Monogamous Species Research Articles

Paternity Loss in Relation to Male Age, Territorial Behaviour and Stress in the Pied Flycatcher

AbstractFor sexual selection to operate in monogamous species, males of poor quality in some factor like age, ornamentation, condition or aggressiveness, should lose paternity compared with higher quality males. We tested this idea in an Iberian population of pied flycatchers (Ficedula hypoleuca). Microsatellite analysis of 67 broods revealed moderate levels of extra‐pair paternity (22.4% of broods, 7.5% of young). In a sample of 58 broods for which the caring male was identified, a higher paternity loss was associated with younger males, males that were less aggressive during territorial intrusion tests performed before the commencement of laying, and with males that showed higher levels of corticosterone metabolites in faecal samples collected at the end of the nestling period. Plumage darkness, forehead patch size and condition were not related to paternity loss. Paternity loss is more related to behavioural or physiological traits than to morphological ones in this population.

First Documented Cases of Polygyny in the Grasshopper Sparrow

We studied the breeding biology of Grasshopper Sparrows (Ammodramus savannarum) on restored grasslands in Maryland from 1999 to present. We report the first documented cases of social polygyny in this species. Polygyny increased reproductive success for males in two of four cases, but its rarity suggests it is only a facultative behavior for this usually socially monogamous species

Mate replacement entails a fitness cost for a socially monogamous seabird

Studies of the selective advantages of divorce in socially monogamous bird species have unravelled extensive variation among different lineages with diverse ecologies. We quantified the reproductive correlates of mate retention, mate loss and divorce in a highly philopatric, colonially breeding biparental seabird, the Australasian gannet Morus serrator. Estimates of annual divorce rates varied between 40-43% for M. serrator and were high in comparison with both the closely related Morus bassanus and the range of divorce rates reported across monogamous avian breeding systems. Mate retention across seasons was related to consistently higher reproductive success compared with mate replacement, while divorce per se contributed significantly to lower reproductive output only in one of two breeding seasons. Prior reproductive success was not predictive of mate replacement overall or divorce in particular. These patterns are in accordance with the musical chairs hypothesis of adaptive divorce theory, which operates in systems characterised by asynchronous territorial establishment.

Long tails matter in sugarbirds—positively for extrapair but negatively for within-pair fertilization success

Extrapair mating is known to occur in many animals and potentially has a significant influence on reproductive success. Female extrapair mate choice may explain the occurrence of exaggerated ornaments in socially monogamous species, but the influence of ornamentation on extrapair mating success has rarely been investigated experimentally. Cape sugarbirds (Promerops cafer) are socially monogamous, almost always lay 2 egg clutches and have long-term pair bonds often lasting several seasons. However, they also display sexually dimorphic extravagant ornamentation in the form of a long, graduated tail and have one of the highest rates (65% of young) of extrapair paternity recorded in birds. We provide a test of the hypothesis that the ornamented tail is used in mate choice for extrapair partners by conducting an experiment in which tail length was manipulated after social mating but before copulation. This experiment therefore allowed females to respond to the manipulation of male tail length when making a choice of copulation partner but not social mate. We show that the tail length of male sugarbirds has a significant effect on the success of males in gaining extrapair paternity, with long-tailed males obtaining significantly more extrapair young than shorttailed males. However, males with short tails sire a significantly greater proportion of the nestlings in their own nests than longtailed individuals. This result suggests that males may adopt alternative strategies dependent on their ornamentation. Key words: extrapair mating, mate choice, Pomerops cafer, sexual selection, sugarbird, tail ornamentation. [Behav Ecol]

Proximate and ultimate factors explaining floating behavior in long-lived birds

Avian populations are composed of reproductive individuals coexisting in space and time with young, non-breeding conspecifics or “floaters”. Despite the fact that first breeding can be delayed for years and can exert profound effects on fitness, many aspects of the behavior, ecology and physiology of young floaters remain poorly understood. By means of combining endocrine, behavioral and life history information from a population of black kites ( Milvus migrans) monitored long-term, we tested several hypotheses suggesting endocrine function as a determinant of floating status. Sexual function in non-breeding males, estimated through determination of systemic testosterone and progesterone levels, was similar to that in reproductively active conspecifics. Floating females, on the contrary, displayed an endocrine pattern of circulating estrogens and progesterone that was parallel in timing but reduced in magnitude as compared to breeders. Our results suggest that floaters are not physiologically constrained to reproduce, but the cost–benefit balance of attaining complete gonadal function is sexually dependent. While young, unmated males could increase their breeding prospects by attaining sexual maturity regardless of their social environment, natural selection would favor females relying on social cues to mature. Consistent with the sexual roles of socially monogamous species, gonadal recrudescence and testosterone production would allow unmated males to access breeding resources (e.g. through male–male competition and extra-pair fertilizations). Unmated females, on the contrary, would reduce physiological costs by means of delaying ovarian maturation until establishing pair bonds with a male providing access to breeding resources.

Bi‐parental vs. cooperative breeding in a passerine: fitness‐maximizing strategies of males in response to risk of extra‐pair paternity?

In socially monogamous species, males that risk cuckoldry more than others might gain inclusive fitness by yielding paternity to relatives. We tested this prediction in the Tibetan ground tit Pseudopodoces humilis, an unusual facultative cooperative breeder wherein most helpers (87% males) join a mated pair shortly before clutch completion. Extra-pair paternity among bi-parental broods occurred less often (26% of broods, 9% of young) compared with cooperative broods (68%, 25%). In the former, most extra-pair sires (88%) were pair breeders unrelated to the cuckolded males, whereas in the latter, sires (87%) were mainly helpers related to the dominant males. Brood productivity did not differ between the bi-parental and cooperative breeders, but helpers' partitioning over group paternity reduced the realized reproductive success of helped males. After taking inclusive fitness into account, however, there was no difference in success of dominant males between the two social systems. One possible explanation for the differences in the rates of cuckoldry in the two systems was body size, because pair-bond males in bi-parental situations were significantly larger than those in cooperative ones. We propose two alternative strategies for males to maximize fitness: breed as a pair if large to avoid cuckoldry from helpers, or breed cooperatively if small but compromise some paternity to relatives. Our results provide an unusual route to the incidence of cooperative groups, based on constraints imposed by low competitive ability of breeding males rather than some external ecological or demographic factors.

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.

Mate-guarding intensity increases with breeding synchrony in the colonial fairy martin, Petrochelidon ariel

Extrapair paternity (EPP) is common in many socially monogamous species, influencing patterns of sexual selection and shaping many aspects of reproductive behaviour. However, factors explaining variation in the occurrence of EPP, both within and between populations, remain poorly understood. One ecological factor that has received considerable attention is breeding synchrony, but the proposed mechanisms remain contentious and the findings from the large number of correlational studies have been inconsistent. Mate guarding, a behavioural tactic to limit paternity loss, may be fundamental to any relationship between EPP and breeding synchrony. However, few studies have investigated how guarding behaviour varies with breeding synchrony, and the theoretical predictions are unclear. We examined how mate-guarding intensity in the colonial fairy martin varied with changes in breeding synchrony. To eliminate likely confounding effects of individual quality, we measured guarding intensity on multiple days during the fertile period of individual females and related this to daily variation in colony-level breeding synchrony. Similarly, we examined whether extrapair interest in fertile females varied with change in breeding synchrony. Both mate-guarding intensity and extrapair pursuit rate increased sharply several days prior to egg laying, before declining once laying commenced. When we controlled for this effect of female fertility status, guarding intensity increased with breeding synchrony. These novel findings suggest that the risk of paternity loss increases with breeding synchrony, at least among colonial species. Moreover, adjustment of guarding intensity to the risk of paternity loss may explain why most correlational studies do not reveal a relationship between EPP and breeding synchrony.

Ecological factors regulating brood attendance patterns of the Western Sandpiper Calidris mauri

Parental brood attendance patterns vary greatly among shorebird species. For monogamous calidridine species, biparental care with female‐first brood departure is most common. It is believed that adult sandpipers balance potential individual survival costs associated with extended parental care against the benefit gained by their brood of prolonged parental care. These costs and benefits are difficult to quantify and factors affecting the termination of parental brood attendance are unclear. We compared clutch size, nesting phenology, and parental attendance patterns of Western Sandpipers Calidris mauri at Nome and Kanaryarmiut, Alaska, sites separated by three degrees of latitude. The sites differed in breeding density and duration of breeding season, but the distribution of clutch sizes did not differ between sites or between nesting attempts. Parental attendance patterns were similar between sites, suggesting that parental attendance is a highly conserved life‐history trait in Western Sandpipers. Male Western Sandpipers attended broods longer than females, and the duration of parental attendance decreased at a similar rate for both sexes as the season progressed. Male and female Western Sandpipers undertake differential migrations to their non‐breeding grounds, with males typically settling at more northerly locations and females at more southerly sites, a migration pattern shared by certain other monogamous calidridine species. These same species exhibit similar parental brood attendance patterns, suggesting the strong role of overall migration distance in shaping the expression of parental attendance behaviours. A contrast of more geographically disjunct sites coupled with a better understanding of the migratory connectivity between Western Sandpiper breeding and non‐breeding populations would elucidate the role of cross‐seasonal effects on parental brood attendance decisions.

Breeding Ecology of the Malagasy Endemic Red-Tailed VangaCalicalicus madagascariensis

The behavior and parental care of the endemic Red-tailed Vanga Calicalicus madagascariensis were studied in Ranomafana National Park, south-eastern Madagascar, from December 2007 to January 2008. Both sexes are similar in size, but show striking plumage-color dimorphism. The studied breeding pair shared duties in nest building, egg incubation and care of the young, but the male provided more parental care than the female. No helpers were observed at the nest during the study. Incubation lasted about 24 days and the nestling period was 15 days during which time chicks were fed on different types of insects and arthropods (mainly butterflies, spiders and locusts) obtained from the systematic inspection of the branches and leaves. The extensive male investment in the breeding might be due to ensure high rates of nestling growth and to avoid nest predation. To conclude, Red-tailed vanga is a socially monogamous species that exhibits classic biparental care.

The relationship between body mass and relative investment in testes mass in amniotes and other vertebrates

In terrestrial placental mammals, there is a well‐known negative allometric relationship between body mass and relative investment in testes mass. Such a negative relationship means that males of relatively monogamous small species invest proportionately more in their reproductive tissues than males of more polyandrous larger species. The selective pressure responsible for this relationship remains unclear and is it not known if this is a general allometric relationship that is similar across all vertebrate lineages. To investigate this, we conducted the first comparison of relationships between body mass and testes mass (using percentage testes mass as the dependent variable) across a variety of vertebrate groups. In all amniote lineages examined, the allometric relationship between body mass and testes mass was relatively strong and negative. We show, for the first time, that reptiles, birds and terrestrial placental mammals followed the same allometric relationship and, contrary to previous expectations, this relationship is sigmoidal rather than linear. Within this data set, there was no significant difference between this general amniote relationship and any of the 13 orders of reptiles, birds and terrestrial placental mammals examined. As a result, we propose that a sigmoidal relationship should be considered the default assumption for the form of the body mass – testes mass relationship within the amniote lineage. However, we also identify significant differences within some additional mammal groups (marsupials, bats and cetaceans). In each of these cases, only some sub‐groupings differed significantly from the general amniote relationship. In contrast to the amniotes, the relationship is relatively weak and positive in teleost fish and frogs suggesting that a negative allometric relationship is not universal in vertebrates. We explore whether variation in the body mass – testes mass relationships can be linked to sperm competition or a variety of ecological characteristics, either for amniotes in particular or vertebrates in general.

“Compatible Alleles“ and Extra-Pair Paternity: Conclusions Depend on the Microsatellite Loci Used

Although females' mating with multiple males is widespread in socially monogamous species, its evolutionary significance is poorly understood. Tests of the hypothesis that socially monogamous females seek extra-pair copulations to increase the heterozygosity of their offspring have produced mixed results. Some of the inconsistency may be the result of technical limitations of the molecular analyses used. In a previous analysis using five microsatellite loci, we showed that in the House Wren (Troglodytes aedon) extra-pair sires had fewer alleles common to the population than did other nearby males that could have sired offspring but did not, suggesting a “rare male” effect (Masters et al. 2003, Proceedings of the Royal Society of London, Series B 270:1393–1397). We repeated the previous analysis, including an additional set of seven microsatellite loci. An analysis that used all 12 loci (both the original and additional loci) produced results suggesting that genotype affects extra-pair paternity. By contrast, an analysis using only the seven new loci alone showed no significant effects. We conclude that studies of this type are likely to be sensitive to the loci employed, particularly when relatively low numbers of loci are analyzed.

Sexual Size Dimorphism and Bohemian Waxwings, <em>Bombycilla garrulus</em>

Sexual size dimorphism is common among birds, with males generally being larger than females. Sexual size dimorphism is typically more extreme in polygynous species; socially monogamous males are typically only 5% larger than females. However, cryptic sexual size dimorphism has been found in some socially monogamous species. I used standard external measurements as well as two internal measurements (keel length and pectoral muscle mass) to determine whether, or to what extent, Bohemian Waxwings (Bombycilla garrulus) exhibit sexual size dimorphism. Males were only slightly larger than females in all of the characters measured except keel and tarsus length. Keel and tarsus length were 0.6% and 1% longer, respectively, in females than in males. The similar size exhibited by males and females may be related to the amount of parental care provided by males. Smaller body size in males may reflect a trade-off between selection for increased male size and energetic constraints imposed by parental care.

Natural selection and genital variation: a role for the environment, parasites and sperm ageing?

Male genitalia are more variable between species (and populations) than other organs, and are more morphologically complex in polygamous compared to monogamous species. Therefore, sexual selection has been put forward as the major explanation of genital variation and complexity, in particular cryptic female choice for male copulatory courtship. As cryptic female choice is based on differences between males it is somewhat paradoxical that there is such low within-species variation in male genitalia that they are a prime morphological identification character for animal species. Processes other than sexual selection may also lead to genitalia variation but they have recently become neglected. Here I focus on pleiotropy and natural selection and provide examples how they link genitalia morphology with genital environments. Pleiotropy appears to be important because most studies that specifically tested for pleiotropic effects on genital morphology found them. Natural selection likely favours certain genital morphology over others in various environments, as well as by reducing re-infection with sexually transmitted diseases or reducing the likelihood of fertilisation with aged sperm. Both pleiotropy and natural selection differ locally and between species so may contribute to local variation in genitalia and sometimes variation between monogamous and polygamous species. Furthermore, the multitude of genital environments will lead to a multitude of genital functions via natural selection and pleiotropy, and may also contribute to explaining the complexity of genitalia.

Adult sex ratio affects divorce rate in the monogamous endoparasite Schistosoma mansoni

“Divorce” (mate switching) rate is known to vary largely both between and within socially monogamous species. Although the adult sex ratio can have an important influence on mating patterns, very few studies have investigated the influence of sex ratio on divorce rate in monogamous species, and even less so from an experimental point of view. In addition, most studies on the causes and consequences of divorce have been performed on vertebrate species, whereas data for invertebrate monogamous species remain scarce. Schistosoma mansoni is a monogamous endoparasite with a complex life cycle characterized by asexual reproduction in the intermediate host and sexual reproduction in the definitive host. In the wild, populations of S. mansoni inside their definitive hosts are characterized by a male-biased sex ratio. We studied the influence of experimentally varying the adult sex ratio on divorce rate in S mansoni, using controlled infections of hosts with clonal populations. The more male-biased the sex ratio was, the more the divorce rate increased, whereas no such effect was observed under a female-biased sex ratio. In this study and for the first time, we showed, by handling the sex ratio, that the divorce rate increases in adult male-biased sex ratio conditions in a monogamous species.

Age‐specific effect of heterozygosity on survival in alpine marmots, Marmota marmota

The fitness consequences of heterozygosity and the mechanisms underpinning them are still highly controversial. Using capture-mark-recapture models, we investigated the effects of individual heterozygosity, measured at 16 microsatellite markers, on age-dependent survival and access to dominance in a socially monogamous mammalian species, the alpine marmot. We found a positive correlation between standardized multilocus heterozygosity and juvenile survival. However, there was no correlation between standardized multilocus heterozygosity and either survival of older individuals or access to dominance. The disappearance of a significant heterozygosity fitness correlation when individuals older than juveniles are considered is consistent with the prediction that differences in survival among individuals are maximal early in life. The lack of a correlation between heterozygosity and access to dominance may be a consequence of few homozygous individuals attaining the age at which they might reach dominance. Two hypotheses have been proposed to explain heterozygosity-fitness correlations: genome-wide effects reflected by all markers or local effects of specific markers linked to genes that determine fitness. In accordance with genome-wide effects of heterozygosity, we found significant correlations between heterozygosities calculated across single locus or across two sets of eight loci. Thus, the genome-wide heterozygosity effect seems to explain the observed heterozygosity-fitness correlation in the alpine marmot.

Extra-pair young in house wren broods are more likely to be male than female.

Sex-allocation theory predicts that females should preferentially produce offspring of the sex with greater fitness potential. In socially monogamous animal species, extra-pair mating often increases the variance in fitness of sons relative to daughters. Thus, in situations where offspring sired by a female's extra-pair mate(s) will typically have greater fitness potential than offspring sired by the within-pair mate, sex-allocation theory predicts that females will bias the sex of offspring sired by extra-pair mates towards male. We examined the relationship between offspring sex and paternity over six breeding seasons in an Illinois population of the house wren (Troglodytes aedon), a cavity-nesting songbird. Out of the 2345 nestlings that had both sex and paternity assigned, 350 (15%) were sired by extra-pair males. The sex ratio of extra-pair offspring, 0.534, was significantly greater than the sex ratio of within-pair offspring, 0.492, representing an increase of 8.5 per cent in the proportion of sons produced. To our knowledge, this is the first confirmed report of female birds increasing their production of sons in association with extra-pair fertilization. Our results are consistent with the oft-mentioned hypothesis that females engage in extra-pair mating to increase offspring quality.

Extra‐pair paternity in the socially monogamous mountain bluebird Sialia currucoides and its effect on the potential for sexual selection

Sexual selection theory posits that ornamental traits can evolve if they provide individuals with an advantage in securing multiple mates. That male ornamentation occurs in many bird species in which males pair with a single female is therefore puzzling. It has been proposed that extra‐pair mating can substantially increase the variance in reproductive success among males in monogamous species, thus increasing the potential for sexual selection. We documented the frequency of extra‐pair paternity and examined its effect on variation in male reproductive success in the mountain bluebird Sialia currucoides, a socially monogamous songbird in which males possess brilliant plumage ornamentation. Extra‐pair paternity was common in our Wyoming study population, with 72% of broods containing at least one extra‐pair offspring. The standardized variance in actual male reproductive success (i.e., the total number of within‐pair and extra‐pair offspring sired) was more than seven times higher than the variation in apparent success (i.e., success assuming that no extra‐pair mating occurred). Success at siring within‐pair and extra‐pair offspring both contributed to the variation in overall male reproductive success. Within‐pair success, however, did not predict a male's level of extra‐pair success, suggesting that males do not sacrifice within‐pair paternity to gain extra‐pair paternity. Calculation of the sexual selection (Bateman) gradient showed that males sire approximately two additional offspring for each extra‐pair mate that we identified. Thus, in this sexually dichromatic species, extra‐pair mating increases the variance in male reproductive success and provides the potential for sexual selection to act.

Effects of extrapair paternity and sex on nestling growth and condition in the collared flycatcher, Ficedula albicollis

Extrapair fertilizations (EPFs) have been found in most socially monogamous passerine species. EPFs are generally beneficial for males because they increase the number of sired offspring. The benefit accrued by females, however, is less obvious. Maternal benefits may involve fertility insurance, increased genetic variability of the offspring, and improved offspring quality via compatible genes or ‘good genes’. In a Hungarian population of the collared flycatcher, we investigated whether the occurrence of extrapair young (EPY) in a brood could be predicted by the traits of the females or their social mates, and whether EPY were superior to their half sibs in terms of growth and fledging condition. We found that 55.7% of the broods contained EPY. The females' participation in extrapair copulations (EPCs) was not related to any of the characteristics of their mates (body size, condition, wing and forehead patch size). The EPY did not differ from their half sibs in any measures of offspring quality. The half sibs had similar embryonic and postembryonic growth and fledged with similar body condition. Female body size was related to extrapair paternity: larger females were less likely to produce mixed-paternity broods. This suggests that the role of female traits in EPCs deserves more attention. We also found that male nestlings grew faster than females, although females could catch up by the time of fledging, so we argue that sex-dependent development should be taken into account in studies using nestling growth as a measure of nestling quality.

Dopamine regulation of social choice in a monogamous rodent species

There is growing appreciation that social decision making in humans is strongly influenced by hedonic and emotional processing. The field of social neuroeconomics has shown that neural systems important for reward are associated with social choice and social preferences in humans. Here, we show that the neurobiology of social preferences in a monogamous rodent species, the prairie vole, is also regulated by neural systems involved in reward and emotional processing. Specifically, we describe how mesolimbic dopamine transmission differentially mediates the formation and maintenance of monogamous pair bonds in this species. Thus, reward processing exerts tremendous regulation over social choice behaviors that serve as the foundation of a rather complex social organization. We conclude that prairie voles are an excellent model system for the neuroscience of social choice and that complex social decision-making can be robustly explained by reward and hedonic processing.