Elsevier

Hormones and Behavior

Volume 89, March 2017, Pages 145-156
Hormones and Behavior

Neuromolecular correlates of cooperation and conflict during territory defense in a cichlid fish

https://doi.org/10.1016/j.yhbeh.2017.01.001Get rights and content

Highlights

  • Astatotilapia burtoni males show reduced to aggression to familiar neighbors.

  • Familiar neighbors cooperate in territory defense dependent on perceived threat.

  • Residents modulate their own behavior based on help received.

  • Neural activity and dopamine in specific brain regions correlate with cooperation.

  • Neural activity patterns differ depending on individual role in defense coalition.

Abstract

Cooperative behavior is widespread among animals, yet the neural mechanisms have not been studied in detail. We examined cooperative territory defense behavior and associated neural activity in candidate forebrain regions in the cichlid fish, Astatotilapia burtoni. We find that a territorial male neighbor will engage in territory defense dependent on the perceived threat of the intruder. The resident male, on the other hand, engages in defense based on the size and behavior of his partner, the neighbor. In the neighbor, we find that an index of engagement correlates with neural activity in the putative homolog of the mammalian basolateral amygdala and in the preoptic area, as well as in preoptic dopaminergic neurons. In the resident, neighbor behavior is correlated with neural activity in the homolog of the mammalian hippocampus. Overall, we find distinct neural activity patterns between the neighbor and the resident, suggesting that an individual perceives and processes an intruder challenge differently during cooperative territory defense depending on its own behavioral role.

Introduction

Cooperation both within and between species has evolved repeatedly in numerous lineages of vertebrates and invertebrates (Dugatkin, 1997, Sachs et al., 2004). Cooperation is the ‘acting together’ of two or more individuals to achieve an end situation which could not be achieved individually (Taborsky, 2007, Brosnan and de Waal, 2002). A cooperator pays a cost for another individual to receive a benefit, often resulting in an average increase in direct fitness (Brosnan and Bshary, 2010, Nowak, 2006). A defector, however, pays no cost and does not provide benefits (Nowak, 2006). Knowledge about and awareness of the actions of social partners are often key features of cooperative behavior. Importantly, without examining how the brain is processing and responding to social information our understanding of cooperative behavior remains quite limited (de Waal and Ferrari, 2010). To address this gap in our knowledge of cooperation, in this study, we examine neural correlates of cooperation and conflict in the form of cooperative territory defense.

Competition over resources can serve as a selective force for the evolution of cooperation (Díaz-Muñoz et al., 2014). Familiar neighboring territorial males of many species exhibit restraint in aggression toward each other despite being in direct competition for mates, food, and shelter, though they will ferociously attack trespassing strangers (Fischer, 1954). It can be less costly to cooperate than to renegotiate boundaries with a new neighbor, which is why under certain conditions a territorial male may cooperate with other males by defending a neighboring territory from an intruder (Getty, 1987). Although this form of cooperation is predicted to be widespread in nature, it has been convincingly demonstrated in very few species. For example, in fiddler crabs (Backwell and Jennions, 2004) and possibly chipping sparrows (Goodwin and Podos, 2014) (but see (Akçay and Beecher, 2015)), neighboring males will cooperate and come to the aid of a neighbor depending on the perceived degree of threat posed by an intruder. Interestingly, only the behavior of the neighbor has been examined in these cases. It is unknown how the recipient responds to receiving help. Here, we study both the cooperator and the recipient to gain an understanding of how an individual's behavioral role during territory defense may affect both behavior and the underlying neural processes involved.

The brain regions and gene networks that mediate decision-making in the context of cooperation are as of yet unknown (Taborsky and Taborsky, 2015), although strategic social cooperation very likely involves the integration of spatial and affective memory with reward processing and aggression regulation. We therefore hypothesized that the social decision-making (SDM) network, a deeply conserved neural circuit involved in the integration of salient stimuli and reward processing across vertebrates (O'Connell and Hofmann, 2011, O'Connell and Hofmann, 2012) plays a central role in these processes. Given our current knowledge, SDM network nodes such as the hippocampus, amygdala, striatum, and preoptic area appear to be particularly good targets of investigation in this context. Briefly, across vertebrates, the amygdala is critical for encoding and responding to the affective valence of social (and other) signals (Adolphs, 2010, McGaugh, 2004). The striatum, a central region in the reward system, regulates motivated behavior (Balleine et al., 2007, Báez-Mendoza et al., 2013). The hippocampus is well known for organizing spatial memory and plays a critical role in social recognition (Kogan et al., 2000, Eichenbaum, 2004). The preoptic area is a neuroendocrine relay center essential for sexual and aggressive behavior (Hull and Dominguez, 2007). Finally, excitatory and inhibitory projections between these and other SDM network regions are essential to mediating complex behavior (Felix-Ortiz and Tye, 2014, van der Meer et al., 2014).

Numerous neurochemical pathways regulate social behavior across vertebrates. For example, the glucocorticoid cortisol (Cort) is typically associated with the physiological response to highly salient – e.g., social (Summers et al., 2005) – stimuli, often (though not necessarily) considered stressors. Androgens, such as testosterone (T), are also well-known to mediate social context and are typically released in response to social challenge (Wingfield et al., 1990). It has been proposed that T surges reinforce learning associated with aggressive challenges in a manner dependent on the location where the agonistic encounters take place (Gleason et al., 2009). Importantly, T interacts with the dopaminergic reward system to induce conditioned place preference (Schroeder and Packard, 2000). Dopamine (DA) plays several important roles in the regulation of behavior; it encodes the salience and rewarding properties of social stimuli, and it modulates motivated, goal-directed behavior (Riters, 2012, Trainor, 2011). It is then maybe not surprising that the DA system has been implicated in cooperative cleaning behavior of the Indo-Pacific bluestreak cleaner wrasse, Labroides dimidiatus. Specifically, treatment with a dopamine D1 receptor antagonist increased the number of cleaning interactions, as well as tactile stimulation toward clients, though it is unclear if cooperation was affected per se (Messias et al., 2016). Taken together, these findings suggest that glucocorticoids and androgens, possibly in conjunction with the mesolimbic DA system, could play central roles in regulating cooperative decision-making in general and cooperative territory defense more specifically.

The African cichlid fish, Astatotilapia burtoni, displays extraordinary context-dependent social behavior. As a result, this species has become a powerful model system in social neuroscience for investigating the neural bases of complex social behavior (Hofmann, 2003). Dominant A. burtoni males aggressively defend spawning territories (Parikh et al., 2006). Border conflict behavior occurs between dominant males in neighboring territories along their shared boundary (Fernald and Hirata, 1977). A. burtoni males modulate their behavior based on visually acquired social information (Grosenick et al., 2007, Desjardins et al., 2012, Alcazar et al., 2014, Chen and Fernald, 2011). They are capable of transitive inference and can deduce the dominance hierarchy by observing pairwise interactions between opponents (Grosenick et al., 2007). In addition, males perceive and respond to very small size differences between competitors (± 3 mm, < 8%) with an advantage to the larger of two opponents (Alcazar et al., 2014). Importantly, both the SDM network and the dopaminergic system have been described in detail in this species (O'Connell and Hofmann, 2011, O'Connell et al., 2011, O'Connell et al., 2013a).

To begin to examine the neural basis of cooperation, we investigated whether and if A. burtoni males display cooperative defense behavior in a series of four experiments. In Experiment 1 (habituation), we examined whether and how neighboring males socially habituate to each other (by exhibiting decreasing aggression) and how steroid hormone levels change in response. We hypothesized that neighbor familiarity would lead to a decrease in aggression and steroid hormone levels. In Experiment 2 (cooperative defense), we used male body size differences to assess the extent and attributes of cooperative defense in response to an intruder. We hypothesized that neighbors would engage in cooperative territory defense in a size-dependent manner by aggressing the intruder more when the resident is smaller than the intruder, as smaller residents would benefit more in such a case. We predicted resident males would be aggressive to an intruder independent of size, given the immediate perceived threat, but may modulate behavior based on help received from their neighbor. To gain a better understanding of the interaction between partners and the significance of neighbor assistance, in Experiment 3 (neighbor defection), we simulated neighbor defection during a territorial intrusion and examined the behavioral response of the resident male. We hypothesized that neighbor defection would result in increased aggressive defense from the resident. Finally, in Experiment 4 (neural activity in cooperation and conflict), we analyzed immediate-early gene (IEG) induction to determine how variation in cooperation from neighbors and residents varied with neural activation in SDM network nodes such as the hippocampus, amygdala, striatum, and POA. Immediate-early genes, such as c-Fos, are widely used to assess region and cell type-specific responses to various stimuli (Morgan and Curran, 1991). Further, to gain insight into the function of activated cells, we examined the role of DA in a spatially explicit manner by co-labeling c-Fos with tyrosine hydroxylase (TH), which is often used as a marker of dopaminergic cells. We hypothesized that cooperation would lead to increased activity in reward-related regions and that the specific role an individual plays in a cooperative context might be associated with distinct neural activity patterns across key nodes of the social decision-making network.

Section snippets

Animals

A. burtoni descended from a wild caught stock population were maintained in naturalistic communities, as described previously (Munchrath and Hofmann, 2010), until transfer to the experimental paradigm. All work was done in compliance with the Institutional Animal Care and Use Committee at the University of Texas at Austin.

Behavior

Paired adjacent 38 l aquarium tanks were established with one territorial A. burtoni male and two females taken from stable community tanks, as well as two juveniles from grow

Experiment 1: aggressive behavior and hormone levels decreased with repeated social exposure

Upon repeated visual exposure to a territorial male (Fig. 1), the amount of aggressive displays decreased over time (LMER: t = 11.315, p < 0.001, Fig. 2). Aggressive displays decreased from Day 1 to Day 2 (V = 171, p = 0.001, r = 0.47), and from Day 2 to Day 3 (V = 197.5, p < 0.001, r = 0.51), but not from Day 3 to Day 4 (V = 94, p = 0.98, r = 0.01). Interestingly, small males displayed more frequently to their partner on Day 1 (R2 = 0.14, p = 0.002) and Day 4 (R2 = 0.11, p = 0.006). Using a non-invasive waterborne hormone

Discussion

We identified neural correlates of cooperation and conflict in the context of territory defense coalitions. A neighbor's decision to engage in territory defense is based on the perceived threat of the intruder. Interestingly, as the beneficiary of these actions, the resident modulates his defensive aggression toward an intruder based on the (perceived) level of cooperation by the neighbor. We find that the Engagement Index is associated with activity in the homologs of the mammalian basolateral

Acknowledgements

We thank Sean Maguire, Rayna Harris, Peter Dijkstra, and Esther Osuji for assistance, members of the Hofmann lab for discussion, and Tessa Solomon-Lane for helpful comments on an earlier version of this manuscript. This work was supported by Carl Gottfried Hartman Graduate Endowment Fellowship, The University of Texas Integrative Biology Recruitment Fellowship, and NSF Graduate Research Fellowship to CAW, by the Alfred P. Sloan Foundation (BR-4900) and NSF grants IOS-1354942 and IOS-1501704 to

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