Monogamous Species Research Articles

Male procurement of breeding site is valued over male size by monogamous female convict cichlids (Amatitlania nigrofasciata)

In many monogamous species, sexual selection often occurs through female mate choice, which is usually based on male characteristics such as size. However, the presence of a breeding site also might be equally or more valued than male size for substrate brooders. This study investigated the importance of a large mate versus the presence of a breeding site in the monogamous convict cichlid (Amatitlania siquia). If breeding sites are more valued than male size, then we predict that females will choose the male with breeding site regardless of his size. To test our hypothesis, males were confined to separate compartments with only one male receiving a breeding site, but females swam freely. In the experimental groups, one male was larger than the other, but both males were equal in size for the control group. Females significantly preferred small males with a breeding site more often than large males without a breeding site; thus, the presence of a breeding site seems to be more valued than male size by female convict cichlids.

Neural correlates of mating system diversity: oxytocin and vasopressin receptor distributions in monogamous and non-monogamous Eulemur

Contemporary theory that emphasizes the roles of oxytocin and vasopressin in mammalian sociality has been shaped by seminal vole research that revealed interspecific variation in neuroendocrine circuitry by mating system. However, substantial challenges exist in interpreting and translating these rodent findings to other mammalian groups, including humans, making research on nonhuman primates crucial. Both monogamous and non-monogamous species exist within Eulemur, a genus of strepsirrhine primate, offering a rare opportunity to broaden a comparative perspective on oxytocin and vasopressin neurocircuitry with increased evolutionary relevance to humans. We performed oxytocin and arginine vasopressin 1a receptor autoradiography on 12 Eulemur brains from seven closely related species to (1) characterize receptor distributions across the genus, and (2) examine differences between monogamous and non-monogamous species in regions part of putative “pair-bonding circuits”. We find some binding patterns across Eulemur reminiscent of olfactory-guided rodents, but others congruent with more visually oriented anthropoids, consistent with lemurs occupying an ‘intermediary’ evolutionary niche between haplorhine primates and other mammalian groups. We find little evidence of a “pair-bonding circuit” in Eulemur akin to those proposed in previous rodent or primate research. Mapping neuropeptide receptors in these nontraditional species questions existing assumptions and informs proposed evolutionary explanations about the biological bases of monogamy.

Assortative pairing for boldness and consequences for reproductive success in Montagu’s harrier

AbstractBehavioural combination within pairs depending on personality and plasticity might influence reproductive success. However, studies testing this hypothesis are rare, especially in the case of monogamous species with bi-parental care in which the sexes exhibit different behavioural roles. In this study, we investigated the pairing patterns for both boldness and boldness plasticity in Montagu’s harriers (Circus pygargus), a species with sex-specific care, and the consequences for their reproductive success. We measured individual boldness and plasticity for both sexes, and we assessed the pairing pattern in the Montagu’s harrier population for these two traits. We calculated four indices to characterize the behavioural association within pairs: pair boldness, boldness similarity within pairs, pair plasticity and plasticity similarity within pairs. The relationship between the behaviour of the parents and the reproductive success was then tested through these four indices. We found a pattern of assortative pairing based on both boldness and plasticity in the Montagu’s harrier population. Within-pair similarity of plasticity had a significant effect on the reproductive success, which was higher for less similar pairs than for more similar pairs. Our results question the origin of this pairing pattern and suggest that ecological constraint and not sexual selection could be the major driver.

Coevolution of female fidelity and male help in populations with alternative reproductive tactics.

In socially monogamous species, pair-bonded males often continue to provide care to all offspring in their nests despite some degree of paternity loss due to female extra-pair copulation. Previous theoretical models suggested that females can use their within-pair offspring as ‘hostages' to blackmail their social mates, so that they continue to provide care to the brood at low levels of cuckoldry. These models, however, rely on the assumption of sufficiently accurate male detection of cuckoldry and the reduction of parental effort in case of suspicion. Therefore, they cannot explain the abundant cases where cuckolded males continue to provide extensive care to the brood. Here we use an analytical population genetics model and an individual-based simulation model to explore the coevolution of female fidelity and male help in populations with two genetically determined alternative reproductive tactics (ARTs): sneakers that achieve paternity solely via extra-pair copulations and bourgeois that form a mating pair and spend some efforts in brood care. We show that when the efficiency of mate guarding is intermediate, the bourgeois males can evolve to ‘specialize' in providing care by spending more than 90% of time in helping their females while guarding them as much as possible, despite frequent cuckoldry by the sneakers. We also show that when sneakers have tactic-specific adaptations and thus are more competitive than the bourgeois in gaining extra-pair fertilizations, the frequency of sneakers and the degrees of female fidelity and male help can fluctuate in evolutionary cycles. Our theoretical predictions highlight the need for further empirical tests in species with ARTs.

Variance in within-pair reproductive success influences the opportunity for selection annually and over the lifetimes of males in a multibrooded songbird.

In socially monogamous species, male reproductive success consists of "within-pair" offspring produced with their socially paired mate(s), and "extra-pair" offspring produced with additional females throughout the population. Both reproductive pathways offer distinct opportunities for selection in wild populations, as each is composed of separate components of mate attraction, female fecundity, and paternity allocation. Identifying key sources of variance and covariance among these components is a crucial step toward understanding the reproductive strategies that males use to maximize fitness both annually and over their lifetimes. We use 16 years of complete reproductive data from a population of black-throated blue warblers (Setophaga caerulescens) to partition variance in male annual and lifetime reproductive success, and thereby identify if the opportunity for selection varies over the lifetimes of individual males and what reproductive strategies likely favor maximum lifetime fitness. The majority of variance in male reproduction was attributable to within-pair success, but the specific effects of individual components of variance differed between total annual and total lifetime reproductive success. Positive overall lifetime covariance between within-pair and extra-pair components indicates that males able to maximize within-pair success, particularly with double-brooding females, likely achieve higher overall lifetime fitness via both within-pair and extra-pair reproductive pathways.

Urban life promotes delayed dispersal and family living in a non-social bird species

In some vertebrate species, family units are typically formed when sexually mature individuals delay dispersal and independent breeding to remain as subordinates in a breeding group. This behaviour has been intensively studied in gregarious species but has also been described in non-social species where ecological and evolutionary drivers are less known. Here, we explore factors that favour delayed dispersal and family living and potential benefits associated with this strategy in a non-social, monogamous species (the burrowing owl, Athene cunicularia) occupying urban and rural habitats. Our results show that family units arise when first-year individuals, mainly males, delay their dispersal to stay in their natal nests with their parents. This delayed dispersal, while still uncommon, was more prevalent in urban (7%) than in rural (3%) habitats, and in areas with high conspecific density and productivity. Birds delaying dispersal contributed to the genetic pool of the offspring in 25% of the families analysed, but did not increase the productivity of the nests where they remained. However, their presence was related to an improvement in the body condition of chicks, which was ultimately linked to a slightly positive effect in offspring future survival probabilities. Finally, delayed dispersers were recruited as breeders in high-quality urban territories and closer to their natal nests than individuals dispersing during their first year of life. Thus, our results suggest that delaying dispersal may be mainly related to opportunities to inheriting a good quality territory, especially for males. Our study contributes to understanding the role played by habitat quality in promoting delayed dispersal and family living, not only in social but also non-social species, highlighting its impact in the ecology and evolution of animal populations.

Loss of Extra-pair Paternity is not Associated with Decreased Paternal Investment in Mixed-paternity Broods or Unrelated Nestlings in the Varied Tit, Parus varius

Males of socially monogamous bird species may be faced with providing costly care for unrelated offspring when nests have extra-pair young (EPY). Theoretical models predict that cuckolded males should lower their parental investment as the likelihood of paternity decreases. However, empirical data are not always in support of this prediction. Here, we explore parental behaviours within the context of extra-pair patenity (EPP) in a population of the varied tit Parus varius in China. The results showed that 39.5% of nests were cuckolded and 16.4% of chicks were sired by extra-pair males. We found no evidence that male and female varied tits reduced their feeding rates or relative feeding effort to EPP broods, or that they decreased provisioning for EPY in mixed broods. There was also no direct effect of EPP on the reproductive success of breeding adults and the body condition nestlings near fledging. The lack of reliable cues of EP copulations (EPC)s by social mates available for the males, and/or the absence of strictly environmental pressure on males that would favor discrimination may account for a lack of an adjustment in feeding effort. The absence of discrimination between own and EPP chicks in parental care suggests that females pay no fitness cost as a result of EPCs, which may explain the high frequency of EPY in nests.

Interspecific aggression and defence of extra nest sites in two species of songbirds

AbstractInterspecific competition is expected when two species share resource needs. For example, secondary cavity‐nesting birds may compete vigorously for suitable nest sites both within and among species. However, little is known of whether monogamous species defend more than one nest site on their territory after breeding has begun, and in particular whether they are aggressive against other species. Defending extra nest sites may be adaptive because they may be used for renesting after a failure or to produce a second brood. We studied interactions between a monogamous, resident bird, the great tit Parus major and a migrant, the pied flycatcher Ficedula hypoleuca, providing nest boxes in woodlands in Norway. Agonistic behaviours may be subtle and easily overlooked so we experimentally placed caged male pied flycatchers near nests of great tits and at a dyad of empty nest boxes erected in the territory 25 m away. We filmed interactions between species at 21 sites in the egg‐laying period of the tit, and at 26 nest sites during incubation. Male great tits showed aggression towards the caged flycatcher both at their own nest box and at the nest boxes erected at a distance. We manipulated the external appearance of the nest boxes with painted designs around the entrances but the intensity of aggression at the empty nest boxes did not depend on whether those boxes matched the nest box with the tit nest and was not correlated with tit clutch size. Neither was the intensity of display activity at each nest box by the flycatchers that settled associated with these variables. The results are discussed in relation to hypotheses for nest site choice involving interspecific social learning and aggression.

Pathways linking female personality with reproductive success are trait- and year-specific

AbstractPersonality (i.e., among-individual variation in average behavior) often covaries with fitness, but how such personality–fitness relationships come about is poorly understood. Here, we explore potential mechanisms by which two female personality traits (female–female aggression and female nest defense as manifested by hissing behavior) were linked with annual reproductive success in a population of great tits (Parus major), a socially monogamous species with biparental care. We hypothesized that personality-related differences in reproductive success result from variation in reproductive decision (lay date, brood size) and/or parental provisioning rates. Relative support for these mechanisms was evaluated using path analysis on data collected in two successive years. We reveal that larger broods were provisioned at a higher rate by both parents and that female, but not male, provisioning rate was involved in the trade-off between offspring number (brood size) and fledgling mass. Among-individual variation in female aggression, via its association with female provisioning rate, was negatively linked to fledgling mass (i.e., indirect effect), yet only in one of the study years. Male provisioning rate did not influence these relationships. In contrast, among-individual variation in hissing behavior was directly and negatively linked with fledgling mass in both years, via an underlying mechanism that remains to be identified (i.e., direct effect). Together, our findings emphasize that personality–fitness relationships may come about via different mechanisms across personality traits and/or years, thereby illustrating additional complexity in how selection might act on and maintain among-individual variation in behavioral phenotypes in the wild.

Postcopulatory sexual selection and the evolution of shape complexity in the carnivoran baculum.

The baculum is an enigmatic bone within the mammalian glans penis, and the driving forces behind its often bizarre shape have captivated evolutionary biologists for over a century. Hypotheses for the function of the baculum include aiding in intromission, stimulating females and assisting with prolonged mating. Previous attempts to test these hypotheses have focused on the gross size of the baculum and have failed to reach a consensus. We conducted three-dimensional imaging and apply a new method to quantify three-dimensional shape complexity in the carnivoran baculum. We show that socially monogamous species are evolving towards complex-shaped bacula, whereas group-living species are evolving towards simple bacula. Overall three-dimensional baculum shape complexity is not related to relative testes mass, but tip complexity is higher in induced ovulators and species engaging in prolonged copulation. Our study provides evidence of postcopulatory sexual selection pressures driving three-dimensional shape complexity in the carnivore baculum.

Sexual dimorphism of the major chela and sex ratio as indicators of the mating system in the estuarine snapping shrimpAlpheus colombiensisWicksten, 1988 (Decapoda: Caridea: Alpheidae)

AbstractThe sexual selection over traits that favor access to mating partners could promote the emergence of sexual dimorphism when the pressure is different between sexes. Monogamous species are considered to have a low degree of sexual dimorphism. The highly diverse snapping shrimps are usually regarded as monogamous, but the mating system has been studied only in few species. We aimed to provide insights into the mating system and sexual dimorphism of Alpheus colombiensisWicksten, 1988. The adult sex ratio was female biased, and solitary ovigerous females were found, suggesting a temporary mate guarding type of mating system. Our results also revealed sexual dimorphism on the snapping claw, which is larger in males than in females. The male’s snapping claw is probably under sexual selection, which can be mediated by male-male competition or female choice. We also estimated the A. colombiensis female size at maturity at 5.2 ± 0.76 mm. Our results contradict the common idea that snapping shrimps are monogamous species, and support that A. colombiensis probably have a temporary mate guarding (e.g., males can sexually interact with more than one female, in opposition to sexual monogamy). This study also sustains the growing evidence that alpheid shrimps display snapping claw sexual dimorphism.

Haemosporidian parasites of Neotropical birds: Causes and consequences of infection

Abstract Haemosporidian parasites of the genera Plasmodium, Haemoproteus, and Leucocytozoon are among the best studied parasites of Neotropical birds. Here, we describe variation in haemosporidian prevalence (i.e. the proportion of infected individuals in a sampled population) in Neotropical birds. We review correlates of haemosporidian prevalence (including several avian life-history traits, climate, and season) and the population and evolutionary consequences of infection for Neotropical birds. We find that prevalence varies among avian taxonomic families, genera, and even among species within the same genus, suggesting that prevalence reflects multiple factors, some of which (e.g., avian incubation period) are associated with avian family-level variation in prevalence while others (e.g., avian abundance) are associated with variation in prevalence among closely related host species. We find few correlates of prevalence that have been consistently demonstrated across studies. Prevalence in populations of many Neotropical birds has been estimated by microscopic examination of blood smears, which affords limited opportunity for comparison with data generated by molecular methods. However, at one site in the Brazilian Cerrado for which we have data, prevalence determined by microscopy does not correlate with prevalence determined by molecular methods for Plasmodium, but the 2 data types are positively correlated for Haemoproteus. Haemosporidians have been hypothesized to play a role in avian sexual selection, and we find the prevalence of Haemoproteus to be lower in polygynous species than in socially monogamous species in the Neotropics, confirming a pattern shown previously among Nearctic birds.

Intrasexual selection: Kin competition increases male-male territorial aggression in a monogamous cichlid fish.

During intrasexual competition, individuals of the same sex compete for access to breeding sites and mating partners, often accompanied by aggressive behavior. Kin selection theory predicts different kin‐directed social interactions ranging from cooperation to aggression depending on the context and the resource in question. Kin competition reducing indirect fitness might be avoided by actively expelling relatives from territories and by showing higher aggression against kin. The West‐African cichlid Pelvicachromis taeniatus is a monogamous cave breeder with males occupying and defending breeding sites against rivals. This species is capable of kin recognition and shows kin‐preference during juvenile shoaling and mate choice. However, subadults of P. taeniatus seem to avoid the proximity of same‐sex kin. In the present study, we examined territorial aggression of territory holders against intruding related and unrelated males as well as intruder's behavior. We observed higher aggression among related competitors suggesting that related males are less tolerated as neighbors. Avoidance of intrasexual competition with relatives might increase indirect fitness of males in monogamous species.

What's in a Moment: What Can Be Learned About Pair Bonding From Studying Moment-To-Moment Behavioral Synchrony Between Partners?

Our understanding of the behavioral and physiological mechanisms of monogamy largely comes from studies of behavioral interactions unique to pair-bonded individuals. By focusing on these highly marked behaviors, a remarkable conservation in the mechanisms underlying pair bonding has been revealed; however, we continue to know very little about the range of behavioral and neurobiological mechanisms that could explain the great diversity of pair-bonding phenotypes that exists both within and across species. In order to capture the dynamic nature of bonds over time and across contexts, we need specific, operationally-defined behavioral variables relevant across such a diversity of scenarios. Additionally, we need to be able to situate these behavioral variables within broader frameworks that allow us to interpret and compare patterns seen across species. Here I review what is known about behavioral synchrony with respect to pair bonding and discuss using synchrony as such a variable as well as a framework to expand on our understanding of pair bonding across timescales, contexts and species. First, I discuss the importance of behavioral synchrony and parental coordination for reproductive success in monogamous biparental bird species. Second, I highlight research documenting the critical importance of interpersonal coordination for human social relationships. Finally, I present recent work that experimentally bridges these lines of research by quantifying moment-to-moment behavioral synchrony during brief social interactions in zebra finch dyads. All together, these distinct perspectives support the notion that synchrony (1) is a shared premise for sociality across species, (2) is deeply shaped by social experiences, and (3) exists across timescales, behaviors, and levels of physiology. Conceptualizing pair bonding through the framework of behavioral synchrony is likely to facilitate a deeper understanding of the nuances of how social experiences and interactions impact the brain and behavior.

Heritability of the extra-pair mating behaviour of the pied flycatcher in Western Siberia.

Males and females take part in extra-pair copulations in most socially monogamous bird species. The mechanisms leading to the frequent occurrence of extra-pair offspring in socially monogamous couples are strongly debated and unresolved, and they are often difficult to distinguish from one another. Most hypotheses explaining the evolution of extra-pair reproduction suggest selective and adaptive scenarios for their origination and persistence. Is extra-pair paternity a heritable trait? We evaluated the heritability of extra-pair paternity in the pied flycatcher (Ficedula hypoleuca) nesting in Western Siberia. Estimated heritability was low: depending on the model used, the point estimate of the heritability (mode) varied from 0.005 to 0.11, and the bounds of the 95% confidence interval are [0–0.16] in the widest range. Thus, it seems that extra-pair mating behaviour in the pied flycatchers is a plastic phenotypic mating tactic with a small or no genetic component. Our data can help to understand the evolution of extra-pair mating behaviour in socially monogamous species.

The dance of the Cape gannet may contain social information on foraging behaviour

Social information percolates through a variety of channels to influence animal decision making, with a notable effect on reproductive and feeding success. Colonial central place foragers can reduce time to locate ephemeral food patches and/or increase foraging rate by following their informed peers, parasitizing direction of returning successful foragers, or being intentionally informed on distant food locations at the colony (e.g. the waggle dance of the honey bee). Ceremonial behaviours may also deliver social foraging information between mates, which can spread inadvertently to neighbours. Here we tested for information display in Cape gannets, Morus capensis, a socially monogamous species, during the elaborate dance ceremony performed each time a partner returns to the nest during the breeding season. We tracked fine-scale foraging behaviour of gannets using bird-borne GPS recorders, and video-recorded their subsequent dance ceremony, which involved up to 14 different displays. As we hypothesized, dance characteristics were associated with foraging trip features. Notably, overall dance duration was negatively linked to foraging trip duration, which was highly positively correlated with foraging range, foraging path length and time spent foraging during the trip. Overall dance duration was also negatively linked with distance to the main foraging grounds. Additionally, the duration of preening behaviour was related to the bearing of the main feeding spot. The latter relationship was supported by a Bayesian model averaging analysis, allowing inferences robust to multiple comparisons. Overall, ceremonial behaviour may provide social foraging information on feeding locations, while evidence for further information transfer to the mate or neighbours was not tested here. Frequent updating on prey spatial distribution, inadvertently communicated or not, should be particularly valuable for predators tracking ephemeral prey patches, providing an additional advantage to colonial living. Our results may have strong implications for cultural evolution in animal societies.

Common Field Data Limitations Can Substantially Bias Sexual Selection Metrics.

Sexual selection studies widely estimate several metrics, but values may be inaccurate because standard field methods for studying wild populations produce limited data (e.g., incomplete sampling, inability to observe copulations directly). We compared four selection metrics (Bateman gradient, opportunity for sexual selection, opportunity for selection, and ) estimated with simulated complete and simulated limited data for 15 socially monogamous songbird species with extrapair paternity (4%-54% extrapair offspring). Inferring copulation success from offspring parentage creates nonindependence between these variables and systematically underestimates copulation success. We found that this introduces substantial bias for the Bateman gradient, opportunity for sexual selection, and . Notably, 47.5% of detected Bateman gradients were significantly positive for females, suggesting selection on females to copulate with multiple males, although the true Bateman gradient was zero. Bias generally increased with the extent of other sources of data limitations tested (nest predation, male infertility, and unsampled floater males). Incomplete offspring sampling introduced bias for all of the metrics except the Bateman gradient, while incomplete sampling of extrapair sires did not introduce additional bias when sires were a random subset of breeding males. Overall, our findings demonstrate how biases due to field data limitations can strongly impact the study of sexual selection.

The role of female investment in a sexual arms race

Forced copulations are common among waterfowl species (Anatidae), a group with relatively large eggs and very precocial young. They can be viewed as the outcome of an overt sexual conflict, and an evolutionary arms race between the sexes. We examined the female choice hypothesis suggested, but not properly tested by Briskie and Montgomerie (1997) and Montgomerie and Briskie (2007), that penis size in male ducks might correlate with female investment in eggs, predicting that in species where females lay larger eggs, penis size might be larger, because females would be more reluctant to abandon their eggs if forced to copulate. A larger data set than in earlier studies enabled us to test that hypothesis in a comparative way. Our results compelled us to reject the female choice hypothesis since egg size is negatively correlated with penis length and the number of vaginal spirals, both being seen as adaptations to frequent forced copulations. The apparent trade‐off between egg size and morphological defences (vaginal spirals) is strong particularly among monogamous species. Overall, we conclude that factors that set a lower limit for egg size constrain the morphological defences of females and the arms race between the sexes in waterfowl.

Why do females of a lekking species mate with multiple males?

In Focus: Rivers, P. R., & DuVal, E. H. (2020). Multiple paternity in a lek mating system: Females mate multiply when they choose inexperienced sires. Journal of Animal Ecology, 89, 1142-1152. In many socially monogamous species with biparental care, some females engage in extra-pair copulations, despite the apparent risk of losing male help in raising their brood. Why females mate with multiple males remains the focus of intense debate, but may be linked to constraints in social mate choice. If so, multiple mating is not expected in a lekking mating system, where females receive no resources from the male other than sperm and are free to choose the 'best' mate to sire their offspring. Rivers and DuVal (2020) report on the occurrence of multiple paternity in lekking lance-tailed manakins and test several hypotheses to explain it. Their study shows that lower-ranked males and males with less experience were more likely to share paternity. However, the process underlying this pattern remains puzzling. The authors suggest female choice related to male characteristics that change with experience as an explanation, but alternative scenarios cannot be excluded.

Season-specific carryover of early life associations in a monogamous bird species

Social relationships can have important fitness consequences. Although there is increasing evidence that social relationships carry over across contexts, few studies have investigated whether relationships formed early in life are carried over to adulthood. For example, juveniles of monogamous species go through a major life history stage transition, pair formation, during which the pair bond becomes a central unit of the social organization. At present, it remains unclear whether pair members retain their early life relationships after pair formation. We investigated whether same-sex associations formed early in life carry over into adulthood and whether carryover was dependent on season, in a monogamous species. We also investigated the role of familiarity, genetic relatedness and aggression on the perseverance of social associations. We studied the social structure before and after pair formation in captive barnacle geese, Branta leucopsis, a highly social, long-lived, monogamous species. We constructed association networks of groups of geese before pair formation, during the subsequent breeding season and in the following wintering season. Next, we studied how these associations carried over during seasonal changes. We found that early life associations in females were lost during the breeding season but resurfaced during the subsequent wintering season. In males, the early life associations persisted across both seasons. Association persistence was not mediated by genetic relatedness or familiarity. The high level of aggressiveness of males, but not females, in the breeding season suggests that males may have played a key role in shaping both their own social environment and that of their partners. We show that early life social relationships can be maintained well into later life. Such relationships can be sustained even if they are temporarily disrupted, for example due to reproductive behaviour. Our findings therefore highlight that the early life social environment can have lifelong consequences for individuals’ social environment.