Order is a standard part of nature, from the mathematical patterns found in natural structures to the predictable variation in sunrise times at different times of year. Indeed, animals and plants rely on regular, logical ordering of events.  For example, in my work on pollinator ecology bees rely on seasonal patterns in flower blooming as a food source. But this regularity is a double-edged sword: just as a bee can exploit regularity in flowering times, so can birds exploit the regularity in bee occurrence. A shared synchrony of life cycles brings costs and benefits. And this is where we bring in the Greek sea-god Proteus (pictured right). Proteus was a god who was able to change his form to avoid having to tell the future, and he has given his name to “protean” phenomena – those phenomena that are changeable or unpredictable. We can see a potential benefit in the plants altering their timing of flowering (of exhibiting protean flowering patterns) – if they remain predictable then the bees on which they rely for pollination are also predictable, which means that they are easy to exploit as food for birds. However, unpredictable flowering times might result in flowers occurring when there are no pollinators, which would be bad for both groups. Synchrony in the seasonality of flowers, insects, and birds is a complex association between populations (or even communities) of animals, and this makes evolutionary change slow.

Protean behaviour and natural selection

A simpler example of evolutionary pressure for protean behaviour can be seen on the African savannah, where a much simpler interaction plays out (for your own sake, mute your speakers):

Note that during a number of chase sequences, the impala exhibit sudden changes in direction, dropping their shoulders and stomping on the ground to alter trajectory (0:43-0:53, 1:15-1:20, 1:54-2:05, and 2:53-3:10).  Impala can run at 80kmph at a peak, but cheetah can run at up to 93kmph.  By introducing unpredictable, sudden changes in direction, the impala can level the playing field (running track?) by removing the cheetah’s straight-line advantage. This is a classic example of how natural selection can act very strongly on individuals to produce an increase in unpredictable behaviour.

Protean behaviour and sexual selection

However, some researchers have suggested that the evolution of protean behaviour could also have a sexual role as well.  The complexity of a male bird’s song is associated with higher levels of sexual selection, suggesting that when there is a lot of competition for mates females tend to choose males with greater complexity. There are many other factors at play, but complexity is one.  Here is an example of the tui singing its unusually complex song (note that some parts of the vocalisation are inaudible to humans):

A role for protean behaviour in humans

Geoffrey Miller (he of the recent “fat students don’t have the willpower to finish a PhD” tweet) proposed a controversial but interesting theory that the human mind itself was the product of sexual selection, and that recent encephalisation (development of brain size and structure) was due to female selection on male protean behaviour.  He described this theory in his book “The Mating Mind“.  Miller has noted, for example, that “music is functionally analogous to sexually-selected acoustic displays in other species” and that in a large sample of classical, jazz and rock musicians, “males produced about 10 times as much music as females, and their musical output peaked in young adulthood, around age 30, near the time of peak mating effort and peak mating activity”. Miller suggests that the human brain is a “protean courtship device” that is designed to generate and appreciate novelty in males and females, respectively. In this sense, the brain is to humans as an elaborate tail is to peacocks: both are immensely complex and expensive traits that are generated by sexual selection.

An experimental test of the role of protean behaviour in human mate choice

The problem is that there have been very few attempts to test these hypotheses experimentally. A 2012 study showed that women were more likely to respond to Facebook requests from men who were holding a guitar in their profile picture (seriously, this is pretty much as good as it gets so far!). Despite the fact that sample sizes were small, the authors tentatively suggest that this represents evidence for the music-as-sexual-selection theory put forward by Miller. More rigorous studies are easy to conceive: record the same male or female participants (say 10 of each) playing a series of four piano pieces. The first piece should be a common piece that everyone knows (Beethoven’s Fur Elise, for example), the second piece should be an unusual piece that all participants are capable of replicating, the third piece should be a unique composition of the pianist, and the fourth could be a nonsense, atonal control that is common across all pianists but utterly without pattern. Ask participants (this can be done online) to rate the performers for attractiveness in a still photo, and then during performance of the pieces. If Miller’s hypothesis holds, we would expect that the unfamiliar tune would be more attractive, controlling for the physical attractiveness of pianists using the still photo.  Actually, that’s pretty interesting – maybe I’ll get an enthusiastic student to look at this this coming year…

Image credits: Proteus wood cut is by Jörg Breu displayed in the Book of Emblems by Andrea Alciato; pianist is by Михаил Аркадьев, both via Wikimedia Commons.