Abstract
Natural selection should favour generalist predators that outperform specialists across all prey types. Two genetic solutions could explain why intraspecific variation in predatory performance is, nonetheless, widespread: mutations beneficial on one prey type are costly on another (antagonistic pleiotropy), or mutational effects are prey-specific, which weakens selection, allowing variation to persist (relaxed selection). To understand the relative importance of these alternatives, we characterised natural variation in predatory performance in the microbial predator Dictyostelium discoideum. We found widespread nontransitive differences among strains in predatory success across different bacterial prey, which can facilitate stain coexistence in multi-prey environments. To understand the genetic basis, we developed methods for high throughput experimental evolution on different prey (REMI-seq). Most mutations (~77%) had prey-specific effects, with very few (~4%) showing antagonistic pleiotropy. This highlights the potential for prey-specific effects to dilute selection, which would inhibit the purging of variation and prevent the emergence of an optimal generalist predator.
Highlights
Natural selection should favour generalist predators that outperform specialists across all prey types
The success of a predator is determined by the efficiency with which it overcomes the various defences of its prey and converts different prey resources into fitness
Whilst REMI mutants and natural spontaneous mutations could potentially differ in their magnitude of effect, or even the extent of pleiotropy, we believe that the pattern we observe likely captures an important property of genetic architecture
Summary
Natural selection should favour generalist predators that outperform specialists across all prey types. Conditional neutrality can promote the persistence of variation and ecological specialisation because it results in the overall relaxed selection, which limits the degree to which selection purges deleterious mutations[21,22,23,24,25] The importance of this process will depend on the extent to which the availability of different prey types exhibits spatial and/or temporal variability, as this will determine the extent to which the influence of selection arising from each prey type is diluted. Our results support the idea that environmental heterogeneity and the conditional nature of the effects of mutations result in relatively weak selection on variation affecting performance on each prey These results are consistent with the idea that relaxed selection, rather than antagonistic pleiotropy associated with trade-offs, better explains how genetic variation in predatory traits is maintained, despite the potential for recurrent selection favouring superior predators
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