simulations indicate that the best-of-n decision rule should be favoured when there is a large variation in male quality and low costs of mate sampling. On the other hand, the probability that the better option rule may invade the population is predicted to increase with male survival rate. However, changes in male mortality had no marked influence on the expected proportion of divorcing pairs, contrary to previous theoretical expectations.Communicated by H. Kokko     

Social organization and nest co-occupancy in Peromyscus californicus,a monogamous rodent

Summary Home ranges, social organization, and nest co-occupancy of Peromyscus californicus were studied using radiotelemetry at the Hastings Natural History Reservation, California. Mated pairs were ascertained by the transfer of fluorescent pigments from lactating females to putative fathers. Mated pairs had largely overlapping home ranges that were not statistically distinguishable, whereas adjacent adults had mostly exclusive, statistically distinguishable home ranges. There was no difference in the mean home range of males and females, but mated females tended to have smaller ranges than their mate. Home range size was extremely variable (range: 150–3788 m²) and averaged 1161 m² across all individuals. Male home range size was inversely correlated with population density, suggestive of a social influence on home range. Putative fathers spent comparable amounts of time to females in the nest — presumably caring for the young — which supports previous laboratory reports of paternal care in this species. All data collected in this study are consistent with previous suggestions that P. californicus live in semi-permanent family groups and are monogamous. Offprint requests to: D.O. Ribble     

Comparing discriminant analysis, neural networks and logistic regression for predicting species distributions: a case study with a Himalayan river bird

We assessed the occurrence of a common river bird, the Plumbeous Redstart Rhyacornis fuliginosus, along 180 independent streams in the Indian and Nepali Himalaya. We then compared the performance of multiple discrimant analysis (MDA), logistic regression (LR) and artificial neural networks (ANN) in predicting this species’ presence or absence from 32 variables describing stream altitude, slope, habitat structure, chemistry and invertebrate abundance. Using the entire data (=training set) and a threshold for accepting presence in ANN and LR set to P≥0.5, ANN correctly classified marginally more cases (88%) than either LR (83%) or MDA (84%). Model performance was assessed from two methods of data partitioning. In a ‘leave-one-out’ approach, LR correctly predicted more cases (82%) than MDA (73%) or ANN (69%). However, in a holdout procedure, all the methods performed similarly (73–75%). All methods predicted true absence (i.e. specificity in holdout: 81–85%) better than true presence (i.e. sensitivity: 57–60%). These effects reflect species’ prevalence (=frequency of occurrence), but are seldom considered in distribution modelling. Despite occurring at only 36% of the sites, Plumbeous Redstarts are one of the most common Himalayan river birds, and problems will be greater with less common species. Both LR and ANN require an arbitrary threshold probability (often P=0.5) at which to accept species presence from model prediction. Simulations involving varied prevalence revealed that LR was particularly sensitive to threshold effects. ROC plots (received operating characteristic) were therefore used to compare model performance on test data at a range of thresholds; LR always outperformed ANN. This case study supports the need to test species’ distribution models with independent data, and to use a range of criteria in assessing model performance. ANN do not yet have major advantages over conventional multivariate methods for assessing bird distributions. LR and MDA were both more efficient in the use of computer time than ANN, and also more straightforward in providing testable hypotheses about environmental effects on occurrence. However, LR was apparently subject to chance significant effects from explanatory variables, emphasising the well-known risks of models based purely on correlative data.     

Female territoriality and the function of scent-marking in a monogamous antelope (Oreotragus oreotragus)

In monogamous species, females often choose between males according to the quality of the territories they defend, but the extent to which females themselves contribute to territory defence is frequently underestimated. Here we test for differences in male and female roles during paired scent-marking bouts, a key component of territorial defence, in a monogamous antelope. In two populations (Kenya, Zimbabwe) of klipspringer, Oreotragus oreotragus, both males and females usually scent-marked at the same site, but there were significant differences between sexes in terms of investment within bouts. Females initiated most bouts, thus dictating the marking strategy of the pair. Males initiated relatively few bouts, but deposited more scent marks per bout than females and were usually the last to scent-mark before leaving the site; they marked on the same branches as the female and thus overmarked her scent. Both sexes deposited more marks during paired than solo visits. Immediately preceding and following scent-marking bouts, males approached females and females left males more often than expected. Female scent-marking rates were higher when they were receptive than at other times, and this increase was matched by elevated marking rates of males. Females may increase marking rates when they are receptive in order to test the quality of their mate or to incite male competition. However, these ideas are unlikely to explain female scent-marking behaviour outside the mating season, which appears to be related primarily to territorial defence. We suggest that these differences in investment in scent-marking bouts are consistent with predictions that females may be autonomously territorial and that overmarking of female scent by males is a form of mate-guarding. Received: 17 November 1999 / Received in revised form: 24 February 2000 / Accepted: 13 March 2000     

Invading together: the benefits of coalition dispersal in a cooperative bird

Dispersal attempts can be costly and may often end in failure. Individuals should therefore only disperse when the benefits of dispersal outweigh the costs. While previous research has focussed on aspects of the individual that may affect dispersal success, social factors may also influence dispersal outcomes. One way of achieving successful dispersal could be through cooperative, or coalition dispersal. I investigated this possibility in the cooperatively breeding Arabian babbler Turdoides squamiceps. I found that coalition dispersal appears to be an effective strategy to ensure the success of dispersal attempts, with coalitions more successful than lone individuals at taking over the breeding position in a new group. Lone dispersal was more costly than coalition dispersal, with lone individuals suffering a greater loss of body mass during dispersal attempts. These results suggest a substantial short-term benefit for this type of cooperative behaviour. There was no evidence for dispersal polymorphism in the population, with no detectable phenotypic difference between dispersers and non-dispersers or those that dispersed as part of a coalition compared with those that dispersed alone.