Cultural evolution via public information. The case of the Melodious Lark?

In my previous blog I focused on a paper that aimed to outline some of the most important current questions in the study of speciation. One of these was 'What is the role of phenotypic plasticity?' Plasticity is variation in phenotype that is determined by environment rather than genetic make-up. How, then, can plasticity cause species to diverge? The idea seems nonsensical, and indeed plasticity is often viewed as an obstacle to speciation. If individuals of a species can adapt to different environmental conditions regardless of their genotype, then surely this cannot lead to speciation. That is, unless plastic phenotypic traits are heritable.

This is where we come to the idea of cultural evolution. Through its development into a global internet phenomenon, the concept of the 'meme' has firmly entered the public consciousness, at least among the younger generation. Memes are the essential unit in cultural evolution, analogous to genes in genetic evolution. However, they differ from genes in that not only can they be transmitted vertically through generations (i.e. from parents to offspring), they can also spread horizontally through the 'meme pool', and obliquely, that is, between unrelated individuals from one generation to the next. For vertical and oblique inheritance of memes to take place, you need overlapping generations. But for any kind of meme exchange, organisms need some way of gathering non-genetically acquired information from other organisms. As Danchin et al. (2004) explain, in an article published in Science, public information (PI) is an important way in which organisms achieve meme transfer.

The concept of public information is simple, but let's first take a step back before we delve into it. There are two types of non-genetically acquired information: personal and social. Non-private personal information generates social information, which itself consists of cues (inadvertent social information [ISI]), and signals (deliberate communication). Danchin et al. (2004) divide ISI into location cues and performance cues, and define the latter as PI. Organisms can learn by making use of PI provided by other organisms, usually members of their own species, and make use of it to enhance their own ecological performance by making better decisions, for example about where to breed or forage. If this process results in a lastingly altered phenotype, then PI can help to generate culture (i.e. shared traditions and information that vary among groups or populations). Culture can then affect the evolution of species, as well as speciation, as it is passed from one generation to the next. Figure 1 provides a neat summary of this.

Figure 1: The types of non-genetically acquired information and their influence on culture, biological evolution, and each other. The blue text and boxes represent topics covered by Danchin et al. (2004). Taken from Danchin et al. (2004).

Danchin et al. (2004) provide a list of examples of how PI is used by various organisms across a broad taxonomic range, and at times it reads like something out of a David Attenborough production. For example, PI is used by various organisms to assess the level of predation risk in an area. In many fish species, when an individual is predated upon, it releases chemicals that provide PI that other fish can use to assess danger levels and decide on the appropriate response. Even plants seem capable of this, as shown from experiments with wild tobacco. When growing alongside another plant species that has been clipped, tobacco plants produce more flowers than when growing among unclipped members of the same species. The perceived greater predation risk (and hence shorter life expectancy) induces plants to divert more resources to reproduction rather than growth.

Habitat copying, whereby individuals use PI about breeding success of other individuals to choose where to breed, and mate-choice copying, whereby females choose which males to breed with based on the choices of other females (which indicate quality; usually used in situations where females struggle to distinguish fitness levels among competing males), are other examples of the importance of PI in evolution. Habitat copying might lead to the evolution of coloniality in birds. Mate-choice copying might explain how sexual selection causing increasingly exaggerated male traits can be reversed (as observed in some phylogenies), if a mutant female with a preference for drab males is copied by other females, as has been observed in experiments with guppies.

It was one example in particular that got me thinking about a potentially very interesting local case of PI and cultural evolution. 'Eavesdropping', whereby individuals make decisions based on the outcomes of others' interactions, is an example of PI use that has implications for a variety of situations. The authors suggest that PI could play a role in cultural evolution if eavesdropping leads to males adopting the songs of successful males more often than unsuccessful males. In South Africa there is a bird that has been observed engaging in some very unusual behaviour. It's called the Melodious Lark Mirafra cheniana, and males are extraordinarily accomplished mimics. Roberts Birds of Southern Africa (Hockey et al. 2005, p.861), provides the following list of bird groups recorded amongst its vocal repertoire: 'kites, kestrels, francolins, guineafowl, lapwings, coursers, go-away-birds, cuckoos, bee-eaters, swifts, shrikes, swallows, warblers, larks, chats, sunbirds, pipits, longclaws, starlings, weavers, waxbills and canaries.' In his insightful and informative guide to Southern Africa's larks and other 'little brown jobs', Faansie Peacock (2012) notes that each male can probably mimic over 50 different species of bird, and mentions another interesting aspect of its behaviour that I can find no other reference to. Males often gather and sing in loose aggregations, and interestingly, will often simultaneously mimic the same species as other males in the group. Clearly, this 'copycatting' behaviour involves the transmission of ISI between singing males - their singing is certainly not directed at one another. But what purpose does it serve? And might PI and culture play a role in this behaviour?

Melodious Lark

Many species of bird engage in group display behaviour known as 'lekking', which can often be amazingly well coordinated. Blue Manakins are a fantastic example of this. Groups of four or so males display to females as a 'team', leapfrogging over one another while rapidly 'buzzing' their wings to create a spectacular effect. In the end, only one male will mate with any suitably impressed females, but the 'losers' on his team stand a chance to take over as 'team leader' in the future, and so their sacrifice in the short-term is offset by their potential benefit in the long run. 

The copycatting behaviour of male Melodious Larks might be a form of lekking. However, an interesting question is whether it is genetically or culturally determined. Do males learn to copycat other males, or is it a genetically determined trait? Melodious Lark males are often found displaying singly, meaning that this lekking behaviour isn't the only means by which males attract mates. If they do learn, then what kind of information do they employ in the learning process? As a first step, it would be interesting to compare breeding success between males displaying in lekking groups and males displaying singly. Do males that lek have higher paternity? Does a single male 'win out' within lekking groups and breed with the majority of females in the area? Also, is competition for mates (i.e. sexual selection) stronger among lekking males? This last question could potentially be answered by comparing the vocal repertoires of males that do and don't lek. The question of whether lekking males have higher quality territories would also be interesting to explore in this regard. One might hypothesize that males that lek can mimic more species, perhaps because they are more experienced (i.e. older and hence fitter, and able to maintain a hold on higher quality territories), or perhaps because they are more likely to be shown up as being pretenders if they can't 'keep up' with the other males. This is where the possibility of cultural evolution comes into play, but it's something that I can't quite get my head around. Is copycatting a meme used by males to fool females into thinking that 'I'm as fit as the next guy', or is it an honest, genetically determined signal used by females to more efficiently distinguish the fittest males in (perhaps) the highest-quality territories? I think it would be fascinating to do an in-depth study on the breeding biology of these birds, and particularly to delve into the 'Why?' and 'How?' of their curious copycatting behaviour.  

References

Danchin E, Giraldeau L, Valone TJ and Wagner RH. 2004. Public Information: From Nosy Neighbors to Cultural Evolution. Science. 305: 487-491. 

Hockey PAR, Dean WRJ and Ryan PG (eds). 2005. Roberts - Birds of Southern Africa VII^th
ed. The Trustees of the John Voelker Bird Book Fund. Cape Town.

Peacock F. 2012. Chamberlain's LBJs. Mirafra publishing. Pretoria.