A game of thrones: Neural plasticity in mammalian social hierarchies
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SOCIAL NEUROSCIENCE, 2014
Vol. 9, No. 2, 108–117, http://dx.doi.org/10.1080/17470919.2014.882862
A game of thrones: Neural plasticity in mammalian social
hierarchies
Skyler J. Mooney, Diana E. Peragine, Georgia A. Hathaway, and Melissa M. Holmes
Department of Psychology, University of Toronto Mississauga, Mississauga ON, Canada L5L 1C6
Social status is a key regulator of health and reproduction in mammals, including humans. Despite this, relatively
little is known about how social status influences the mammalian brain. Furthermore, the extent to which status is
an independent construct, i.e., not simply acting as a psychosocial stressor, is yet to be determined. Research to
date reveals several promising mechanisms and/or systems associated with social status, including monoamine
systems, hypothalamic neuroendocrine axes, and the hippocampus, though whether these differences are the cause
or effect of status is often unclear. We review these candidates and propose how best to approach this research
question in the future.
Keywords: Dominance; Neurogenesis; Plasticity; Social defeat; Social status.
Animals living in groups rarely form a truly egali- and, in turn, how status influences the brain is parti-
tarian society. Rather, individuals have differing sta- cularly challenging, given the diversity and variabil-
tus or rank with the group. This translates to varying ity of social hierarchies seen across species. For
access to resources where dominant individuals with example, the canonical view in behavioral neu-
high status have preferential access over individuals roscience is that it is stressful to be socially subor-
of low status, though the resources in question vary dinate. Thus, low social rank is a psychosocial
across species (e.g., mates versus food versus terri- stressor, translating to physiological stress (e.g., ele-
tories, etc.). These social hierarchies can be rigid vated glucocorticoid levels) in subordinate animals.
and stable or remarkably fluid, also depending on While this is often true in circumstances with large
species and context. Import antly, social status resource inequality or with winner/loser paradigms,
affects physiological and behavioral function in it is not the case for many naturally occurring hier-
diverse mammals, including humans, with some- archies such as those seen in wolves, lemurs, mar-
times profound effects on direct reproductive fitness mosets, and macaques (reviewed in Creel (2001)). In
and overall health. addition to affecting stress physiology by influen-
While great strides have been made in under- cing the function of the hypothalamic–pituitary–
standing the hormonal and behavioral correlates of adrenal (HPA) axis, social status also directly regu-
social status in mammals (e.g., alterations in stress lates reproduction. In many species, subordinates
and reproductive function), much less is known exhibit dampened activity of the hypothalamic–
about how the central nervous system differs pituitary–gonadal (HPG) axis, resulting in lower
between dominant and subordinate animals. levels of circulating gonadal steroid hormones
Understanding how the brain controls social status (e.g., testosterone) than their dominant counterparts
Correspondence should be addressed to: Melissa M. Holmes, Department of Psychology, University of Toronto Mississauga, Mississauga
ON, Canada L5L 1C6. E-mail: melissa.holmes@utoronto.ca
S.J. Mooney and D.E. Peragine have contributed equally to this manuscript.
This work was funded by a NSERC Discovery Grant to MMH, Ontario Graduate Scholarships to SJM and DEP, and a NSERC CGS award
to GAH.
© 2014 Taylor & FrancisSOCIAL STATUS AND NEURAL PLASTICITY 109
(e.g., Carlson et al., 2004; Creel, Creel, Mills, & dominance relationship is established (Filipenko,
Monfort, 1997; Holmes, Goldman, Goldman, Alekseyenko, Beilina, Kamynina, & Kudryavtseva,
Seney, & Forger, 2009). 2001; Filipenko, Beilina, Alekseyenko, Dolgov, &
Here, we explore what is really known about Kudryavtseva, 2002a, 2002b). In the food competition
how status affects the mammalian brain and attempt paradigm, social hierarchies are established by com-
to tease apart direct effects of status from poten- petition for a limited food supply, in either a single
tially indirect effects of stress and/or reproduction. food hole (Hoshaw, Evans, Mueller, Valentino, &
Are these distinctions even important? We believe Lucki, 2006) or worker–parasite context (Dhingra,
the answer is an unequivocal “yes”. If we are to Raju, & Meti, 1997). Despite their popularity, these
truly understand the “social brain”, we need to paradigms often fail to mirror the natural ecology of
know how the brain navigates and responds to the the species and consistently result in increased stress
social hierarchies that shape an organism’s day-to- in the loser or subordinate, as indicated by circulating
day life. However, there is a striking paucity of this glucocorticoids (e.g., Berton et al., 1998; Keeney
specific issue in the mammalian literature. Status et al., 2006; Marini et al., 2006; Mitra, Sundlass,
and psychosocial stressor are often used as syno- Parker, Schatzberg, & Lyons, 2006). Furthermore,
nyms, and this is simply inaccurate in many cases. much of this work does not directly compare subordi-
Similarly and relatedly, dominance and aggression nate and dominant animals and, instead, compares
are often used interchangeably and that is also often subordinates/losers to unmanipulated controls. Thus,
incorrect. The relationships between status, stress, the social defeat approach is actually studying psy-
and aggression are highly species-specific and con- chosocial stress and not social status per se.
text-dependent. Based on the current status of the Unfortunately, this distinction is sometimes lost
field, we are certainly not in a position to make any when interpreting results. Interpretation is further
sweeping generalizations about how status affects complicated by differences in the paradigms them-
the brain. Nor are we exhaustively reviewing every selves, control groups (e.g., single- vs. social-housed),
paper that suggests status-induced plasticity. length of social exposure, etc., that make it difficult to
Instead, our goal for this Short Review is to know if effects are due to some other variable (e.g.,
highlight the importance of this research environmental complexity). As such, we caution how
question and shed light on how best to tackle it in these studies are interpreted in the context of social
the future. status and categorize them as “indirect” evidence.
Social defeat is accompanied by a depressive-like
behavioral profile. Therefore, much of the work
INDIRECT EVIDENCE FOR STATUS investigating associated neural plasticity has focused
EFFECTS ON NEURAL PLASTICITY on monoamine systems. For example, serotonin (5-
HT) 1a receptor numbers and responsivity are
The majority of work investigating social status in decreased in subordinate rats and tree shrews
traditional laboratory rodents focuses on social defeat, (Berton et al., 1998; Flügge, 1995; Flügge, Kramer,
including resident–intruder, winner–loser, and food Rensing, & Fuchs, 1998; but see Berton et al.
competition paradigms. In the resident–intruder (1999)). Interestingly, pharmacological manipulation
model, a resident/dominant animal selected for size, of these receptors affects the submissiveness of
aggression, and/or prior winning experience is rodents and primates during experimental models of
exposed in its home territory to an unfamiliar animal, social stress (Cooper, McIntyre, & Huhman, 2008;
prompting attack and defeat of the intruder/subordi- Raleigh, McGuire, Brammer, Pollack, & Yuwiler,
nate (Berton, Aguerre, Sarrieau, Mormede, & 1991), suggesting a possible bidirectional role.
Chaouloff, 1998, 1999; Gardner, Thrivikraman, Social defeat has numerous other effects on this sys-
Lightman, Plotsky, & Lowry, 2005; Paul et al., tem, such as increases in the activation of serotoner-
2011). This most popular and widely applied defeat gic neurons (Gardner et al., 2005; Paul et al., 2011),
paradigm is also the most artificial, with dominance serotonin transporter activity (Filipenko et al., 2002a,
contests “rigged” by the size, experience, and territori- 2002b; Zhang et al., 2012) and 5-HT2a receptor bind-
ality of the resident. By contrast, winner–loser and ing (Berton et al., 1998). These effects extend to the
food competition paradigms pit “matched” individuals dopaminergic system where defeat decreases dopa-
against one another. In the winner–loser model, two mine transporter binding in the brains of mice, rats,
mice share a sensory contact cage, with the partition and tree shrews (Filipenko et al., 2001; Isovich,
lifted daily to allow regular dominance bouts. After Engelmann, Landgraf, & Fuchs, 2001; Isovich,
repeated encounters, a victor emerges, and a clear Mijnster, Flügge, & Fuchs, 2000).110 MOONEY ET AL.
Given its robust effects on circulating glucocorti- Fuchs & Flügge, 2002; Gould et al., 1997; Isovich
coids, it is not surprising that varying periods of social et al., 2000; Thomas et al., 2007), it can be difficult to
defeat or subordination also alter corticotropin- determine direction of causality. For example, in
releasing factor receptor expression in the brains of female bonnet macaque (Macaca radiata) groups,
mice, rats, and tree shrews (Fekete et al., 2009; Fuchs stress-induced decreases in dominance rank are corre-
& Flügge, 1995; Funk, Li, & Le, 2006; Keeney et al., lated with decreased hippocampal neurogenesis
2006; Kozicz, Bordewin, Czéh, Fuchs, & Roubos, (Perera et al., 2011). Fluoxetine, a selective serotonin
2008; Marini et al., 2006; Panksepp, Burgdorf, reuptake inhibitor, reverses the effects on rank but not
Beinfeld, Kroes, & Moskal, 2007; Reber et al., if animals are irradiated, suggesting that neurogenesis
2007). This is coupled with both short- and long- is necessary for maintaining dominance (Perera et al.,
term changes in α 2-adrenoceptor, glucocorticoid 2011). However, this pattern is also seen with depres-
receptor and mineralocorticoid receptor expression sion-scores instead of dominance rank, thus we cannot
(Buwalda et al., 2001; Flügge, 1996; Flügge, Jöhren, conclude whether it is social rank or depressive beha-
& Fuchs, 1992; Jöhren, Flügge, & Fuchs, 1994; vior that is directly related to changes in neurogenesis.
Marini et al., 2006; Sutanto et al., 1992). These altera-
tions in stress physiology appear to trigger morpholo-
gical and functional plasticity in the hippocampus. DIRECT EVIDENCE FOR STATUS
Repeated social defeat and/or subordination results EFFECTS ON NEURAL PLASTICITY?
in morphological blunting of the apical dendrite in
hippocampal pyramidal neurons of rats and tree A more direct approach for studying social status
shrews, with corresponding effects on cell excitability effects on the brain is the study of longer-term, natural
(Kole, Costoli, Koolhaas, & Fuchs, 2004; Magariños, hierarchies that are formed by colonial or highly
McEwen, Flügge, & Fuchs, 1996). Acute and chronic social species. Colony housing and caging that more
defeat and/or subordination inhibits both cell prolif- closely approximate the natural habitat of an animal,
eration and survival in the hippocampus of mice, rats, such as the visible burrow system (VBS) in laboratory
tree shrews, and monkeys, although effects vary con- rodents (see Blanchard et al. (1995) for review), may
siderably across experiments (Czéh et al., 2001, 2002, offer insights into the effects of status that are due to
2006; Ferragud et al., 2010; Gould, McEwen, multiple elements of the animal’s natural social
Tanapat, Galea, & Fuchs, 1997; Gould, Tanapat, ecology.
McEwen, Flügge, & Fuchs, 1998; Hoshaw et al., At first glance, rodents housed in the VBS appear
2006; Mitra et al., 2006; Thomas, Hotsenpiller, & to exhibit similar changes in the serotonergic and
Peterson, 2007; Van Bokhoven et al., 2011; Yap dopaminergic systems compared to rodents in social
et al., 2006). Decreases in cell proliferation and survi- defeat paradigms. For example, mice in the VBS have
val are associated with a decrease in hippocampal reduced 5-HT1a receptor (McKittrick, Blanchard,
volume (Czéh et al., 2001; Lucassen et al., 2001; Blanchard, McEwen, & Sakai, 1995) and serotonin
Ohl, Michaelis, Vollmann-Honsdorf, Kirschbaum, & transporter (McKittrick et al., 2000) binding.
Fuchs, 2000) that is mimicked with cortisol treatment However, this is true for both dominants and subordi-
(Ohl et al., 2000), suggesting that defeat-induced nates compared to controls, suggesting that the
effects on the hippocampus are directly due to stress. decreased 5-HT1a binding in social defeat paradigms
While stress-induced structural changes also occur in is due to stress and not status. Similarly, subordinate
the medial prefrontal cortex (mPFC), plasticity related mice in the VBS have increased 5-HT2 receptor bind-
to defeat and the acquisition of subordinate behavior ing; dominants exhibited the same pattern though it
does not appear to occur in this region (Markham, failed to reach statistical significance (McKittrick
Luckett, & Huhman, 2012). Instead, defeat-induced et al., 1995). As with social defeat, subordinate rats
changes within the mPFC manifest at a functional in the VBS show decreased dopamine transporter
level, with mPFC inactivation enhancing, and stimu- binding but only compared to controls, not dominants
lation impairing the acquisition of conditioned defeat (Lucas et al., 2004). This pattern is also seen with D2
(Markham et al., 2012). Correspondingly, subordinate receptor binding (Lucas et al., 2004).
mice have lower excitatory synaptic strength in mPFC Albeit still indirect, the best evidence for social
pyramidal cells than dominants, and dominance beha- status regulating the serotonergic system comes from
vior can, in turn, be altered by modulating synaptic rhesus monkeys (Macaca mulatta) living in natural
strength in this region (Wang et al., 2011). matrilineal hierarchies where subordinate females
Precisely because social defeat is associated with a show increased binding of both the 5-HT1a receptor
depressive-like behavioral profile (Flügge et al., 1998; in the hypothalamus and of the serotonin transporterSOCIAL STATUS AND NEURAL PLASTICITY 111 in the orbital prefrontal cortex relative to dominant for sex might prove difficult because the formation of females (Embree et al., 2013). For the dopaminergic stable hierarchies appears to be sex-specific in certain system, dominant animals show increased D2 receptor species (Tamashiro et al., 2004). However, when sex availability and subordinates show decreased dopa- comparisons can be made, valid status-specific effects mine transporter availability in cynomolgus monkeys are more likely to be detected. (Macaca fascicularis) (Morgan et al., 2002; Nader In our lab, we use the naked mole-rat et al., 2012). (Heterocephalus glaber) to study the effects of social Importantly, social status in more natural para- status on brain plasticity. These eusocial rodents exhi- digms also triggers changes in the HPA axis as well bit the strictest reproductive and social hierarchies as hippocampal plasticity. For example, subordinate among mammals: breeding is restricted to a single mice in the VBS show enhanced CRF mRNA relative dominant female, called the queen, and her 1–3 male to controls in areas that mediate fear/anxiety responses consorts in colonies that can include hundreds of such as the central amygdala (Albeck et al., 1997) and subordinate animals. We have found that social status the oval nucleus of the bed nucleus of the stria termi- is more important than sex for determining morphol- nalis (BNST) (Choi et al., 2006), and reduced hippo- ogy of several reproductively relevant brain regions campal glucocorticoid and mineralocorticoid receptor where breeders have larger volumes of the paraven- mRNA (Chao, Blanchard, Blanchard, McEwen, & tricular nucleus (PVN), BNST, and medial amygdala Sakai, 1993). However, while these effects are not (MeA) than subordinates (Holmes, Seney, Goldman, significant in dominant animals, the pattern is often & Forger, 2011; Holmes et al., 2007). Furthermore, similar, again suggesting a role for stress and not subordinates have a higher percentage of androgen social status. Indeed, as in social defeat, both domi- receptor-immunoreactive neurons throughout the nant and subordinate animals housed in the VBS social decision making network (Holmes, Goldman, show reductions in apical dendritic arborization within & Forger, 2008; Holmes et al., 2013) and increased the hippocampus (McKittrick et al., 2000). Therefore, numbers of oxytocin-immunoreactive neurons in the the best example of a stress-independent effect of PVN (Mooney & Holmes, 2013). However, several social status on the hippocampus is the increased variables differ between dominant and subordinate survival of newborn neurons in dominant rats in the naked mole-rats including age (breeders are almost VBS compared to subordinates despite no status dif- always the oldest animals in the colony), stress, gona- ferences in glucocorticoids (Kozorovitskiy & Gould, dal steroid hormones, and behavioral profile. While 2004). However, in this case, we need to be concerned age does not appear to be a key player when included about reproduction-induced effects. The VBS is a as a statistical variable, our efforts to tease apart the mixed-sex environment, permitting dominant males effects of stress and reproduction have yielded inter- to have reproductive experience during the experi- esting results. By removing subordinates from their mental paradigm and, indeed, both sexual experience colony and controlling their reproductive activity (via and circulating testosterone can increase neurogenesis gonadal manipulation and/or opposite- versus same- in adult male rats (Leuner, Glasper, & Gould, 2010; sex partner housing), we can begin to identify the Spritzer & Galea, 2007). social and endocrine cues associated with transitions This highlights another important point, which is in social status. For example, removing subordinates that sex differences and social status have not been from the colony—a release from subordination—is sufficiently explored. Social defeat paradigms are sufficient to trigger plasticity in the PVN (Holmes almost entirely male-biased, and females are typically et al., 2011; Mooney & Holmes, 2013), but not the included in the VBS only as stimuli to facilitate hier- BNST or MeA, suggesting regional specificity for the archies in experimental males (Albeck et al., 1997; underlying mechanisms. Thus far, a role for gonadal Chao et al., 1993; Choi et al., 2006; Kozorovitskiy & steroid hormones seems limited given that dominant Gould, 2004; Lucas et al., 2004; McKittrick et al., animals maintain their status and associated neural 1995, 2000). When females are examined, some morphology following gonadectomy (Goldman, social-rank correlates such as D2 receptor availability Forger, & Goldman, 2006; Holmes et al., 2011) and appear similar in both sexes (Morgan et al., 2002; that gonads are not required for the transition to a Nader et al., 2012). However, if we consider that breeder-like number of oxytocinergic neurons 5-HT1a binding in subordinate female monkeys (Mooney & Holmes, 2013). (Embree et al., 2013) differs from that of subordinate We are also beginning to uncover how social status male rats and tree shrews (Berton et al., 1998; Flügge, affects neurogenesis in naked mole-rats. We find that 1995; Flügge et al., 1998), it is difficult to tease apart breeders have reduced doublecortin-immunoreactive the effects of species, paradigm, and sex. Accounting cells in the dentate gyrus, piriform cortex, and
112 MOONEY ET AL.
basolateral amygdala, compared to subordinates, and activation of the dorsolateral prefrontal cortex, occipi-
these effects are more pronounced in females tal/parietal cortex, ventral striatum, and parahippo-
(Peragine, Simpson, Mooney, & Holmes, 2013). campal cortex when viewing an individual who is
Interestingly, subordinates that were removed from superior at a given task. The amygdala and mPFC
their colony and pair-housed were comparable to in- also show increased activation, but only in unstable
colony subordinates, indicating that release from the hierarchies.
social hierarchy is not sufficient for breeder-like neu- In a larger social context, SES encompasses many
rogenesis profiles. These results contrast prior reports interdependent and diverse factors such as income,
on neurogenesis and social rank in noncooperative access to health and education, and parental nurtur-
breeders (Ferragud et al., 2010; Hoshaw, Evans, ance (Hackman, Farah, & Meaney, 2010). Not unlike
Mueller, & Lucki, 2004; Kozorovitskiy & Gould, animals subjected to repeated social defeat, people of
2004). We are now investigating the underlying neu- low SES are more likely to experience chronic stress,
roendocrine mechanisms of status-induced changes in and are therefore at a greater risk of cardiovascular
neurogenesis and, importantly, how they might relate and metabolic diseases as well as depression and
to status differences in behavior. anxiety (McEwen & Gianaros, 2010). Certain compo-
nents of SES appear to mediate brain structure in
children. Lawson, Duda, Avants, Wu, and Farah
SOCIAL HIERARCHIES AND NEURAL (2013) found that greater parental education is corre-
PLASTICITY IN HUMANS lated with greater cortical thickness in the right ante-
rior cingulate gyrus and left superior frontal gyrus of
Similar to the research on nonhuman animals, emer- the child. Additionally, lower parental education is
ging evidence suggests that social status in small- associated with increased amygdala volume and a
group settings (e.g., classrooms and the workplace) greater income-to-needs ratio correlates with greater
and socioeconomic status (SES) has measurable influ- hippocampal volume (Noble, Houston, Kan, &
ences on human brain structure and function. In the Sowell, 2012). Lower childhood SES leads to
context of small groups, bullying might be an analog decreased adult hippocampal volume (Staff et al.,
to the social defeat paradigms employed in laboratory 2012), which might be consistent with the decreases
animals, with the bully as the dominant individual and in hippocampal neurogenesis observed in rodents in
the victim as the subordinate (Björkqvist, 2001). social defeat paradigms and the VBS. However, as
Victims subjected to ongoing incidences of bullying with the rodent literature, because SES alters stress
experience chronic stress and are more likely to exhi- profiles in humans, we need to question whether mor-
bit depression, low self-esteem, and other problems phological differences in the brain are due to stress
(Hawker & Boulton, 2000). These psychosocial pro- rather than status, per se.
blems appear to mirror the depressive behavior of SES also mediates activation of several brain areas,
subordinate rodents in social defeat paradigms. including the left fusiform gyrus and left inferior frontal
Youths with conduct disorders (essentially bullies) gyrus, areas important for phonological awareness,
show greater activation of the amygdala and ventral word rhyming, and overall language function (Noble,
striatum and decreased amygdala–prefrontal coupling Wolmetz, Ochs, Farah, & McCandliss, 2006; Raizada,
compared to healthy controls in response to pictures Richards, Meltzoff, & Kuhl, 2008). Similarly, low-SES
of intentionally inflicted pain (Decety, Michalska, children exhibit decreased prefrontal activity during a
Akitsuki, & Lahey, 2009). However, as bullies tend novelty task (Kishiyama, Boyce, Jimenez, Perry, &
to be unpopular and disadvantaged (Lagerspetz, Knight, 2009) and lower-SES adolescents exhibit
Björkqvist, Berts, & King, 1982), the extent to decreased left frontal activity, which is also associated
which this is a study of social status is questionable. with the individual’s risk for depression (Tomarken,
In actuality, dominant children use coercive or pro- Dichter, Garber, & Simien, 2004). The effects of status
social strategies instead of aggression to compete with on the prefrontal cortex in humans might align with
their peers (Hawley, 1999). Attaining dominance may rodent studies that demonstrate a role for this region in
therefore be the result of strategic social interactions the acquisition of conditioned defeat (Markham et al.,
and not of agonistic behavior per se, a possibility that 2012) and the expression of dominance behaviors
has been largely overlooked in both human and non- (Wang et al., 2011).
human animal literature. Thus, the best evidence for Interestingly, perceived social status also plays an
status influences in small-group hierarchies comes important role in neural function and overall health
from a recent report by Zink et al. (2008). In both (Sapolsky, 2004). For example, lower subjective
stable and unstable hierarchies, people show greater social status covaries with less gray matter volumeSOCIAL STATUS AND NEURAL PLASTICITY 113
in the perigenual area of the anterior cingulate cortex or will not be involved as mechanisms underlying
(Gianaros et al., 2007), and perceiving one’s parents status-induced plasticity. The hormones and receptors
as low in status is associated with higher amygdala in these axes have broad, complex, and dynamic
reactivity to threatening facial expressions (Gianaros effects on brain and behavior beyond the simple defi-
et al., 2008). It is possible that differences in amyg- nitions of “stress” or “sex.”
dala reactivity might be due to altered activity of the In regard to human research, creative experimental
HPA axis, as indicated by social defeat studies in design is critical for answering questions about status.
nonhuman animals (Albeck et al., 1997). As with nonhuman animals, it is important to study
more natural (i.e., preexisting) small-group hierarchies.
For example, members of a team share a common goal
WHERE DO WE GO FROM HERE? and similar environment but have differing ranks.
Furthermore, while short-term manipulations of social
In order to understand how social status regulates status and/or SES are somewhat simple in the labora-
reproductive fitness and health, we need to know tory setting, long-term changes, though challenging,
whether it is a direct mediator of neural plasticity need to be investigated. One possibility here would be
beyond its associations with stress and reproduction. to capitalize on lotteries that have a predetermined
While we believe in the strength of our work with number of participants or situations where people
naked mole-rats, the best way to test social status could be assessed pre- and post-promotion, graduation,
effects on mammalian neural plasticity is a compre- job loss, etc. These are complicated and elaborate para-
hensive, comparative approach. Naked mole-rats have digms that would likely be heavily confounded but they
many advantages for the study of status but they have might shed light on how status influences the human
many species-specific adaptations, not the least of brain in a natural context.
which is their extreme sociality, which might not In this Short Review, we have focused on a subset
generalize to other mammals. Thus, the single biggest of the literature, highlighting those areas that have
step forward we can make is to expand social defeat received the most attention to date and where conver-
paradigms to directly compare dominants and subor- gence of evidence is strongest. It is clear that we
dinates or winners and losers. Even though these cannot yet conclude whether social status is a distinct
animals are often intentionally mismatched in age, construct or the result of numerous other variables that
size, and/or experience, these are powerful compari- vary in importance between sex and species. While it
sons to make given the built-in control for social is likely that plasticity in the serotonergic system and
environment; the pairs experience the same events hippocampus will continue to provide insight into the
but from different status perspectives. Second, we neural mechanisms of social status, there are numer-
need the work with less traditional species, including ous other candidates, including the neuropeptides
those that live in natural hierarchies and/or in which oxytocin and vasopressin, which hold promise. With
status is not linked to circulating glucocorticoids, to a greater appreciation for the importance of social
include more neural end points. Of course, we under- status effects on reproductive fitness and health, and
stand this is not easy when working with unique with a comprehensive and systematic effort, we can
species as we face many of the same challenges in make great strides in this area in the coming years.
our own efforts. Finally, we need to consider different
subtypes of dominants and subordinates. For example, Original manuscript received 5 November 2013
naked mole-rat subordinates can be further classified Revised manuscript accepted 8 January 2014
into subcastes with distinct behavioral and physiolo- First published online 30 January 2014
gical profiles (Lacey & Sherman, 1991). Furthermore,
a subset of subordinate animals in the VBS shows a
blunted stress response and these subordinate animals
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