Harsh environment for pluralism in animal societies: behavioural specialisation within populations

Two extreme approaches to consider species-specific behaviour exist in ecological and ethological studies: to distinguish unique individualities of members of species and to consider a population as a whole treating conspecific individuals as ecologically equivalent. Applying ideas of evolutionary ecology helps to find a middle course and to reveal relatively stable fractions of populations that differ by sets of behavioural characteristics, a differentiation that covers routine differences of individuals by sex and age.

There are at least two levels of behavioural specialisation within populations. In some species members of a population comprise distinct groups that behave differently according to their evolutionary stable strategies. In some cases members of these groups can be easily distinguished by certain morphological markers. Besides, more flexible individual specialisation can be expressed in differences in diets, techniques of getting food, forming searching images, escaping predators, nestling and so on. Relatively stable groups can exist in population that differ by complexes of behavioural characteristics.

Evolutionary stable strategies: a battle of behavioural phenotypes. The theory of evolutionary stable strategy (or ESS) introduced by Maynard Smith and Price in 1973 is based on the concept of a population of organisms divided into several groups which use different strategies.

A group is in a stable state if it is disadvantageous for any individual to change its strategy. In other terms the proportion of individuals using each strategy is optimal; natural selection suppresses any deviation from the current proportion.

Maynard Smith’s best known work incorporated game theory into the study of how natural selection acts on different kinds of behaviour. He developed the idea of an evolutionary stable strategy as a behavioural phenotype that cannot be invaded by a mutant strategy. A classic example is a balance between hawks-like (aggressive) and doves - like (non-aggressive) individuals in natural populations. Maynard Smith and Price (Maynard Smith and Price, 1973; Maynard Smith, 1974, 1982) demonstrated that both carriers of aggressive and non-aggressive behavioural strategies can co-exist comfortable and stable in populations for a long time, and neither aggressors nor non-aggressors invade the population (see also McFarland, 1985, for a detailed description).

Males of many species are characterised by alternative mating strategies and thus compose a representative set of examples concerning distinct behavioural strategies of carriers of different ESS. These strategies are based on complex behaviour sequences and thus may make an impression of deliberate choice of variants on observers.

For instance, Sinervo and Lively (1996) revealed impressive mating strategies within populations of the side-blotched lizard (Uta stansburiana) native to California. These lizards have three mating strategies: distinct types of behaviour that constantly compete with one another in a perpetual cycle of dominance. Carriers of different behavioural strategies are marked by morphological signs. Researchers described the cycle of dominance in lizards in terms of ESS as the “scissors-paper-rock” game.

In the side-blotched lizards males have one of three throat colours, each one declaring a particular strategy. Dominant, orange-throated males establish large territories within which live several females. Orange males are ultra-dominant and very aggressive owing to high levels of testosterone, and attack intruding blue-throated males that typically have more modest levels of testosterone. “Blue” males defend territories large enough to hold just one female. These males spend a lot of time challenging and displaying, presumably allowing males to assess one another. Territories of both orange and blue males are vulnerable to infiltration by males with yellow-striped throats - known as sneakers. Sneakers have no territory of their own to defend, and they mimic the throat colour of receptive females. It is interesting that yellows also mimic female behaviour. When a yellow male meets a dominant male, he pretends he is a female - a female that is not interested in the act. In many cases, females will nip at the male and drive him off. By co-opting the female rejection display, yellow males use a dishonest signal to fool some territory holding males. The ruse of yellows works only on orange-throated males. Blues are not fooled by yellows. Blue males root out yellow males that enter their territories. Blue males are a little more circumspect when they engage another blue male during territory contests. Attack may or may not follow as blue males very often back down against other blue males. Indeed, neighbouring males use a series of bobs to communicate their identity, and the neighbours usually part without battle.

Thus, each strategy has strengths and weaknesses and there are strong asymmetries in contests between morphs. Trespassing yellows, with their female mimicry, can fool oranges. However, trespassing yellows are hunted down by blue males and attacked. While oranges can handily defeat blues, they are susceptible to the charms of yellows. In contrast, contests between like morphs (e.g., blue vs blue, orange vs orange or yellow vs yellow) are usually more symmetric. Field data showed that the populations of each of these three types, or morphs, of male lizard oscillate over a six-year period. When a morph population hits a low, this particular type of lizard produces the most offspring in the following year, helping to perpetuate the cycle. This arrangement somehow succeeds in maintaining substantial genetic diversity while keeping the overall population reasonably stable. This is a good example of genetically-based control over morpho- and behavioural type development (Sinervo and Globert, 2003).

Another good example of male’s alternative behavioural strategies came from Bluegill sunfish (Lepomis macrochirus). Gross (1979, 1984) discovered that in this species males come in three different size morphs: (1) A large territorial parental male that courts females, and then defends a nest in which he rears eggs that the female oviposits; (2) A medium sized satellite or sneaker male that mimics females, interrupts a courting territorial male and attempts to fertilise the female, and (3) A very small satellite that dives in between a mating territorial male and female and squirts ejaculate in an attempt to fertilise the female. Gross argues that such morphs are condition dependent tactics in which all males have the capability to become any of the alternative types. As a result, “developmental decisions" are made, based up the condition of the male. Males that are in poorer condition become the smaller male types and the males that are in the best condition adopt the territorial-holder strategy.

This study is considered an example of condition-dependent strategies contrasting with genetically-based control over the development of a distinct strategy.