An evolutionary chase: how mimicry remains imperfect despite rapid evolution of mimics.

Using a 50 year time series of egg photos of prinias and their mimic, the cuckoo finch, we showed that although cuckoo finch eggs evolve towards prinia eggs, concurrent evolution of prinia eggs maintains imperfection in the degree of mimicry.
Published in Ecology & Evolution

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In the wet grasslands of Choma district, Zambia, a remarkable evolutionary struggle takes place. A female cuckoo finch, a nondescript brown bird, lays an egg in the nest of a tawny-flanked prinia. Like her well-known namesake, the common cuckoo, a female cuckoo finch will leave the rearing of her young to the prinia pair, who – unless they can identify this imposter egg – will end up wasting the rest of the breeding season raising the cuckoo finch chick. To make matters worse, the cuckoo finch chick (or chicks, if the female cuckoo finch laid multiple eggs) will outcompete any prinia chicks in the nest, so the prinia pair fail to raise any of their own young.

Unsurprisingly, therefore, prinias have evolved to recognise (and remove from their nests; Image 1) eggs that look dissimilar from their own. Cuckoo finches in turn have evolved mimicry of prinia eggs. And just like humans who use individually-distinctive signatures and passwords to make it difficult for them to be copied, prinia eggs have evolved individually-distinctive egg signatures comprising a range of colours and patterns (Image 2).

Image 1: A video grab of a prinia removing a foreign egg from her nest. Image: Tanmay Dixit and Jana Riederer.

Image 1: A video grab of a prinia removing a foreign egg from her nest. Image: Tanmay Dixit and Jana Riederer.

Photograph of eggs illustrating prinia egg signatures and cuckoo finch 'forgeries'

Image 2: Prinia eggs (outer circle) and cuckoo finch eggs (inner circle). Each egg was laid by a different female, illustrating the range of colours and patterns that make up the egg signatures of individual prinias and the ‘forgeries’ of individual cuckoo finches. Image: Claire Spottiswoode.

In the human world, more complex signatures and passwords are harder to copy – as we all know, the simple 1234 is not a good password! By analogy, high egg pattern complexity would also benefit prinias faced with cuckoo finch forgeries.

Not only is complexity a property of effective signatures, in a previous study (Dixit et al., 2022, Proceedings of the Royal Society B), we found that a greater difference in complexity between eggs in a nest makes egg recognition more likely. In other words, if we put an egg with low complexity in a nest with eggs of high complexity (or vice versa), that additional egg was quite likely to be recognised.

How might this system evolve? Our previous study had also found that prinia eggs tended to have more complex egg patterns than cuckoo finches. We could therefore predict the course of evolution – cuckoo finches should benefit from increased complexity of egg patterns (making their eggs more similar to prinia eggs) and prinias should also benefit from increased complexity (making their eggs more different from cuckoo finch eggs). In other words, cuckoo finches and prinias should coevolve – that is, each species should evolve in response to the other. This predicted coevolutionary process is illustrated in Image 3.  

Schematic illustrating how complexity would be predicted to evolve in this system.

Image 3: Schematic illustrating how we might predict complexity to evolve, given that prinia eggs are more complex than those of cuckoo finches. In this schematic, higher complexity is illustrated as more spots, though in reality complexity does not necessarily correspond directly to the number of markings on eggs. Bird images:

Testing whether these coevolutionary predictions hold true in reality would require going back in time to look at lots of eggs from the distant past, and compare them to more recent eggs. In Zambia, we were in the fortunate position of being able to do this. From 1970 to the early 2000s, an egg collection was amassed by the late John Colebrook-Robjent (a co-author on this study), and a team of skilled nest finders led by Lazaro Hamusikili (also a co-author; Image 4). The prinia clutches collected by them (some of which also contained cuckoo finch eggs) allowed us to compare the complexity of historical eggs to the complexity of eggs from our own fieldwork in recent years (Image 5). Colebrook-Robjent’s remarkable egg collection and its associated data are now safely housed at the Livingstone Museum in Livingstone, Zambia.

Image of nest-finders and co-author Lazaro Hamusikili.
Image 4: Left: Three of the top nest-finders who enabled our recent field research – from foreground to background: Oliver Kashembe, Oscar Siankwasiya, and Sylvester Mukonko. Right: Co-author Lazaro Hamusikili (R; with his son Tom), who contributed substantially to the historical dataset, holds a tawny-flanked prinia. Images: Tanmay Dixit and Claire Spottiswoode.
Examples of prinia and cuckoo finch eggs from different years.

Image 5: Examples of prinia and cuckoo finch eggs from historical (1970–2002) and current (2012–2020) time periods. Bird images: Egg images: Tanmay Dixit and Claire Spottiswoode.

Using data collected from 1970 until 2020, we observed that egg pattern complexity had increased over time across both prinias and cuckoo finches (Image 6), conforming to the coevolutionary predictions that cuckoo finches should evolve ‘towards’ prinias and prinias ‘away’ from cuckoo finches. Remarkably, this evolutionary change occurred over a mere 50 years, an extremely short period of time for evolution to be observed in a vertebrate. Vertebrates have relatively long generation times, resulting in typically slower evolution than that seen in organisms such as bacteria. This suggests that the evolutionary pressures on cuckoo finches and prinias must have been strong to result in observable changes over a short timespan.  

Illustration of complexity increase in prinias and cuckoo finches.

Image 6: Increases in egg pattern complexity (measured on a log scale) in (a) cuckoo finches and (b) prinias. Bird images:

What does the evolution we observed mean for the battle over identity between cuckoo finches and prinias? We tested whether the accuracy with which cuckoo finch eggs mimic prinia eggs (‘mimetic fidelity’) had changed over time, and found that it had not (Image 7). In other words, cuckoo finches are just as good mimics of prinias as they were 50 years ago, despite evolving rapidly. It is the evolution of prinias away from cuckoo finches (so-called ‘chase-away evolution’)  that maintains imperfect mimicry in the cuckoo finch. Effectively, the increase in complexity of cuckoo finch eggs is ‘chasing’ prinias into evolving even higher complexity. Because both species have evolved at approximately similar rates, the mimicry remains as imperfect as it used to be 50 years ago! Our study therefore found evidence for the hypothesis that chase-away evolution can maintain imperfect mimicry.

Illustration of the lack of change in the accuracy of mimicry over time.

Image 7: Box plot showing the overall distribution of differences in complexity between prinia and cuckoo finch eggs, in two time periods (historical and current). The distributions for historical eggs and current eggs are almost identical, illustrating that mimetic fidelity has not changed.

The evolutionary fitness of prinias and cuckoo finches is likely to depend, at least in part, on how well cuckoo finch eggs are able to mimic prinia eggs. Therefore, our results suggest that although both species have been evolving rapidly, there has been no change in fitness in either species. Such dynamics, where evolution in one species effectively ‘cancels out’ evolution in the other, are often called red-queen dynamics. This is because the Red Queen in Lewis Carroll’s Through the Looking Glass says “Now, here, you see, it takes all the running you can do, to keep in the same place”. Prinias and cuckoo finches have done a lot of running over the last fifty years, with cuckoo finches chasing prinias to ever higher complexity. But, just like the Red Queen, all of this running has left them in the same place that they were in 50 years ago.

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