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One of the most intriguing questions in evolution is how organisms exhibit suitable phenotypic variation to rapidly adapt in novel selective environments. Such variability is crucial for evolvability, but poorly understood. In particular, how can natural selection favour developmental organisations that facilitate adaptive evolution in previously unseen environments? Such a capacity suggests foresight that is incompatible with the short-sighted concept of natural selection. A potential resolution is provided by the idea that evolution may discover and exploit information not only about the particular phenotypes selected in the past, but their underlying structural regularities: new phenotypes, with the same underlying regularities, but novel particulars, may then be useful in new environments. If true, we still need to understand the conditions in which natural selection will discover such deep regularities rather than exploiting ‘quick fixes’ (i.e., fixes that provide adaptive phenotypes in the short term, but limit future evolvability). Here we argue that the ability of evolution to discover such regularities is formally analogous to learning principles, familiar in humans and machines, that enable generalisation from past experience. Conversely, natural selection that fails to enhance evolvability is directly analogous to the learning problem of over-fitting and the subsequent failure to generalise. We support the conclusion that evolving systems and learning systems are different instantiations of the same algorithmic principles by showing that existing results from the learning domain can be transferred to the evolution domain. Specifically, we show that conditions that alleviate over-fitting in learning systems successfully predict which biological conditions (e.g., environmental variation, regularity, noise or a pressure for developmental simplicity) enhance evolvability. This equivalence provides access to a well-developed theoretical framework from learning theory that enables a characterisation of the general conditions for the evolution of evolvability., Author summary A striking feature of evolving organisms is their ability to acquire novel characteristics that help them adapt in new environments. The origin and the conditions of such ability remain elusive and is a long-standing question in evolutionary biology. Recent theory suggests that organisms can evolve designs that help them generate novel features that are more likely to be beneficial. Specifically, this is possible when the environments that organisms are exposed to share common regularities. However, the organisms develop robust designs that tend to produce what had been selected in the past and might be inflexible for future environments. The resolution comes from a recent theory introduced by Watson and Szathmáry that suggests a deep analogy between learning and evolution. Accordingly, here we utilise learning theory to explain the conditions that lead to more evolvable designs. We successfully demonstrate this by equating evolvability to the way humans and machines generalise to previously-unseen situations. Specifically, we show that the same conditions that enhance generalisation in learning systems have biological analogues and help us understand why environmental noise and the reproductive and maintenance costs of gene-regulatory connections can lead to more evolvable designs.

Adaptive plasticity allows organisms to cope with environmental change, thereby increasing the population’s long-term fitness. However, individual selection can only compare the fitness of individuals within each generation: if the environment changes more slowly than the generation time (i.e., a coarse-grained environment) a population will not experience selection for plasticity even if it is adaptive in the long-term. How does adaptive plasticity then evolve? One explanation is that, if competing alleles conferring different degrees of plasticity persist across multiple environments, natural selection between genetic lineages could select for adaptive plasticity (lineage selection). We show that adaptive plasticity can evolve even in the absence of such lineage selection. Instead, we propose that adaptive plasticity in coarse-grained environments evolves as a by-product of inefficient short-term natural selection: populations that rapidly evolve their phenotypes in response to selective pressures follow short-term optima, with the result that they have reduced long-term fitness across environments. Conversely, populations that accumulate limited genetic change within each environment evolve long-term adaptive plasticity even when plasticity incurs short-term costs. These results remain qualitatively similar regardless of whether we decrease the efficiency of natural selection by increasing the rate of environmental change or decreasing mutation rate, demonstrating that both factors act via the same mechanism. We demonstrate how this mechanism can be understood through the concept of learning rate. Our work shows how plastic responses that are costly in the short term, yet adaptive in the long term, can evolve as a by-product of inefficient short-term selection, without selection for plasticity at either the individual or lineage level., Author summary Organisms respond to different environments by changing how they act, look or function. When these responses improve the chances of survival, we call them adaptive plasticity. But observing adaptive plasticity does not prove that the response evolved because it improved survival. Being plastic is only selected for if individuals experience environmental variation, so that in slow changing environments plasticity may be selected against even if it is adaptive in the long term. Can adaptive plastic responses still evolve under these conditions? Yes. We use learning theory to describe how genetic changes accumulate when individual lifespan is shorter than the time between environmental changes, and show that adaptively plastic responses can evolve even when they are selected against. This is because adaptive plastic responses can evolve as the by-product of selection for different functions in different environments, as long as organisms retain some plasticity until the next environmental change. Our work demonstrates that evolution can reach general solutions even when each individual is only presented with a simple fraction of a more complex problem. This intuition could explain why plastic responses to past environments can be adaptive even to environments the entire lineage has never seen before.