Correlates and Consequences of the Pair Bond in Steller's Jays

Individuals that maintain pair bonds over multiple breeding attempts are often able to improve reproductive success compared to conspecifics that switch partners. However, the behavioral mechanisms driving this ‘mate familiarity effect’ are still largely unknown. We investigated whether long‐standing pairs in the long‐lived, socially monogamous Steller's jay improved their coordination of movements and behaviors, invested more time in pair bond maintenance, or became more compatible in their tendency to take risks over time compared to newly established pairs. We then compared these pair bond characteristics for successful and unsuccessful partnerships in terms of producing offspring. Jay partners regularly perched together, gave soft contact calls and travelled as a pair even in the non‐breeding season. However, the proportion of observations jay partners spent in each other's company (pair tenacity) was unrelated to risk‐taking behavior of pair members, pair bond duration, or the performance of subtle pair bond maintenance behaviors (i.e., a principle component of behaviors, including soft contact calls, proximity to mates, and frequency of arrival and departure flights with mate). However, evidence suggests that reproductive performance still improved in continuing compared to new pair bonds in Steller's jays. Variation in pair tenacity and frequency of pair bond behaviors may be inconsequential because of jays’ overall high level of contact with partners. Additionally, if jays are able to maximize familiarity early in the pair bond through high overall pair tenacity, the additional benefit of increasing coordination and familiarity with increasing pair bond age may be limited.     

Testosterone and Partner Compatibility: Evidence and Emerging Questions

In socially monogamous species pair partners often form and maintain long‐term pair‐bonds. Relationships between pair partners are dynamic and driven by both cooperation and conflicts between the sexes. Successful reproduction depends on behavioural coordination and cooperation, which includes continuing mutual responsiveness between the pair partners, as well as conflicts, for example, over parental investment. Gonadal hormones, such as testosterone, centrally regulate reproduction and are potentially involved in the formation and maintenance of pair‐bonds. In greylag geese ( Anser anser), a positive within‐pair testosterone co‐variation (TC) among pair partners has been observed at the seasonal level. Goose pairs with a higher TC have a higher reproductive output and long‐term success than pairs with lower TC, but it is still not clear whether TC is cause or consequence. In this article, I (i) summarize the evidence for hormonal partner compatibility in geese, (ii) ask whether TC is restricted to monogamous and biparental systems and (iii) synthesize open questions or new aspects of information we may draw by studying hormonal partner compatibility. From longitudinal studies in geese, we know that TC decreases with pair‐bond duration. This indicates some form of ‘attritional effect’ over the years rather than an improved breeding performance with increasing familiarity between the partners (the ‘mate familiarity hypothesis’). Under certain circumstances, for example, during ageing, selection may not act in the same direction for males and females. Partner preference increased female androgen levels during laying and social instability may impinge on the pair's TC. Data from other species show that TC is not restricted to monogamous species, but presumably the link between TC and reproductive output may be primarily relevant in species with biparental care. This article surveys the major unanswered questions relating to hormonal partner compatibility and previews potential future work for addressing those open issues.     

Mate Familiarity Affects Pairing Behaviour in a Long‐Term Monogamous Lizard: Evidence from Detailed Bio‐Logging and a 31‐Year Field Study

Long‐term monogamy is most prevalent in birds but is also found in lizards. We combined a 31‐year field study of the long‐lived, monogamous Australian sleepy lizard, Tiliqua rugosa, with continuous behavioural observations through GPS data logging, in 1 yr, to investigate the duration of pair bonds, rates of partner change and whether either the reproductive performance hypothesis or the mate familiarity hypothesis could explain this remarkable long‐term monogamy. The reproductive performance hypothesis predicts higher reproductive success in more experienced parents, whereas the mate familiarity hypothesis suggests that effects of partner familiarity select for partner retention and long‐term monogamy. Rates of partner change were below 34% over a 5‐yr period and most sleepy lizards formed long‐term pair bonds: 31 partnerships lasted for more than 15 yr, 110 for more than 10 yr, and the recorded maximum was 27 yr (ongoing). In the year when we conducted detailed observations, familiar pairs mated significantly earlier than unfamiliar pairs. Previous pairing experience (total number of years paired with previous partners) had no significant effect. Early mating often equates to higher reproductive success, and we infer that is the case in sleepy lizards. Early mating of familiar pairs was not due to better body condition. We propose two suggestions about the proximate mechanisms that may allow familiar pair partners to mate earlier than unfamiliar partners. First, they may have improved coordination of their reproductive sexual cycles to reach receptivity earlier and thereby maximise fertilisation success. Second, they may forage more efficiently, benefiting from effective information transfer and/or cooperative predator detection. Those ideas need empirical testing in the future. Regardless of the mechanism, our observations of sleepy lizard pairing behaviour support the mate familiarity hypothesis, but not the reproductive performance hypothesis, as an explanation for its long‐term monogamous mating system.     

Does time after pair bond disruption affect subsequent reproduction in the socially monogamous woodland vole (Microtus pinetorum)?

Disruption of the pair bond between socially monogamous animals leads to changes in behavior, which may have reproductive consequences. There are two alternative hypotheses to explain the effect of the length of time since pair bond disruption on subsequent reproduction. One hypothesis predicts that voles housed immediately with a new opposite-sex conspecific will be as likely to produce litters and will produce them as quickly as voles separated from their initial mate for longer. Alternatively, if attachment between mates is enduring, we expect that more voles separated longer from their previous mates will produce litters and produce them sooner than voles re-paired immediately after separation from their initial mates. Woodland voles, paired with opposite-sex conspecifics, remained together until parturition. Mates were then separated for 0, 7, or 14 days until re-pairing with an opposite-sex conspecific. Pair bond disruption did not prevent males and females from mating subsequently, which was consistent with data from our breeding colony. In addition, the length of time an individual remained alone after pair bond disruption did not affect the latency to produce a litter. Our results show that having been paired previously does not affect subsequent reproduction in this socially monogamous vole.     

Survival costs of within‐ and between‐season mate change in the European blackbird Turdus merula

Many studies of socially monogamous birds discuss the adaptive role of between‐season partner change, but only a handful of them refer to the benefits of pair fidelity in terms of increased survival. Moreover, there are no studies describing the benefits of within‐season mate retention. Our data relating to an urban population of European blackbirds Turdus merula enabled us to test the dependence of survival on pair faithfulness. Because blackbirds divorce within and between seasons, we were able to test the influence of pair faithfulness on their within‐ and between‐season survival and mate fidelity. For this purpose, we used a multievent capture–mark–recapture (MECMR) statistical model, which is based on recapture rates and different pair states (faithful to mate, paired with new partner, or dead). Our study indicated that between‐ and within‐season survival depends on pair states: pair‐bond duration increases survival to the next capture occasion in both sexes. We found that the pair‐bond duration to the current partner increased the chances of being with the same partner during the next breeding occasion, although we failed to find any within‐season pair‐bond influence for females. Our results showed sex differences in mating at the end of the season: females had a much smaller chance of breeding with the current new partner in the next year. This study has demonstrated that within‐ and between‐season survival is dependent on mate retention, and we discuss this in the context of how searching for a new partner could affect the birds’ survival.     

Variable Social Mating System in the Sedge Warbler,Acrocephalus schoenobaenus

We studied the mating system in a local population of colour-ringed sedge warblers in south Central Sweden in 1990–92. Of 58 territorial males, 59% were socially monogamous, 14% socially polygynous and 27% unpaired. Socially polygynous males in general paired with two females: the only exception was one male that formed pair bonds with three females. Among the males that formed a pair bond, 38% resumed singing after their first female had started egg-laying or incubation and 50% of the paired males that resumed singing succeeded in attracting a second female. Hence, despite a consistently male-biased sex ratio in the population a large proportion of the males tried to become polygynous and they were often successful. The frequency of extra-pair matings did not differ between monogamous and polygynous males. Of 47 breeding females, 6.4% were sequentially socially polyandrous. In two out of three cases, the females fed the young of their first broods until independence before initiating the second brood. In the third case the female deserted her newly fledged young and these were instead cared for by a neighbouring male. DNA fingerprinting revealed that this male had not sired any of these young. Each of the sequentially polyandrous females successfully raised both their broods, and their annual reproductive success was slightly higher than the average for the polygynous males. When the sequentially socially polyandrous females initiated their second brood, their primary male (in all cases polygynous males), cared for young in their secondary female's nest. In all cases, the sequentially polyandrous females formed second pair bonds with unpaired males that were close neighbors. This suggests that females switched pair male for their second brood to obtain a mate that was more likely to provide them with direct benefits (e.g. parental care).     

Correlates of genetic monogamy in socially monogamous mammals: insights from Azara's owl monkeys

Understanding the evolution of mating systems, a central topic in evolutionary biology for more than 50 years, requires examining the genetic consequences of mating and the relationships between social systems and mating systems. Among pair-living mammals, where genetic monogamy is extremely rare, the extent of extra-group paternity rates has been associated with male participation in infant care, strength of the pair bond and length of the breeding season. This study evaluated the relationship between two of those factors and the genetic mating system of socially monogamous mammals, testing predictions that male care and strength of pair bond would be negatively correlated with rates of extra-pair paternity (EPP). Autosomal microsatellite analyses provide evidence for genetic monogamy in a pair-living primate with bi-parental care, the Azara''s owl monkey (Aotus azarae). A phylogenetically corrected generalized least square analysis was used to relate male care and strength of the pair bond to their genetic mating system (i.e. proportions of EPP) in 15 socially monogamous mammalian species. The intensity of male care was correlated with EPP rates in mammals, while strength of pair bond failed to reach statistical significance. Our analyses show that, once social monogamy has evolved, paternal care, and potentially also close bonds, may facilitate the evolution of genetic monogamy.     

Genetic monogamy in single-male groups of acorn woodpeckers, Melanerpes formicivorus

Acorn woodpeckers have one of the most complex social systems of any bird species. Breeding units range in size from monogamous pairs to groups of 15 birds that include multiple breeding males and females as well as nonreproductive helpers-at-the-nest. Groups form when young remain at their natal nest to help their parents breed or when single-sex coalitions of siblings disperse to fill a reproductive vacancy on another territory. Plural breeding and helping behaviour are thought to be favoured through indirect fitness benefits for individuals that would otherwise be unable to breed due to a shortage of reproductive vacancies on territories with acorn stores. We report the results of multi-locus DNA fingerprinting of 51 offspring from 18 nests of 16 socially monogamous pairs of acorn woodpeckers. If socially monogamous females mate outside the pair-bond, indirect fitness benefits for cobreeders and helpers will be significantly reduced. Monogamous pairs accounted for all but one of the 51 offspring we tested; the single exception was apparently sired by the putative father, but the putative mother was excluded from maternity. Our results indicate that individuals remaining on their natal territories as helpers are generally the genetic offspring of the pair they help. They also suggest that single-sex coalitions offspring dispersing together from nests of socially monogamous pairs will be full-siblings.     

Mated pairs of owl monkeys (Aotus nancymaae) exhibit sex differences in response to unfamiliar male and female conspecifics

In socially monogamous species, mate‐guarding could be a reproductive strategy that benefits both males and females, especially when males contribute to parental care. By actively guarding mates, males may reduce their chances of being cuckolded, whereas females that mate‐guard may reduce the likelihood that their mates will desert them or acquire additional mates, and hence limit or reduce paternal care of offspring. Owl monkeys (Aotus spp.) are socially monogamous with biparental care of young and, hence, potential beneficiaries of mate‐guarding. We presented mated pairs of captive owl monkeys (A. nancymaae) with unfamiliar male and female conspecifics, to determine if either member of the pair exhibits intraspecific aggression toward an intruder or stays close to its mate, behaviors indicative of mate‐guarding. Male mates were more responsible for the maintenance of close proximity between mates than females. Male mates also exhibited elevated levels of behavior that signify arousal when presented with a male conspecific. These responses by mated male owl monkeys are consistent with patterns that may help prevent cuckoldry. Am. J. Primatol. 72:942–950, 2010. © 2010 Wiley‐Liss, Inc.     

Extra‐pair fertilizations contribute to selection on secondary male ornamentation in a socially monogamous passerine

Despite considerable research effort, it remains unclear whether extra‐pair fertilizations (EPF) drive the evolution of male secondary ornamentation in socially monogamous systems. In this study, we test the hypothesis that EPF contribute to the evolution or maintenance of male feather ornamentation in a sexually dichromatic passerine, the Scarlet Rosefinch, Carpodacus erythrinus. We show that the colouration of ornamental breast feathers is a good predictor of basic sources of variation in male annual reproductive output in rosefinches and that the annual realized reproductive success of males is positively associated with measures of ornamental colouration only when gains and losses because of EPF are considered. The results indicate that EPF in rosefinches may rely on absolute (good genes) rather than self referential (genetic complementarity) criteria of mate choice. Our study corroborates the potentially important role of EPF in the evolution and/or maintenance of elaborate male ornaments in socially monogamous taxa.     

Does competition for nests affect genetic monogamy in Cory's shearwater Calonectris diomedea?

Most bird species are socially monogamous. However, extra‐pair copulations (EPCs), resulting in extra‐pair paternity (EPP), commonly occur. EPCs should allow females to adjust social mate choice and allow males that fail to obtain a nest a chance to avoid missing a breeding season, especially when poor nest supply constrains social mate choice. Procellariiformes (albatrosses and petrels) are socially monogamous seabirds which seldom divorce, even when nest availability constrains social mate choice. In Cory's shearwater Calonectris diomedea, a burrow‐nesting petrel, two studies conducted in the Mediterranean, where competition for nests is weak, detected no EPP. EPP remains to be investigated at localities where competition for nests is much stronger, such as Vila islet, Azores archipelago, Atlantic Ocean. We conducted a genetic (microsatellites) study over two successive years on Vila, involving the breeding pairs of the same 65 nests each year and their single chick. EPPs occurred each year, the overall rate being 11.6%. Coupling genetic analyses to a 7‐year demographic survey provided additional data on pair bonds and competition for nests. Overall, cuckoldry was unrelated to divorce, nest density and inbreeding avoidance, but was more frequent when the social male was small. Nest changes were more costly for males than for females, and some apparently unpaired males attempted to dislodge social males during within‐pair copulations. These results are compatible with the existence of a link between poor nest availability and EPP and confirm that even species considered strongly monogamous can adopt flexible mating strategies.     

Female mate guarding: no evidence in a socially monogamous species

To understand the behavioural aspects of sperm competition, the costs and benefits to both sexes should be considered. However, few studies have addressed the costs to females of their social mate engaging in extrapair copulations (EPCs). Measures of female mate guarding have concentrated on female solicitation and copulation; however, females may also control access to their mate by maintaining close proximity, as is common in males. I recorded the maintenance of pair proximity behaviour of an urban population of the socially monogamous European blackbird, Turdus merula, over three breeding seasons. There was no evidence that females guarded their mates to prevent them from engaging in EPCs, nor were there any effects of the potential quality indicators of age, body size or male bill colour on the intensity of mate guarding between individuals. The study adds to a small body of literature suggesting that female mate guarding may be found in (facultatively) polygynous species, but not in socially monogamous ones. Copyright 2000 The Association for the Study of Animal Behaviour.     

Familiarity breeds success: pairs that meet earlier experience increased breeding performance in a wild bird population

In socially monogamous animals, including humans, pairs can meet and spend time together before they begin reproduction. However, the pre-breeding period has been challenging to study in natural populations, and thus remains largely unexplored. As such, our understanding of the benefits of mate familiarity is almost entirely limited to assessments of repeated breeding with a particular partner. Here, we used fine-scale tracking technology to gather 6 years of data on pre-breeding social associations of individually marked great tits in a wild population. We show that pairs which met earlier in the winter laid their eggs earlier in all years. Clutch size, number of hatched and fledged young, and hatching and fledging success were not influenced by parents'' meeting time directly, but indirectly: earlier laying pairs had larger clutches (that also produce higher number of young), and higher hatching and fledging success. We did not detect a direct influence of the length of the initial pairing period on future mating decisions (stay with a partner or divorce). These findings suggest a selective advantage for a new pair to start associating earlier (or for individuals to mate with those they have known for longer). We call for more studies to explore the generality of fitness effects of pair familiarity prior to first breeding, and to elucidate the mechanisms underlying these effects.     

Assessing the reproductive consequences of mate retention and pair bond duration in Thorn-tailed Rayadito (Aphrastura spinicauda), a short-lived,socially monogamous neotropical bird

The adaptive value of mate retention has been studied in several socially monogamous birds but evidence of reproductive benefits for short-lived species is inconclusive. Most studies come from northern latitudes but more research on tropical birds is needed, as these species typically show higher survival rates and longer pair bonds than those from temperate regions. We gathered data on the reproductive biology of a subtropical, isolated population of Thorn-tailed Rayadito Aphrastura spinicaudaduring 2008–2017 to evaluate the reproductive consequences of mate retention. We examined data from 243 breeding attempts made by 159 breeding pairs. We found that ~30% of all breeding pairs bred together during at least two consecutive years, and some were mated for 6 years. The main cause of pair dissolution was mate loss, not divorce. Mixed-effects models provided moderate evidence for positive effects of mate retention and successive remating on reproductive success. Newly formed pairs laid eggs later and had slightly smaller clutches than remated pairs. Furthermore, clutch size seemed to increase with successive remating. Overall, our results suggest that newly formed pairs are less efficient in reproduction and that minor yearly reproductive benefits of mate retention might accumulate for birds that are able to breed with the same partner over many years. Because breeding habitat is limited in our study population, Thorn-tailed Rayaditos could benefit from remating if the number of individuals that can breed exceeds the number of available breeding positions. Profitable long-term pair bonds might be more frequent in tropical birds and therefore more studies are needed to assess the prevalence of remating-mediated effects on reproduction in relatively short-lived monogamous species breeding in tropical regions.     

The logic of Ménage à Trois.

Recent studies of socially monogamous species have shown that in many cases females do not copulate exclusively with their pair mates, but are also receptive to other males. The explanation usually given for unfaithful female behavior is that most females are unable to bond with a male they would prefer as genetic father to their offspring. To secure male assistance the female therefore pairs with an available male but also copulates with males of supposedly higher genetic quality. Here we offer an alternative evolutionary explanation for female infidelity, which does not rely upon this ''Good Genes hypothesis of female choice. We show with a simple model that in an evolutionary game between three players, a male, a female and a male lover, solutions exist in which the female can secure more assistance from her mate by being receptive to other males. We conclude that female sexuality can have a decisive role in regulating social behaviour, in which the fertile female is the driving force.     

Promiscuity drives sexual selection in a socially monogamous bird

Many socially monogamous species paradoxically show signs of strong sexual selection, suggesting cryptic sources of sexual competition among males. Darwin argued that sexual selection could operate in monogamous systems if breeding sex ratios are biased or if some males attract highly fecund females. Alternatively, sexual selection might result from promiscuous copulations outside the pair bond, although several recent studies have cast doubt on this possibility, in particular by showing that variance in apparent male reproductive success (number of social young) differs little from variance in actual male reproductive success (number of young sired). Our results from a long-term study of the socially monogamous splendid fairy-wren (Malurus splendens) demonstrate that such comparisons are misleading and do not adequately assess the effects of extra-pair paternity (EPP). By partitioning the opportunity for selection and calculating Bateman gradients, we show that EPP has a strong effect on male annual and lifetime fitness, whereas other proposed mechanisms of sexual selection do not. Thus, EPP drives sexual selection in this, and possibly other, socially monogamous species.     

Red coloration of male northern cardinals correlates with mate quality and territory quality

I investigated how mate quality and territory quality influencean extravagant ornament in a socially monogamous species thatdefends multipurpose territories. Northern cardinals (Cardinaliscardinalis) are a highly dichromatic, socially monogamous species,and males are a brilliant red. I conducted a 3-year field studyof northern cardinals and found that redder males produced moreoffspring in a breeding season. Two selective factors mediatedthis fitness gain. Redder males were paired with earlier breedingfemales, an established measure of mate quality in birds. Second,redder males obtained territories of higher quality, as measuredby vegetation density. Interactions among these factors werealso important in explaining variance in male reproductive success.Multivariate analysis indicated that earlier breeding increasedreproductive success independent of territory quality. In turn,territory quality contributed to male reproductive success throughits effect on nest survival and possibly through its role in attractingan earlier breeding female.     

Hormonal correlates of development and natal dispersal in wild female owl monkeys (Aotus azarae) of Argentina

Pair-living and socially monogamous primates typically do not reproduce before dispersing. It is currently unclear whether this reproductive suppression is due to endocrine or behavioral mechanisms. Cooperatively breeding taxa, like callitrichids, may forego reproduction in natal groups because they reap inclusive fitness benefits and/or they are avoiding inbreeding. However, neither of these benefits of delayed reproduction appear to adequately explain the lack of reproduction prior to leaving the natal group in pair-living monogamous species. In this study, we determined whether wild Azara's owl monkeys (Aotus azarae) in the Argentinean Chaco establish reproductive maturity prior to dispersing. We utilized 635 fecal extracts to characterize reproductive hormone profiles of 11 wild juvenile and subadult females using enzyme immunoassays. Subadult females showed hormone profiles indicative of ovulatory cycling and had mean PdG and E1G concentrations approximately five times higher than juveniles. Contrary to expectations from the inbreeding avoidance hypothesis, female owl monkeys do not delay puberty, but rather commence ovarian cycling while residing in their natal group. Still, subadults appear to have a period during which they experience irregular, non-conceptive cycles prior to reproducing. Commencing these irregular cycles in the natal group may allow them to develop a state of suspended readiness, which could be essential to securing a mate, while avoiding costs of ranging solitarily. Our results indicate that reproductive suppression in female owl monkeys is not due to endocrine suppression. We suggest that adults likely use behavioral mechanisms to prevent subadults from reproducing with unrelated adult males in their natal group.     

Experimental evidence for a causal effect of pair-bond duration on reproductive performance in oystercatchers (Haematopus ostralegus)

Many studies have suggested that reproductive performance improvesduring the pair-bond, which might explain why individuals rematewith the same partner in many species. However, discussion existsabout whether the association between reproductive performanceand pair-bond duration that is reported in these studies reflectsa causal relationship. Usually it is unclear whether a positiveassociation is caused by pairs improving during their pair-bondor by high-quality pairs staying together for longer. Furthermore,reproductive performance often also depends on the age or breedingexperience of parents, which all covary with pair-bond duration.A much needed experimental approach is lacking so far. We investigatedthe effect of pair-bond duration on reproductive performancein a long-lived monogamous bird species based on natural aswell as experimental variation. The duration of oystercatcher(Haematopus ostralegus) pair-bonds, which were followed for21 years, strongly affected reproductive output, even aftercontrolling for effects of age and breeding experience. Pairsimproved during their pair-bond, and there were no indicationsof selective disappearance of low-quality pairs; however, pairsthat stayed together for very long performed badly. Experimentalremoval of one partner showed that the reproductive cost ofdivorce depended on the pair-bond duration with the old partner.In addition, after remating, the newly formed pairs stronglyimproved again, independent of the age and breeding experienceof the remated pair members. As such, this study provides thefirst experimental evidence of a causal effect of pair-bondduration on reproductive performance.     

Social monogamy in the cleaning goby Elacatinus evelynae: ecological constraints or net benefit?

We tested predictions from four hypotheses to explain the occurrence of long-term socially monogamous pairs in the Caribbean cleaning goby Elacatinus (=Gobiosoma) evelynae, namely (1) resource limitation, (2) low population and/or low mate density, (3) territorial defence and (4) net benefit of single-mate sequestration. We found no evidence that resources, in terms of available cleaning stations or clients to clean, were limited (1) or that after experimental goby removals, single individuals could not maintain cleaning stations alone (2). Population density was low but this did not prevent artificially widowed fish from remating quickly with individuals as large as their initial partners (3). Social monogamy in E. evelynae appears to result from the benefits associated with sequestering a large, high-quality mate (4). Both males and females showed intrasexual aggression towards experimental intruders consistent with mate guarding. Opportunities for polygynous matings by males, assessed by comparing the sizes, distances between and mating synchrony of neighbouring pairs, appeared both low and of limited value. Males therefore benefit most from guarding a larger, more fecund female. Females spent longer cleaning when paired with a large male, indicating that the benefits of guarding a high-quality mate may extend outside of the reproductive period for socially monogamous species. These results add to an increasing number of studies on coral reef fish showing mate-guarding behaviour and benefits to males and females from sequestering a single mate. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.