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Review
, 220 (Pt 1), 103-113

Cognitive Skills and the Evolution of Social Systems

Affiliations
Review

Cognitive Skills and the Evolution of Social Systems

Russell D Fernald. J Exp Biol.

Abstract

How do animal social skills influence evolution? Complex animal social behaviors require many cognitive skills including individual recognition and observational learning. For social systems to evolve, these abilities need to be transmitted genetically or culturally and supported by the evolution of underlying neural systems. Because animal skill sets are so varied, it seems best to describe animal cognitive behaviors as being a social calculus that can change with experience, which has evolved to match and facilitate the complexity of the social system where it arose. That is, acquiring and using social information in response to a rapidly changing complex world leads to social competence enabling success in essential behavioral interactions. Here, we describe the remarkable suite of social skills discovered in the African cichlid fish Astatotilapia burtoni, including an attention hierarchy, male deception, transitive inference, the mechanistic bases of social dominance, female mate choice and the neural control of female reproductive behavior. The social calculus of this species is presented as an example of a potential causal factor in the evolution of sophisticated social behavior necessary for the evolutionary success of their social system.

Keywords: Astatotilapia burtoni; Cichlid fish; Individual recognition; Social behavior; Social calculus; Social evolution.

Conflict of interest statement

The author declares no competing or financial interests.

Figures

Fig. 1.
Fig. 1.
Sketch of an observation site along the edge of a shore pool on the north end of Lake Tanganyika, near Bujumbura, Burundi, Africa. Solid dots represent grid stakes spaced at ∼50 cm intervals that label grids (1–5; A–D) for identification. Circles represent spawning pit locations of dominant Astatotilapia burtoni males. Lighter outlines circumscribe the approximate territories of dominant individuals. Male territories are located over the food source of detritus on the bottom of the pool. This detritus accumulates at the northeast edge of pools as a result of the strong daily southerly winds. Non-dominant males and females school together near the territorial area that they have to enter to eat. Based on Fernald and Hirata (1977a).
Fig. 2.
Fig. 2.
Three-dimensional plot of mean soma diameter of preoptic area irGnRH1 neurons in males of different social status. There are significant differences between dominant (D) and D→non-dominant (ND) males and between ND and ND→D males. Soma size is a proxy for gonadotropin releasing hormone 1 (GnRH1) abundance. The percentage of individuals with mean soma size in a given size bin is plotted for each treatment condition. Redrawn from Francis et al. (1993).
Fig. 3.
Fig. 3.
An example of eye movements during social interactions. Fish and their eye positions have been drawn from individual film images at 160 ms intervals with the 1st to 11th frames labeled. Relative eye locations of the dominant animal are shown by lines extending from stalks attached to the eyes at an arbitrary angle behind the central axis of the eye. Note that the ND animals move out of the region being approached by the D male well before he arrives. Redrawn from Fernald (1985).
Fig. 4.
Fig. 4.
Schematic illustration of typical D male behavior in the presence of an intermediate ND male attempting to ascend to dominance. Large rectangles represent the D male has entered his shelter and cannot be seen by the ND males. Thin black bars show when an individual chases or attacks another fish. Note that intermediate ND males only attack other animals when the D male is in his shelter and cannot see them. From data presented in Desjardins et al. (2012).
Fig. 5.
Fig. 5.
Schematic diagram of aquarium used for behavioral observations. Front view of an aquarium (45 l), divided in half with a watertight, clear divider (gray mid-line) and a removable opaque barrier (black mid-line); in one side there is a small male fish (left) and in the other there is a large male fish (∼4 times larger, right). The half terracotta pot (red curved line) was cut so that the two fish ‘shared’ the same shelter, though they were not aware of each other's presence. This ‘shared’ shelter was hemisected by both center dividers. A layer of gravel covered the bottom of the tank. Once the two males had established their territories on the opposite sides of the barrier, the black divider was removed. Modified from Chen and Fernald (2011).
Fig. 6.
Fig. 6.
Tank arrangement and bystander training. Five rival males (a–e) were arranged in visually, chemically and physically isolated compartments around a central bystander unit. To train a bystander on a particular fight, the male scheduled to be the ‘loser’ was removed from his unit and placed in the territory of the scheduled ‘winner’. The opaque barrier separating the bystander from the rivals was then removed to allow the bystander to view the fight. Fish were trained for either a>b>c>d>e or a=b=c=d=e. The fight d versus e (e ‘wins’, d ‘loses’) is shown here in diagrammatic form. Modified from Grosenick et al., (2007).
Fig. 7.
Fig. 7.
Arena for testing male choice after observing fights. Following training in the reconfigured test arena (A), fish were tested in a novel arena (B). Fish moved towards the weaker animal (d) (Oliveria et al., 1998; Clement et al., 2005), indicating they considered b would beat d in a fight. Modified from Grosenick et al. (2007).
Fig. 8.
Fig. 8.
Pulsatile urine release from a dominant male. A D male, injected with dye was exposed visually to another D male. The D male produced pulses of urine in response to the other male (arrow). After Maruska and Fernald (2012).
Fig. 9.
Fig. 9.
Experimental design and results from testing injections. (A) Males that had never be socially dominant (N=60) were randomly divided into three groups of size-matched pairs. (B) In control animals, both members of the pair received vehicle injections. In experimental animals of one group (left), one member of the pair received l-methionine and the other received vehicle control; in the other group (right), one member of the pair received zebularine and the other received vehicle control. (C) Animals receiving l-methionine injections became socially dominant while those receiving zebularine did not. Modified from Lenkov et al. (2015).
Fig. 10.
Fig. 10.
Behavior and corresponding regulatory signals leading to female behavior. (A) Schematic illustration of the natural progression of spawning behavior. The male quivers his body in front of the female and leads her to his spawning site (flower pot) and they circle, with the male pecking the female to elicit egg laying followed by egg collection, and the female collecting the sperm from the male anal fin to fertilize the eggs in her mouth. (B) Neural pathway from the receipt of social signals triggering activation of GnRH1 neurons; release of luteinizing hormone (LH) and follicle stimulating hormone (FSH) stimulates the reproductive tract, where progestin (PR) and PGF act on the Ptgfr receptor to stimulate the final stages of egg laying. Modified from Juntti et al. (2016).

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