High frequency of social polygyny reveals little costs for females in a songbird

Mating system theory predicts that social polygyny—when one male forms pair bonds with two females—may evolve by female choice in species with biparental care. Females will accept a polygynous male if the benefit of mating with a male providing high-quality genes or rearing resources outweighs the cost of sharing mate assistance in parental care. Based on this rationale, we hypothesise that the population frequency of social polygyny (FSP) varies due to changes in mate sharing costs caused by changing environmental conditions. We predicted that: (1) polygamous females (i.e. mated with a polygynous male) pay a survival cost compared to monogamous females; (2) FSP would be higher in years with better rearing conditions and (3) the difference in survival rates between monogamous and polygamous females would be small following years with higher FSP. We tested these predictions using regression and multistate analyses of capture-recapture data of pied flycatchers, Ficedula hypoleuca, in central Spain collected over 26 years (1990–2016). Monogamous females had a higher mean survival rate than polygamous females (prediction 1), but there was no difference in survival between polygynous and monogamous males. In addition, FSP was positively associated with annual reproductive success (a proxy of the quality of rearing conditions—prediction 2). Finally, following years with high FSP, the survival of polygamous females was similar to that of monogamous females (prediction 3), while the chance of breeding in a polygamous state for 2 years in a row increased for both males and females. Our findings suggest that fluctuating environmental conditions may be a necessary but neglected aspect of understanding social polygyny mechanisms.

Sex differences in parental response to offspring begging are associated with pair bond strength across birds

Mothers, fathers, and offspring regularly clash over how much care offspring receive. Offspring beg to solicit for more resources--but how much begging is rewarded can depend on who is listening. While both parents benefit from provisioning offspring, each would benefit from their partner shouldering more of the burden of care, leading to sexual conflict. Additionally, if the costs and benefits of provisioning differ by sex, parent-offspring conflict should vary by sex. How these evolutionary conflicts influence sex differences in parent-offspring communication is unknown. To determine whether the sexes differ in their response to offspring signals, we conducted a meta-analysis on 30 bird species, comparing responsiveness to social and physiological traits affecting conflict. We found that a species' typical pair bond strength predicts whether males or females respond more to offspring begging. In species with stable and/or monogamous bonds, and thus lower sexual and paternal-offspring conflict, males' provisioning effort is more strongly correlated with offspring begging than females'. The opposite holds for species with weak pair bonds: females respond more to begging, perhaps compensating for males' lower responsiveness. These results demonstrate that sex differences in parental care can arise via sex differences in parent-offspring communication, driven by evolutionary conflicts.

Emergent intra-pair sex differences and behavioral coordination in pair bonded prairie voles

In pair bonding animals, coordinated behavior between partners is required for the pair to accomplish shared goals such as raising young. Despite this, experimental designs rarely assess the behavior of both partners within a bonded pair. Thus, we lack an understanding of the interdependent behavioral dynamics between partners that likely facilitate relationship success. To identify intra-pair behavioral correlates of pair bonding, we used socially monogamous prairie voles, a species in which females and males exhibit both overlapping and distinct pair bond behaviors. We tested both partners using social choice and non-choice tests at short- and long-term pairing timepoints. Females developed a preference for their partner more rapidly than males, with preference driven by different behaviors in each sex. Further, as bonds matured, intra-pair behavioral sex differences and coordinated behavior emerged – females consistently huddled more with their partner than males did, and partner huddle time became correlated between partners. When animals were allowed to freely interact with a partner or a novel in sequential free interaction tests, pairs spent more time interacting together than either animal did with a novel. Pair interaction was correlated with female, but not male, behavior. Via a social operant paradigm, we found that pair-bonded females, but not males, are more motivated to access and huddle with their partner than a novel vole. Together, our data indicate that as pair bonds mature, sex differences and coordinated behavior emerge, and that these intra-pair behavioral changes are likely organized and driven by the female animal.

The many functions of vocal learning

The capacity to learn novel vocalizations has evolved convergently in a wide range of species. Courtship songs of male birds or whales are often treated as prototypical examples, implying a sexually selected context for the evolution of this ability. However, functions of learned vocalizations in different species are far more diverse than courtship, spanning a range of socio-positive contexts from individual identification, social cohesion, or advertising pair bonds, as well as agonistic contexts such as territorial defence, deceptive alarm calling or luring prey. Here, we survey the diverse usages and proposed functions of learned novel signals, to build a framework for considering the evolution of vocal learning capacities that extends beyond sexual selection. For each function that can be identified for learned signals, we provide examples of species using unlearned signals to accomplish the same goals. We use such comparisons to generate hypotheses concerning when vocal learning is adaptive, given a particular suite of socio-ecological traits. Finally, we identify areas of uncertainty where improved understanding would allow us to better test these hypotheses. Considering the broad range of potential functions of vocal learning will yield a richer appreciation of its evolution than a narrow focus on a few prototypical species. This article is part of the theme issue ‘Vocal learning in animals and humans’.

Deceptive affection is strategically expressed under relational threat—but not towards partners with low mate value

Drawing on data from 1,993 participants, we demonstrated that deceptive affectionate messages (DAMs; e.g., faking sexual pleasure, expressing affection when feeling negatively) are the behavioral output of an evolved psychological system that strategically operates to maintain significant pair bonds (i.e., high mate value partners)—but not non-significant pair bonds (i.e., low mate value partners)—and regulates the expression of this behavioral output depending on an underlying cost-benefit ratio. This system is uniquely and nonrandomly designed to increasingly generate DAMs when the target individual’s highly-valued partnership is under relational threat and increasingly withdraw DAMs when the highly-valued partnership is not under threat—but neither increasingly generate nor withdraw DAMs for non-valuable partnerships—to maximize the benefits afforded by valuable romantic partnerships.

Medial amygdala ERα expression influences monogamous behaviour of male prairie voles in the field

Formation of long-term pair-bonds is a complex process, involving multiple neural circuits and is context- and experience-dependent. While laboratory studies using prairie voles have identified the involvement of several neural mechanisms, efforts to translate these findings into predictable field outcomes have been inconsistent at best. Here we test the hypothesis that inhibition of oestrogen receptor alpha (ERα) in the medial amygdala of male prairie voles would significantly increase the expression of social monogamy in the field. Prairie vole populations of equal sex ratio were established in outdoor enclosures with males bred for high levels of ERα expression and low levels of prosocial behaviour associated with social monogamy. Medial amygdala ERα expression was knocked down in half the males per population. Knockdown males displayed a greater degree of social monogamy in five of the eight behavioural indices assessed. This study demonstrates the robust nature of ERα in playing a critical role in the expression of male social monogamy in a field setting.

A Critical Look at Linus Pauling’s Influence on the Understanding of Chemical Bonding

The influence of Linus Pauling on the understanding of chemical bonding is critically examined. Pauling deserves credit for presenting a connection between the quantum theoretical description of chemical bonding and Gilbert Lewis’s classical bonding model of localized electron pair bonds for a wide range of chemistry. Using the concept of resonance that he introduced, he was able to present a consistent description of chemical bonding for molecules, metals, and ionic crystals which was used by many chemists and subsequently found its way into chemistry textbooks. However, his one-sided restriction to the valence bond method and his rejection of the molecular orbital approach hindered further development of chemical bonding theory for a while and his close association of the heuristic Lewis binding model with the quantum chemical VB approach led to misleading ideas until today.

Prolonged partner separation erodes nucleus accumbens transcriptional signatures of pair bonding in male prairie voles

The loss of a spouse is often cited as the most traumatic event in a person's life. However, for most people, the severity of grief and its maladaptive effects subside over time via an understudied adaptive process. Like humans, socially monogamous prairie voles (Microtus ochrogaster) form opposite-sex pair bonds, and upon partner separation, show behavioral and neuroendocrine stress phenotypes that diminish over time. Eventually, they can form a new bond, a key indicator of adapting to the loss of their partner. Thus, prairie voles provide an ethologically-relevant model for examining neuromolecular changes that emerge following partner separation for adapting to loss. Here, we test the hypothesis that extended partner separation diminishes pair bond-associated behaviors (partner preference and selective aggression) and causes pair bond transcriptional signatures to erode. Pairs were cohoused for 2 weeks and then either remained paired or were separated for 48hrs or 4wks before collecting fresh nucleus accumbens tissue for RNAseq. In a separate cohort, we assessed partner preference and selective aggression at these time points. Surprisingly, pair bond-associated behaviors persist despite prolonged separation and are similar between same-sex and opposite-sex paired voles. In contrast, we found that opposite-sex pair bonding, as compared with same-sex pairing, led to changes in accumbal transcription that were stably maintained as long as animals remained paired but eroded following prolonged partner separation. Eroded genes are primarily associated with gliogenesis and myelination, suggesting a previously undescribed role for glia in maintaining pair bonds and adapting to partner loss. We further reasoned that relevant neuronal transcriptional changes may have been masked by the prominent transcriptional signals associated with glia. Thus, we pioneered neuron-specific translating ribosomal affinity purification in voles. Neuronally-enriched transcriptional changes revealed dopaminergic-, mitochondrial-, and steroid hormone signaling-associated gene clusters whose expression patterns are sensitive to acute pair bond disruption and loss adaptation. Together, our results suggest that partner separation results in erosion of transcriptomic signatures of pair bonding despite core behavioral features of the bond remaining intact, revealing potential molecular processes central to priming a vole to be able to form a new bond.

Pair bonds during the annual cycle of a long-distance migrant, the Arctic Tern (Sterna paradisaea)

Background The extent to which pairs remain together during the annual cycle is a key question in the behavioural ecology of migratory birds. While a few species migrate and winter as family units, for most the extent to which breeding partners associate in the non-breeding season is unknown. The Arctic Tern (Sterna paradisaea) has one of the longest migrations of any species, and the aim of this study was to establish whether or not partners remain together after breeding. Methods Leg-mounted geolocators were fitted to breeding pairs of Arctic Terns nesting on the Farne Islands, Northumberland, UK. The devices were recovered for analysis the following year. Results Analysis of data for the six pairs which returned the following year showed that partners departed from the colony at different times after breeding and migrated independently to different Antarctic regions. Partners also departed from the Antarctic and turned to the breeding colony independently. One third of the pairs divorced on return. Conclusions For long-distance migrants reliant on unpredictable foraging opportunities, it may not be viable to remain as pairs away from the breeding colony. Synchrony in arrival times at the breeding colony may maximise the chance of retaining a familiar partner, but could be affected by environmental factors in wintering areas or along migration routes.

The Allomothering Hypothesis: an Examination of the Adaptiveness of Female Sexual Fluidity in Self Identified Heterosexual and Mostly Straight Women

Exclusive same-sex sexual behaviour is problematic from the viewpoint of evolutionary theory because one of evolutionary psychology’s fundamental tenets is that species need to survive and reproduce. I contend that female sexual fluidity is an evolved predisposition in heterosexual women and the behaviour evolved as a result of the need for allomothering— helping each other’s offspring survive—and also providing assistance with survival of the females themselves. The Allomothering hypothesis asserts that same-sex sexual behaviour can be adaptive in condition-dependent circumstances because it promotes pair bonds that ultimately contribute to the survival of offspring. A revised definition of sexual fluidity, one that is different from the traditional definition, was devised. In this dissertation the revised definition states “sexual fluidity occurs when self-identified heterosexual (straight) or predominantly heterosexual females experience short-term fleeting physical (sexual) attraction to and/or a deep emotional connection (like romantic love) with other females in a condition-dependent circumstance.” Four studies were conducted to find evidence in support of the allomothering hypothesis. The first study compared self-identified heterosexual (mostly straight) women and men in terms of same-sex sexual experience. Overall, women more than men have engaged in various dimensions of same-sex sexual behaviour. The second study compared pornography geared toward heterosexual women and pornography geared toward heterosexual men. Female same-sex sexual behaviour occurred in almost all the top selling movies for both heterosexual women and men. The third study tested the allomothering hypothesis by having self-identified heterosexual (mostly straight) women who have engaged in same-sex sexual behaviour rate the person they had the experience with on “good mothering traits.” The more the women enjoyed same-sex sexual behaviour, the higher they rated the person they had the sexual experience with. Various aspects of same-sex sexual behaviour among heterosexual (mostly straight) women and allomothering were explored. The final study was an assessment of captive Bonobos (Pan paniscus) at the Milwaukee Zoo. Bonobos are humans’ closest genetic relative along with Chimpanzees (Pan troglodtyes). The study examined the connection between female same-sex sexual activity among bonobos in relation to pair bonding, grooming, play, and allomothering.