Chase-away evolution maintains imperfect mimicry in a brood parasite-host system despite rapid evolution of mimics.

We studied a brood parasite-host system (the cuckoo finch Anomalospiza imberbis and its host, the tawny-flanked prinia Prinia subflava) to test (1) the fundamental hypothesis that deceptive mimics evolve to resemble models, selecting in turn for models to evolve away from mimics ('chase-away evolution') and (2) whether such reciprocal evolution maintains imperfect mimicry over time. Over only 50 years, parasites evolved towards hosts and hosts evolved away from parasites, resulting in no detectible increase in mimetic fidelity. Our results reflect rapid adaptive evolution in wild populations of models and mimics and show that chase-away evolution in models can counteract even rapid evolution of mimics, resulting in the persistence of imperfect mimicry.

Repeatable randomness, invariant properties, and the design of biological signatures of identity.

What makes a perfect signature? Optimal signatures should be consistent within individuals and distinctive between individuals. In defense against avian brood parasitism, some host species have evolved "signatures" of identity on their eggs, comprising interindividual variation in color and pattern. Tawny-flanked prinia (Prinia subflava) egg signatures facilitate recognition and rejection of parasitic cuckoo finch (Anomalospiza imberbis) eggs. Here, we show that consistency and distinctiveness of patterns are negatively correlated in prinia eggs, perhaps because non-random, repeatable pattern generation mechanisms increase consistency but limit distinctiveness. We hypothesize that pattern properties which are repeatable within individuals but random between individuals ("invariant properties") allow hosts to circumvent this trade-off. To find invariant properties, we develop a method to quantify entire egg phenotypes from images taken from different perspectives. We find that marking scale (a fine-grained measure of size), but not marking orientation or position, is an invariant property in prinias. Hosts should therefore use differences in marking scale in egg recognition, but instead field experiments show that these differences do not predict rejection of conspecific eggs by prinias. Overall, we show that invariant properties allow consistency and distinctiveness to coexist, yet receiver behavior is not optimally tuned to make use of this information.

Visual complexity of egg patterns predicts egg rejection according to Weber's law.

Visual complexity is ubiquitous in nature. Drivers of complexity include selection in coevolutionary arms races between antagonists. However, the causes and consequences of biological complexity and its perception are largely understudied, partly because complexity is difficult to quantify. Here, we address this by studying egg pattern complexity and its perception in hosts (tawny-flanked prinia Prinia subflava), which visually recognize and reject mimetic eggs of their virulent brood parasite (cuckoo finch Anomalospiza imberbis). Using field data and an optimization algorithm, we compute a complexity metric which predicts rejection of experimentally placed conspecific eggs in prinia nests. Real cuckoo finch eggs exhibit significantly lower pattern complexity than prinia eggs, suggesting that high complexity benefits hosts because it distinguishes host eggs from parasitic eggs. We show that prinias perceive complexity differences according to Weber's law of proportional processing (i.e. relative, rather than absolute, differences between stimuli are processed in discrimination, such that two eggs with simple patterns are more easily discriminable than two with complex patterns). This may influence coevolutionary trajectories of hosts and parasites. The new methods presented for quantifying complexity and its perception can help us to understand selection pressures driving the evolution of complexity and its consequences for species interactions.