Sensing, communication, navigation, decision-making, memory and learning are key components in a standard cognitive tool-kit that enhance an animal's ability to successfully survive and reproduce. However, these tools are not only useful for, or accessible to, animals-they evolved long ago in simpler organisms using mechanisms which may be either unique or widely conserved across diverse taxa. In this article, I review the recent research that demonstrates these key cognitive abilities in the plasmodial slime mould Physarum polycephalum, which has emerged as a model for non-animal cognition. I discuss the benefits and limitations of comparisons drawn between neural and non-neural systems, and the implications of common mechanisms across wide taxonomic divisions. I conclude by discussing future avenues of research that will draw the most benefit from a closer integration of Physarum and animal cognition research. 

/pdf/thoughts-from-the-forest-floor-a-review-of-cognition-in-the-3crjnrkb.pdf

Thoughts from the forest floor: a review of cognition in the slime mould Physarum polycephalum

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.

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

The persistence of imperfect mimicry in nature presents a challenge to mimicry theory. Some hypotheses for the existence of imperfect mimicry make differing predictions depending on how mimetic fidelity is measured. Here, we measure mimetic fidelity in a brood parasite–host system using both trait-based and response-based measures of mimetic fidelity. Cuckoo finches Anomalospiza imberbis lay imperfectly mimetic eggs that lack the fine scribbling characteristic of eggs of the tawny-flanked prinia Prinia subflava, a common host species. A trait-based discriminant analysis based on Minkowski functionals—that use geometric and topological morphometric methods related to egg pattern shape and coverage—reflects this consistent difference between host and parasite eggs. These methods could be applied to quantify other phenotypes including stripes and waved patterns. Furthermore, by painting scribbles onto cuckoo finch eggs and testing their rate of rejection compared to control eggs (i.e. a response-based approach to quantify mimetic fidelity), we show that prinias do not discriminate between eggs based on the absence of scribbles. Overall, our results support relaxed selection on cuckoo finches to mimic scribbles, since prinias do not respond differently to eggs with and without scribbles, despite the existence of this consistent trait difference.

Combined measures of mimetic fidelity explain imperfect mimicry in a brood parasite–host system

Most mimicry systems involve imperfect mimicry, whereas perfect and high-fidelity mimicry are rare. When the fidelity of mimicry is high, mimics might be expected to have the upper hand against their antagonists. However, in coevolving systems, diversification of model phenotypes may provide an evolutionary escape, because mimics cannot simultaneously match all model individuals in the population. Here we investigate high-fidelity mimicry in a highly specialized, Afrotropical brood parasite–host system: the African cuckoo and fork-tailed drongo. Specifically, we test whether host egg polymorphisms are an effective defence against such mimicry. We show, using a combination of image analysis, field experiments and simulations, that: (1) egg colour and pattern mimicry of fork-tailed drongo eggs by African cuckoos is near-perfect on average; (2) drongos show fine-tuned rejection of foreign eggs, exploiting unpredictable pattern differences between parasitic eggs and their own; and (3) the high degree of interclutch variation (polymorphic egg ‘signatures’) exhibited by drongos gives them the upper hand in the arms race, with 93.7% of cuckoo eggs predicted to be rejected, despite cuckoos mimicking the full range of drongo egg phenotypes. These results demonstrate that model diversification is a highly effective defence against mimics, even when mimicry is highly accurate.

When perfection isn't enough: host egg signatures are an effective defence against high-fidelity African cuckoo mimicry

During mate choice, receivers often assess the magnitude (duration, size, etc.) of signals that vary along a continuum and reflect variation in signaller quality. It is generally assumed that receivers assess this variation linearly, meaning each difference in signalling trait between signallers results in a commensurate change in receiver response. However, increasing evidence shows receivers can respond to signals non-linearly, for example through Weber's Law of proportional processing, where discrimination between stimuli is based on proportional, rather than absolute, differences in magnitude. We quantified mate preferences of female green swordtail fish, Xiphophorus hellerii, for pairs of males differing in body size. Preferences for larger males were better predicted by the proportional difference between males (proportional processing) than the absolute difference (linear processing). This demonstration of proportional processing of a visual signal implies that receiver perception may be an important mechanism selecting against the evolution of ever-larger signalling traits.

https://onlinelibrary.wiley.com/doi/pdfdirect/10.1111/ele.14179

Proportional processing of a visual mate choice signal in the green swordtail, Xiphophorus hellerii.

Abstract 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. 

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

Abstract 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. 

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

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

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

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