Abstract

Reciprocal coevolutionary changes in predation and anti-predator behaviours have long been hypothesized, but evolutionary-scale evidence is rare. Here, we reconstructed the evolutionary-scale changes in the diel activity patterns of a predator-prey system (carnivorous and herbivorous mammals) based on a molecular phyloecological approach, providing evidence of long-term antagonistic coevolutionary changes in their diel activities. Our molecular reconstruction of diel activity patterns, which is supported by morphological evidence, consistently showed that carnivorous mammals were subjected to a shift from diurnality to nocturnality, while herbivorous mammals experienced a shift from nocturnality to diurnality during their evolutionary histories. A shift in the diel activity of the herbivores as a result of carnivore avoidance is hypothesized based on molecular, morphological and behavioural evidence, and our results suggest an evolutionary-scale arms race of diel activity shifts between carnivorous and herbivorous mammals.

Highlights

  • Interactions between carnivorous and herbivorous mammals, representing one of the classic coevolutionary systems, lead to long-term reciprocal evolutionary changes in predation and anti-predator behaviours[1]

  • To test the antagonistic coevolution hypothesis of the evolution of diel activity between carnivores and ungulates, in the present study, we used this molecular phyloecological approach and employed both restricted models (PAML)[15] and unrestricted models (BUSTED, branch site-random effects likelihood (BS-REL))[16,17] to identify intensified selection of bright-light vision genes and dim-light vision genes involved in the cone/rod phototransduction pathway[18,19,20] along various branches of carnivorous mammals and ungulates, in the context of the Laurasiatheria phylogeny (Figs 1 and 2, Supplementary Table S1)

  • To determine the diel activity patterns of ancestral carnivores, we analysed the adaptive evolution of 33 phototransduction genes along the ancestral carnivore branch using PAML, branch site-unrestricted statistical test for episodic diversification (BUSTED) and BSREAL

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Summary

Introduction

Interactions between carnivorous and herbivorous mammals, representing one of the classic coevolutionary systems, lead to long-term reciprocal evolutionary changes in predation and anti-predator behaviours[1]. To test the antagonistic coevolution hypothesis of the evolution of diel activity between carnivores and ungulates, in the present study, we used this molecular phyloecological approach and employed both restricted models (PAML)[15] and unrestricted models (BUSTED, BS-REL)[16,17] to identify intensified selection of bright-light vision genes and dim-light vision genes involved in the cone/rod phototransduction pathway[18,19,20] along various branches of carnivorous mammals and ungulates, in the context of the Laurasiatheria phylogeny (Figs 1 and 2, Supplementary Table S1) This approach enabled us to track the long-term evolutionary changes in the diel activity patterns of carnivorous and herbivorous mammals for the first time. Our study supports the long-term antagonistic coevolution of temporal partitioning between carnivorous and herbivorous mammals

Methods
Results
Conclusion

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