• Pair bonding has been defined differently across animal taxa.
• We review these definitions as well as the occurrence of probable pair bonding behavior.
• We revise the definition of pair bonding, with an emphasis on affective components.
Abstract: Pair bonding is a psychological construct that we attempt to operationalize via behavioral and physiological measurements. Yet, pair bonding has been both defined differently in various taxonomic groups as well as used loosely to describe not just a psychological and affective phenomenon, but also a social structure or mating system (either social monogamy or just pair living). In this review, we ask the questions: What has been the historical definition of a pair bond? Has this definition differed across taxonomic groups? What behavioral evidence do we see of pair bonding in these groups? Does this observed evidence alter the definition of pair bonding? Does the observed neurobiology underlying these behaviors affect this definition as well? And finally, what are the upcoming directions in which the study of pair bonding needs to head?
3. Pair bonding across the animal kingdom
3.1. Invertebrates
Invertebrates account for 94% of identified animal species (Peterson, 2001). Due to the diversity of invertebrate species and said species' wide ranging sensory systems, defining a pair bond (or even pair living) in invertebrates can be challenging, and thus far few studies have tried. However, some observational work suggests that a few groups of invertebrate animals display behaviors potentially consistent with pair bonding. In many invertebrates, the relationship between mates involves some degree of proximal living or joint territoriality either to defend mates or to protect resources. In addition to proximal living, in some invertebrate species individuals preferentially live with another individual even outside of the reproductive period. Some invertebrates also display territorial behavior (Hultgren et al., 2017; Osaki and Kasuya, 2021), cooperative duty sharing (Hultgren et al., 2017), or biparental care (Osaki and Kasuya, 2021). These observations may potentially indicate that pair bonding exists in some invertebrate species.
A few key examples highlight the diversity of pair behavior shown in invertebrate taxa. Crustaceans show wide variation in social structure, but a large portion of species are pair living. Although pair-living snapping shrimp (Synalpheus spp.) do not exhibit parenting, they do perform sponge-cleaning duties cooperatively and participate in joint territorial sponge defense (Hultgren et al., 2017). Notably, Synalpheus species that are polygamous do participate in parental care. Another unique example of pair living arises in limpets (Schaefer et al., 2020). Limpets (Siphonaria gigas) are flexible in their living condition: even in the absence of territoriality, parental care, or mate-guarding, 75% of S. gigas live in pairs as opposed to living alone. Though S. gigas participate in extra-pair copulations, paired individuals primarily mate with each other and produce twice as many egg masses as single individuals, suggesting fitness benefits to pair living that are likely tied to limpets' reciprocally hermaphroditic mating (Schaefer et al., 2020).
At least one invertebrate species does show evidence of enduring preferential living encompassing more than a single reproduction. Wood-feeding cockroaches (Salganea taiwanensis) mate and live as pairs; quite notably, after choosing a mate, paired cockroaches chew off each other's wings (Osaki and Kasuya, 2021). After cannibalizing their pair mate's non-fleshy wings, paired individuals mate and produce multiple cycles of offspring that are cared for by both parents. Paired wood-feeding cockroaches mate with each other exclusively and for life (Osaki and Kasuya, 2021). The pairs appear to be more or less continuously reproducing (Maekawa et al., 2008), and thus it is not possible to study a post-pairing non-reproductive period in this species.
The majority of termite species display pair behavior in which one male (the king) and one female (the queen) are the sole breeders of their colony. Pair formation occurs when sexually mature individuals disperse from their natal colonies and participate in mass swarming events, during which male and female individuals form pairs, then set off in search of a suitable nest site (Hartke and Baer, 2011). Once the colony is formed, the male and female can remain together for years; termite kings are able to provide viable sperm to the queen for decades (Hartke and Baer, 2011). Often, colonies do not survive the death of their king and queen. Termites show biparental care in which both the king and queen care for young. In some species, queens provide more care for offspring than kings (Brossette et al., 2019), but in other species the division of labor is fairly equal and not sex-specific (Rosengaus and Traniello, 1991). Termites are aggressive to non-colony members (Nel, 1968), particularly reproductive individuals who could usurp the king or queen (Hartke and Baer, 2011). Termites and wood-feeding cockroaches therefore both represent species which are potentially pair bonding, but for which little data exists on affective components of the bond.
Very few studies have examined the underlying neurobiology and endocrinology of explicitly pair living and pair-bonded invertebrates. However, a few promising directions suggest conserved neuroendocrine systems may promote invertebrate pair bonds. The serotonergic (5-HT) system plays a critical role in sociality and evidence exists for the importance of 5-HT in many non-pair-bonding invertebrate species. Elevated levels of endogenous 5-HT predict the formation of larger leech groups (Bisson et al., 2012). Beyond 5-HT, oxytocin (OT)––along with its homologs––facilitates sociality across the animal kingdom (Lockard et al., 2017). For instance, nematodes (Garrison et al., 2012), leeches (Wagenaar et al., 2010), and snails (van Kesteren et al., 1995) all show OT-mediated mating behaviors; OT-homologs facilitate cuttlefish reproduction (Bardou et al., 2010) and oviposition in leeches (Fujino et al., 1999) and earthworms (Oumi et al., 1996). Thus, OT homologs could conceivably play a role in the pair behavior seen in the invertebrate species identified above. Future studies should aim to explore 5-HT and OT homologs as mediators of pair bonding and pair living in invertebrates.
3.2. Reptiles and amphibians
Reptiles and amphibians are socially diverse; however, there is limited work on pair bonds, which are uncommon in reptiles outside of the Egernia group of lizards (Whiting and While, 2017). As such, there is no clear definition of a pair bond in these classes of animals. Smith and Schuett (2015) propose that for a “pair association” to be identified, the association must persist for a quarter of the breeding season (Smith and Schuett, 2015). Time spent together outside of reproduction (i.e., spending “quality time” together) is a common feature in the definition of reptilian and amphibian “associations” (Botterill-James et al., 2017; Gillette et al., 2000; Martín et al., 2020). Some definitions require the presence of biparental care (Caldwell, 1997). In general, the study of these “associations” focuses on mating strategy rather than behavior, affect, or physiology of pairs. Nonetheless, there is some evidence that certain reptile and amphibian species may be considered pair bonding.
An example of a reptile that likely forms pair bonds is the Australian sleepy lizard (Tiliqua rugosa). Bonded pairs spend considerable time together before (and for some time after) mating, and pairs will search for one another if separated (Bull and Lindle, 2002; How and Bull, 2002; Leu et al., 2010). This cycle of reunion and pair living repeats each breeding cycle, and re-pairing with a different partner is rare (Bull, 1988), therefore the association is long lasting. The sleepy lizard's behavior matches that of other pair-bonding animals (e.g., prairie voles, zebra finches).
In amphibians there is very limited available evidence of a bonded relationship forming between partners, and when pair bonding is discussed it tends to be in the context of its relationship to biparental care (Brown et al., 2010; Caldwell and de Oliveira, 1999; Roland and O’Connell, 2015). The red-backed salamander (Plethodon cinereus) may be one of the few known cases. During the mating season, red-backed salamanders engage in mate guarding and prefer their partner over unfamiliar conspecifics (Gillette et al., 2000). These associations between pairs dampen outside of the mating season but do not entirely disappear, and associations lasting as long as three years have been observed (Gillette et al., 2000).
Poison frogs represent a group which includes both non-pair-bonding and potentially pair-bonding species (Roland and O’Connell, 2015). Behavioral and ecological differences were found between Dendrobates (later Ranitomeya) variabilis and D. imitator. Imitator was identified as engaging in biparental care and genetic monogamy (Brown et al., 2010); however, reproductive pairs only remained together for a single field season, with little or no interactions outside of mating and offspring care (Brown et al., 2008). These and other poison dart frog species (Caldwell, 1997) therefore may or may not meet a broader definition of pair bonding.
The neurobiology underlying the formation and maintenance of pair bonds has not been studied as extensively in reptiles and amphibians as it has in other classes of animals. However, one line of research has focused on chemosensory communication (e.g., sense of smell), a process that is not only vital for survival in reptiles and amphibians, but also for relationships. In social species of reptiles and amphibians, the chemosensory pathways that regulate self-recognition and recognition of friendly conspecifics (for example, a bonded partner) have been identified (Jaeger and Forester, 1993; Martín et al., 2020). Interestingly, male White's skinks (Liopholis whitii) will punish their female partners for extra-pair copulations, evidence of which can be detected through olfactory cues (Botterill-James et al., 2017). Despite extra-pair copulations, males will remain with their unfaithful partner and tolerate unrelated offspring on their territory. It is unknown if neural and hormonal systems underlying pair-bond formation and maintenance are similar between reptiles, amphibians, and other animals, but this is an area ripe for further research.
3.3. Fish
Pair bonding within the fish literature is defined as a selective, prosocial, and enduring affiliation between two conspecifics (Leese, 2012; Nowicki et al., 2020), with some definitions designating that affiliation must be maintained beyond reproduction (Fischer et al., 2019; Nowicki et al., 2018b). Other definitions indicate that pair bonding is simply the preferential interaction of individuals to the exclusion of other potential partners (Cardoso et al., 2015; O'Connor et al., 2016). Definitions vary concerning the length of the pair bond. Some pairs are considered pair-bonded if they remain together for a single reproductive period and do not include explicit considerations of subsequent breeding seasons, whereas in others, a pair bond persists across several breeding seasons, with or without parental care (Whiteman and Côté, 2004).
Shared parental care is also often included in definitions of pair bonding in fish (de Waal and Gavrilets, 2013), yet others assert that this phenomenon is not a requirement (Fischer et al., 2019). In fact, pair bonding has evolved in several coral reef fishes without biparental care (Nowicki, 2017; Reavis and Barlow, 1998), although some species do display shared parental care such as bass, some types of cichlids, and Murray cod (Avise et al., 2002; Couch et al., 2020; DeWoody et al., 2000; Garcia, 2019; Little, 2014; Reddon et al., 2015).
Pair bonds can be found in a variety of fish, including the convict cichlid (Amatitlania nigrofasciata), daffodil cichlid (Neolamprologus pulcher), Texas cichlid (Herichthys cyanoguttatus), Indo-Pacific cleaner wrasse (Labroides dimidiatus), Caribbean cleaning goby (Gobiosoma evelynae), pipefish (Syngnathinae), butterflyfishes (Chaetodontidae), and Murray cod (Maccullochella peelii) (Cardoso et al., 2015; Couch et al., 2020; Harding et al., 2003; Itzkowitz and Draud, 1992; Leese, 2012; Nowicki et al., 2018b). Moreover, within all vertebrate lineages, teleost (i.e., ray-finned) fishes display the second highest frequency of pair bonding, second only to birds (Nowicki, 2017).
Pair-bonded fish exhibit several affiliative behaviors. In cichlids, pair-bonded individuals display parallel swimming, tail beating, circling, greeting, and affiliative bites (Garcia, 2019; Reddon et al., 2015). Notably, in convict cichlids, color changes indicate pairing status. Females' abdomens change color from black or very dark gray to yellow/orange with some blue when they are courting or engaged in affiliative behaviors with males (Garcia, 2019). Studies with butterflyfishes also demonstrate the importance of visual signals for recognition, identification and location of mates, territorial defense, and as indicators of behavioral state (Hamilton and Peterman, 1971; Nowicki et al., 2018b; Tricas, 1989; Zumpe, 1965). Other behavioral manifestations of partner affiliation occur in the Australian seahorse (Hippocampus whitei) including coordinated motor displays and daily greetings—with these behaviors perhaps supporting pair-bond maintenance outside of the breeding season (Vincent and Sadler, 1995).
Despite some definitions that require pair-bonded individuals to be adult or opposite-sex, studies with coral reef butterflyfishes have suggested that pair bonding may occur within both sexually immature and same-sex partners (Gore, 1983; Nowicki et al., 2018b). However, in these studies, pair bonding or “pair formation” was defined by a fairly low level of association—for instance, in butterflyfishes, merely by remaining within 1 m for 10 min (Pratchett et al., 2006). Preliminary evidence also suggests that there are non-reproductive adaptive benefits of pair bonding like social assistance. For example, cooperative defense of high-value resources (e.g., food, shelter, or nesting sites) by one or both partners may be one such process (Nowicki et al., 2018b), but thus far the role of assisted resource defense in promoting pair bonding has received less attention relative to more common behaviors (i.e., mate guarding or biparental care).
Recent work by Nowicki et al. (2018b) comparing two species of butterflyfishes (C. baronessa and C. lunulatus) that exhibit alternative modes of assisted resource defense (male-prioritized vs. mutual defense, respectively) revealed that while assisted resource defense may drive pairing, males and females contribute equally to and benefit from resource defense. In both species, partner assistance appeared to confer gains in both feeding and energy reserves for pairs compared to solitary fish. Results from this study suggest that pair-bonded partners use territorial defense assistance to increase food and energy reserves. Furthermore, partner fidelity promotes territorial defense assistance between partners, which confers an ecological advantage to pair formation and fidelity in these species. However, the consequences of this advantage are unclear and future studies should seek to discern whether long-term pair bonding improves survivorship and lifetime fitness.
Similar to what has been observed in other pair-bonding vertebrates, elevated levels of species-specific homologs of arginine vasopressin (AVP) and OT are associated with pair bonding in fish (Cardoso et al., 2015; Cunha-Saraiva et al., 2019; O'Connor et al., 2016; Oldfield et al., 2015; Reddon et al., 2015; Shumway, 2010). OT levels have been demonstrated to rise in response to separation from partners in fish (Garcia, 2019). Studies examining the effects of manipulations of the OT and AVP systems have further demonstrated the role of these two neuropeptides in pair bonding, as blocking OT and AVP receptors prevents pair-bond formation in fish (Fischer et al., 2019; Nowicki, 2017; Oldfield and Hofmann, 2011). In addition to OT and AVP, dopamine (DA) receptors within the mesolimbic reward system appear to be important for pair bonding in fish (Fischer et al., 2019; Nowicki, 2017; Nowicki et al., 2020). Interestingly, it appears that neuromodulatory systems within the ventral striatal reward/reinforcement circuits such as AVP, OT, and DA have repeatedly contributed to the convergence of monogamy among vertebrates (Johnson and Young, 2018). In fish, AVP receptors within the lateral septum homologue (Nowicki et al., 2020) as well as OT receptors within the ventral telencephalon and amygdala/bed nucleus of the stria terminalis homologue (Nowicki et al., 2020) play an important role in pair bonding. It is also thought that the preoptic area, lateral septum, amygdala, hypothalamus, and periaqueductal gray are important for pair bonding in fish (Dewan and Tricas, 2011; Nowicki, 2017; Nowicki et al., 2020; O'Connell and Hofmann, 2011; Oldfield et al., 2015). Given the similarity in brain regions associated with pair bonding in fish and other pair-bonding vertebrates, it is possible that pair bonding may have partially converged between taxa through repeated co-option of molecular and anatomical homologies.
3.4. Birds
Monogamy is well studied as a social system in birds (Black, 1996a), and is represented in a large proportion of species, usually cited as 90% (Lack, 1968). However, distinctions exist in the literature between continuous partnerships, as opposed to “part-time” partnerships which do not continue during the non-breeding season (Black, 1996b). Therefore, some bird species which are classified as socially monogamous may not exhibit what we would define as a pair bond, based on these seasonal patterns of association. A number of other bird species do exhibit well-studied, continuous partnerships that include maintenance of association outside of the reproductive season and, while they may not have been experimentally studied in terms of pair bond behaviors, are likely to be pair bonding. Examples include blue ducks, Hymenolaimus malacorhynchos (Williams and McKinney, 1996); barnacle geese, Branta leucopus (Black et al., 1996); swans, genus Cygnus (Rees et al., 1996); jackdaws, Corvus monedula (Kubitza et al., 2015); and Pinyon and Florida scrub jays, Gymnorhinus cyanocephalus and Aphelocoma coerulescens (Marzluff et al., 1996). An interesting study of captive Caribbean flamingos (Phoenicopterus ruber ruber) found that some of the flamingos formed putative pair bonds, characterized mostly by continuous proximity, shared breeding and lack of courtship behaviors towards other animals (Shannon, 2000). Experimental evidence has also shown that greylag geese (Anser anser) show both a separation response and stress buffering (Wascher et al., 2012), although whether the separation response would be specific to the mate is unclear.
In avian species, a pair bond is often defined via behaviors such as higher proximity, allopreening, mate guarding, vocalizations, cohabitation, and courtship, all with a specific partner and over a long duration of time (Adkins-Regan, 1999; Kenny et al., 2017; Tomaszycki and Adkins-Regan, 2005). Compared to other organisms, birds are highly dependent on auditory communication and have physiological reactions to vocalizations, a process that plays major roles in pair bonds (Eriksson and Wallin, 1986; Mello et al., 1992; Tomaszycki and Adkins-Regan, 2005). Though multiple avian species have been identified as pair bonding, the model organism used by most researchers is the zebra finch (Taeniopygia guttata). Zebra finches have been studied in a wide range of paradigms that have both observationally and experimentally determined that they demonstrate strongly coordinated pair behavior and mate-guarding (Adkins-Regan, 2009), preference for the familiar partner (Smiley et al., 2012), and distress upon separation from the partner (Remage-Healey et al., 2003).
Some avian species demonstrate considerable behavioral flexibility in the pair bond. In bearded vultures (Gypaetus barbatus), it was found that in a more competitive environment for resources, the vultures engaged in less monogamous behaviors, instead forming a trio relationship (Carrete et al., 2006). There are also multiple avian species that engage in same-sex pair bonding. A four-year field study of Laysan albatross (Phoebastria immutabilis) in Hawaii demonstrated that 31% of nests identified were home to two pair-bonded females. The characterization of the pair bond was based upon a high frequency of mutual allopreening and mate guarding, and nearly half of the same-sex pair-bonded females remained together for the entire length of the study (Young et al., 2008). In addition, an experiment examining same-sex pair bonds in zebra finch found that same-sex pair-bonded males did not separate from their pair mate even when presented with a female (Tomaszycki and Zatirka, 2014).
Compared to most other groups, birds are highly dependent on auditory cues and communicate vocally. A complex network of taxon-dependent versions of DA, OT, and AVP seem to be involved in the formation and maintenance of pair bonds in avian species. OT receptor antagonists injected into the lateral ventricle of zebra finch disrupted pair-bonded behaviors in a sex-specific manner in both males and females (Klatt and Goodson, 2013). Disruption of AVP production in the paraventricular nucleus also disrupted social group interaction and affected aggression towards the opposite sex in a sex-specific manner (Kelly and Goodson, 2014). When monitoring DA levels in the brain using PET in zebra finches, researchers found that males experience an uptick of DA in response to female mating calls and demonstrate high motivation to work to hear the calls (Tokarev et al., 2017). In addition, injection of a D2 receptor antagonist decreased motivation to work to hear female mating calls (Tokarev et al., 2017). When looking for neurobiological maintenance mechanisms of pair bonding in zebra finches, researchers found increased levels of glucocorticoids (CORT) in pair-bonded mates upon separation from their mate and levels did not return to baseline until reunion (Remage-Healey et al., 2003). In a study investigating ZENK (a gene that is expressed with cell activation) and pair-mate reunion, researchers found an increase in ZENK expression of the nucleus taeniae in females once mates were reunited, indicating a potential neurobiological mechanism in maintenance of a pair bond (Svec et al., 2009).
3.5. Mammals
In class Mammalia, researchers have defined a pair bond in a variety of ways from simply “pair living” to more expansive and specific criteria. Beyond simply living together, a pair bond among mammals has been defined as an element of social structure in which an adult male and adult female form a close and long-lasting association (Kappeler and Van Schaik, 2002). In order Artiodactyla (even-toed ungulates), researchers have defined a pair bond as stable groupings of a single breeding male and female spanning more than one reproductive cycle (Norton, 1980; Tilson, 1980). Researchers of order Primates have considered the definition of a pair bond extensively. Fuentes (1998) defines a pair bond as “a special and exclusive relationship between an adult male and an adult female” (page 890). Anzenberger (1992) defines the pair bond even more explicitly, requiring that there are “indications of a strong mutual attraction, a close spatial relationship, partner specific behaviors and signs of distress during separation from the pair mate.” Fuentes (2002) theorizes that there are two essential components of the pair bond: the social and the sexual. The social component consists of a long-term relationship between opposite-sex, non-kin adults in which partners engage in affiliative and/or energy depleting behaviors that are unique to the pair—or at frequencies of affiliation that are unique to the pair—and maintain greater proximity to the pair mate relative to strangers or other members of the social group (Fuentes, 2002). The sexual component of the pair bond consists of a long-term relationship in which pair mates prefer to copulate with each other to the point of exclusivity, such that the pair demonstrates a monogamous mating pattern (Fuentes, 2002, Fuentes, 1998).
Newer definitions have built on these principles and added additional criteria such as endocrine responses to separation from and reunion with the pair mate in order to differentiate “dispersed pairs”—those pair-living primates with looser association and relationships—from “associated pairs”—those pair-living primates that demonstrate emotional attachments unique to their pair mate (Huck et al., 2020). There are several components that help characterize the emotional attachment an animal forms with their pair mate that have been adapted from research on mother-infant attachment, mainly: a strong and unique desire for proximity, distress upon separation, preference for the attachment figure, and ability of the attachment figure to alleviate or buffer stress (Ainsworth, 1978; Bowlby, 1982; Hazan and Shaver, 1987).
Behavioral components within mammalian pair bonds include affiliation, proximity maintenance, duration, and synchrony. Kleiman (1981) proposed that the strength of mammalian pair bonds could be quantified by several factors: 1) the amount of affiliation in which a pair engages, 2) the duration of pair-bond formation, 3) the degree of synchrony in daily activities between pair mates, and 4) the duration of the relationship. First, the ratio of affiliative behaviors to agonistic and avoidant behaviors––with higher rates of affiliation relative to aggression signaling stronger bonds and affiliative behaviors defined as behaviors that promote proximity between pair mates––can be used to capture variation in affiliation within a given species. These behaviors vary by species, but can include courtship and mating displays, vocal communication while engaging in independent activities, co-sleeping, huddling, and allogrooming. Second, weaker bonds are formed more quickly, are accompanied by more courtship, and are more easily disturbed than bonds that take relatively more time to form. Third, pairs that spend more of their day engaging in the same activities at the same time tend to be more strongly bonded than those who are more independent from their partner. And finally, pairs that associate for a longer duration (relative to species longevity and reproductive frequency), tend to form stronger bonds than pairs that associate for shorter durations.
Several mammalian species assumed to be socially monogamous and capable of forming pair bonds have later been shown to display sexual promiscuity or polygyny under different conditions (Adams et al., 2020; Cavallini, 1996; Pauw, 2000). As such, it can be difficult to decipher from the literature when animals labeled as socially monogamous exhibit intrapair interactions indicative of a pair bond. For example, the aardwolf hyena (Proteles cristata) was found to exhibit either polygynous or socially monogamous mating strategies depending on the study (Kotze et al., 2012; Marneweck et al., 2015). Other species appear fluid in their mating strategy, appearing promiscuous in some wild circumstances but monogamous in captivity (Cavallini, 1996; Kotze et al., 2012; Tardif et al., 2003). Among the wide range of mating strategies there remains a distinct question about the relationships between breeding pairs: can a species with flexible mating systems form pair bonds? And is it possible that some strictly monogamous species do not form pair bonds at all?
Mammalian groups that contain potentially pair-bonding species include Artiodactyla, Carnivora, Macroscelidea, Primates, and Rodentia. Within the order Carnivora, Lukas and Clutton-Brock (2013) classified 16% of species as monogamous, but among that 16%, very few species actually appear to form pair bonds (Lukas and Clutton-Brock, 2013). Among monogamous canids, breeding pairs appear to be capable of forming strong, long-term bonds. Several species of foxes have been observed living in bonded pairs sharing parenting duties, co-sleeping, foraging together, and maintaining proximity, even outside of mating season (Deuel et al., 2017; Macdonald and Courtenay, 1996; Wright et al., 2010). Similarly, bush dogs, raccoon dogs, and coyotes exhibit biparental care and territorial defense as well as scent marking behaviors to advertise their pair bond and ward off strangers (Drygala et al., 2008; Gese and Ruff, 1997; Porton, 1983; Schell, 2015). Pair-bonding behavior in pack-living canids is complicated by the hierarchical structure of the pack. Gray wolves live in packs with multiple adult males and females, but only the alpha animals form a pair bond, rear offspring, maintain proximity, and lead hunts (Ausband, 2019; Bernal-Stoopen and Packard, 1997; Peterson et al., 2002). Despite thorough documentation of canid behavior, very little is understood specifically about intrapair interactions and the neural mechanisms involved in canid pair bonding. Although data collection on many of these species is difficult due to their ecology, it remains valuable for future research to investigate the way sociality and pair bonding in canids, both behaviorally and neurobiologically, compares to other species.
Due to its clear expression of pair-bonding behaviors and suitability for laboratory research, the prairie vole (Microtus ochrogaster) has become the primary animal model for studying pair bonding. Prairie voles engage in a variety of affiliative and maintenance behaviors including huddling, grooming, mate preference, and mate guarding (DeVries et al., 1997). Research has also pinpointed specific biological and behavioral responses apparent in the prairie vole that resemble human pair bonds enough to stand out as a translational research model (Aragona and Wang, 2004). In addition to prairie voles there are many other rodent species that appear capable of forming pair bonds. For example, California mice (Peromyscus californicus) are biparental, live in pairs with their offspring, and express a variety of pair-maintenance behaviors. Paired male California mice will suppress ultrasonic vocalizations (typically emitted during mating behavior) in the presence of a strange female following administration of testosterone, while there was no such effect in unpaired males (Pultorak et al., 2015). Female California mice also form a clear preference for one mate over others and maintain this mate preference outside of estrous (Gubernick and Addington, 1994). Captive Cape porcupines (Hystrix africaeaustralis) engage in several pair-bonding behaviors such as allogrooming, scent marking, proximity maintenance, and copulation outside of the mating season (Morris and van Aarde, 1985; Sever and Mendelssohn, 1988). With the use of telemetry collars, Matsukawa and colleagues found evidence of pair bonding in wild long-tailed porcupines (Trichys fasciculata)––a biparental species that live in small social groups consisting of a single adult pair with their offspring––where the adult pair maintained their bond across multiple breeding seasons (Matsukawa et al., 2019). Behavioral and ecological factors have made it difficult to study many of the other monogamous rodent species.
Among order Artiodactyla, pair bonds are characterized by a single breeding pair of adults sharing and defending a mutual territory. Klipspringers (Oreotragus oreotragus) are defined as pair bonding on the basis that they hold a mutual territory, engage in pair maintenance through mutual scent marking (Burger, 1997; Dunbar and Dunbar, 1974), territorial defense (Dunbar and Dunbar, 1980), and joint vocal displays (Tilson and Norton, 2012). Additionally, klipspringers demonstrate behavioral synchrony and a high degree of proximity maintenance with their pair mates, as well as an intolerance of opposite-sex strangers (Dunbar and Dunbar, 1980; Norton, 1980). Dik-diks (Madoqua kirki) are often referred to as pair-bonded due to the fact that they are typically found in pairs and maintain close proximity in their daily life (Brotherton and Manser, 1997; Kranz, 1991). Male dik-diks are more territorial than their female counterparts: they engage in the majority of territorial scent marking (Kranz, 1991) and aggressively guard their mates during estrus (Brotherton et al., 1997). This is likely due to male mating strategy flexibility demonstrated by a willingness to engage in extra-pair copulations and even polygyny (Brotherton and Manser, 1997). Finally, reedbucks (Redunca arundinum) are sometimes referred to as pair-bonding because they live in single-male single-female pairs accompanied only by their sub-adult offspring (Junguis, 1970).
Within order Primates, researchers have proposed that behaviors that accompany a pair bond would include bond-reinforcing species-specific behavior like duetting, mutual displays, and partner contact behaviors (Anzenberger, 1988; French and Schaffner, 1999; Palombit, 1999) as well as behaviors that carry energetic costs like food sharing, grooming, and assistance in aggressive encounters (Fuentes, 2002). According to the strict definition of a primate pair bond by Fuentes (1998), only a few species of primates truly demonstrate pair bonds: genuses Callicebus and Plecturocebus (titi monkeys), genus Aotus (owl monkeys), Avahi laniger (the eastern woolly lemur), and Indri indri (indris). Titi monkeys (genus Callicebus and genus Plecturocebus) demonstrate behaviors consistent with pair bonding like mate guarding, vocal duets, joint territorial displays, affiliation rates unique to the pair mate, unique attachment to the pair mate, distress upon separation from the pair mate, and amelioration of distress upon reunion with the pair mate (Anzenberger, 1988; Fernandez-Duque et al., 1997; Mason, 1966; Mason and Mendoza, 1998). Gibbons (family: Hylobates) have been referred to as pair living and pair bonding and many species of gibbons do indeed demonstrate preferential pair-living and pair behavior (Cheyne, 2010; Choudhury, 1990), as well as territoriality enforced by vocal displays (Raemaekers and Raemaekers, 1984). However, there are documented cases of fluid sociosexual structure among adult gibbons, which tend to be influenced by resource availability (Savini et al., 2009), and a minority of gibbon species do not engage in coordinated vocalizations (Geissmann, 2002). By some definitions, these observations exclude those species from being considered truly pair bonding (Fuentes, 1998). There is also mixed information on whether sakis (genus: Pithecia) form pair bonds. While some studies found that sakis form preferential close relationships with their mating partners (Porter et al., 2015; Thompson, 2016), others debate whether sakis exhibit enough of the essential pair-bonding behaviors (e.g. mate guarding and maintained interaction beyond one interbirth interval), to be considered a pair-bonding species (Porter et al., 2015; Thompson, 2016; Thompson and Norconk, 2011). Some species of lemurs have also been proposed as pair bonding. Red-bellied lemurs (Eulemur rubriventer) exhibit several intrapair behaviors that indicate the possibility of a pair bond: territorial defense, pair-specific vocalizations, and pair-specific behaviors (Grebe et al., 2021; Tecot et al., 2016).
Years of neurobiological research in prairie voles have revealed a critical role of OT and AVP systems in the formation and maintenance of mammalian pair bonds (see Walum and Young, 2018 for a detailed review). The specific distribution of OT and AVP receptors significantly differ between closely related vole species depending on whether or not they are socially monogamous. Further pharmacological manipulations of OT and AVP, as well as DA and opioids, revealed detailed neural circuits dedicated to the social process of pair bonding (Chappell et al., 2016; Lim et al., 2004; Liu et al., 2001; Liu and Wang, 2003; Resendez et al., 2012). Research in nonhuman primates has expanded our understanding of these neural circuits. Relationship formation in titi monkeys is supported by the dopaminergic reward system, specifically D1 receptors in the lateral septum (Hostetler et al., 2017) and increased activity (measured by glucose uptake) in the nucleus accumbens and ventral pallidum (Bales et al., 2007; Maninger et al., 2017a). Relationship maintenance in titi monkeys is supported by brain areas involved in motivation like the nucleus accumbens, ventral pallidum, caudate, and putamen as well as by areas involved in emotion, reproduction, and social memory like the medial preoptic area, amygdala, lateral septum, and posterior cingulate cortex (Bales et al., 2017, Bales et al., 2007; Maninger et al., 2017b). D1 receptors also play a role in pair-bond maintenance as regulators of mate guarding behaviors, suggesting that the dopaminergic reward system plays an important role in the agonistic components of pair-bond maintenance (Rothwell et al., 2019).
Despite the evidence for some commonalities in the neurobiology of pair bonding across mammal species, primate studies suggest that we still do not fully understand neural mechanisms for pair bonding. A recent study in monogamous and non-monogamous Eulemur species (Grebe et al., 2021) examined the distribution of AVP and OT receptors in the brains of two monogamous and five non-monogamous lemur species. Surprisingly, the differences between OT and AVP receptor distributions in monogamous and non-monogamous lemurs were minimal, even in dopaminergic areas. This finding was unexpected, given the striking differences found between monogamous and non-monogamous voles (Insel and Shapiro, 1992) and between monogamous titi monkeys vs. non-monogamous rhesus monkeys (Freeman and Young, 2016). These findings suggest that there could be distinctive mechanisms underlying pair bonding in lemurs, or that lemurs might not really form pair bonds.
The lemur study and its deviation from expected patterns suggests that it is likely that the presence of some combination of molecular mechanisms out of a larger suite may better predict whether a species will form an emotional pair bond or not. This idea of a “redundant systems model” was previously proposed to explain how all behavioral aspects of pair bonding are not reliably expressed by all pair-bonding species (Mendoza et al., 2002). It is possible that a combination of the activity of certain molecular mechanisms, such as OT, AVP, DA, and CORT, play some role in the expression of pair bonding; however, these mechanisms and their sites of action may differ based on how pair bonding evolved in that species. In our quest to understand the evolution of pair bonding, we must also continually return to our behavioral definitions to understand whether we are all talking about the same phenomenon.
3.6. Humans
Definitions of human pair bonding typically include proximity or cohabitation, relative stability over time, and a strong affective attachment to the partner (Fernandez-Duque et al., 2020; Fletcher et al., 2015; Quinlan, 2008). The behavioral expression of pair bonding in humans has many common elements with the behaviors observed in other pair-bonding species, as well as many unique elements. As in other species, human pair bonds typically follow a normative developmental course, including initiation, maintenance, and occasionally dissolution (Clark et al., 2018; Eastwick et al., 2019; Rusbult et al., 2004). Human pair bonds are also studied in the context of romantic love, a construct characterized by compassion, intimacy, and caregiving (for a discussion of the robustness of this three-factor structure, see Fletcher et al., 2015). However, the term “romantic love” has been used somewhat inconsistently across the fields of social and evolutionary psychology, with some using the term “romantic love” as an equivalent to “pair bonding” (Carter and Perkeybile, 2018), and others describing “romantic love” as a separate process that is related to human pair bonding and has potential parallels in other animal species (Diamond, 2003). In this article, we consider romantic love and pair bonding as related and largely overlapping constructs.
Given the human capacity for language, human pair mates sometimes express romantic affection verbally, sometimes through song, poetry, or music. Humans also show cognitive bias, and in committed pair bonds, pair mates tend to hold positive illusions about their partner (Clark et al., 2018; Lemay and Clark, 2015). There is also large variation between (and within) cultural groups in how humans form and express pair bonds (Eastwick, 2013; Quinlan, 2008). Moreover, humans are the only species in which monogamous pair bonding is imbedded within complex, multi-level male/female groups (Chapais, 2013). Although it could be argued that some of these elements of human pair bonding exist to some degree in other animal species, in most cases it is impossible to know, given that animal pair bonding can only be assessed through behavior and physiology.
There has been much debate on the evolutionary origins and timing of human pair bonding and social structure. There are two primary competing hypotheses: either (1) human pair bonding evolved to support the large investment needed to rear offspring, or (2) human pair bonding evolved because it was too costly for males to have multiple mates (Chapais, 2013; Fletcher et al., 2015; Quinlan, 2008; Stanyon and Bigoni, 2014). Many pressures may have selected for human pair bonding, including sex ratios, the spatial distribution of females, innovation of hunting and cooking technologies, alloparenting, life history (i.e., slow maturation of offspring), male-female division of labor (i.e., paternal provisioning), and shortened inter-birth intervals (although note, in some cases, pair bonding may have evolved first or concurrently) (Quinlan, 2008; Quinlan and Quinlan, 2008). Regardless of how pair bonding evolved, it is generally agreed that, in humans, it evolved after maternal care (common to all mammals), but before paternal (i.e., biparental) care (Chapais, 2013; Diamond, 2004). This could potentially explain why the neural processes that support mother-infant bonding (particularly those involving DA and OT) overlap with those that support romantic-partner bonding (Diamond, 2004; Feldman, 2017; Ortigue et al., 2010). Further, Chapais (2013) argued that human pair bonding first evolved in a polygamous context, and that monogamy evolved after pair bonding. If this is true, it raises important questions about whether exclusivity should be included in the definition of “pair bonding” in humans (and other species), or whether multiple pair bonds can be maintained at a time (Fletcher et al., 2015).
Human pair bonding is supported by various brain regions and neurotransmitters, many of which are implicated across other pair bonding species. For examples, a large body of comparative research suggests that across humans (Feldman, 2017), non-human primates (Bales et al., 2017), and many other species (Fischer et al., 2019) pair bonding is supported by systems including DA,OT, and AVP in the hypothalamus, ventral tegmental area, nucleus accumbens, and the globus pallidum, as well as other limbic and cortical regions (Feldman, 2017; Fischer et al., 2019). However, in humans there may be an increased role for the cortex (see Feldman, 2017), a brain region that is greatly expanded in humans compared to other species and that likely enables many human-specific cognitive and emotional processes (Teffer and Semendeferi, 2012). For example, in humans, many regions in the prefrontal cortex, cingulate cortex, and insula project to the mid-brain pair-bonding circuitry (Bartels and Zeki, 2000; Feldman, 2017; Marsh, 2018). These neural processes likely enable a vast suite of cognitive abilities that allow partners to evaluate and interpret each other's thoughts, feelings, intentions, goals, emotions, and character (Fletcher et al., 2015), manifest in both behavior and language.
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