Abstract
Although signal characteristics and sensory systems are predicted to co-evolve according to environmental constraints, this hypothesis has not been tested for acoustic signalling across a wide range of species, or any mammal sensory modality. Here we use phylogenetic comparative techniques to show that mammal vocal characteristics and hearing sensitivity have co-evolved to utilise higher frequencies in forest environments – opposite to the general prediction that lower frequencies should be favoured in acoustically cluttered habitats. We also reveal an evolutionary trade-off between high frequency hearing sensitivity and the production of calls with high frequency acoustic energy that suggests forest mammals further optimise vocal communication according to their high frequency hearing sensitivity. Our results provide clear evidence of adaptive signal and sensory system coevolution. They also emphasize how constraints imposed by the signalling environment can jointly shape vocal signal structure and auditory systems, potentially driving acoustic diversity and reproductive isolation.
Highlights
Signal characteristics and sensory systems are predicted to co-evolve according to environmental constraints, this hypothesis has not been tested for acoustic signalling across a wide range of species, or any mammal sensory modality
Relative high frequency hearing sensitivity was significantly higher for forest mammals than those living in other terrestrial environments (PGLMM: effective sample size (ESS) = 1199, H2 = 0.75, β = −5.82, Credible Interval (CI) = −10.63 to −1.17, PMCMC = 0.021) (Fig. 3b) and negatively correlated to log[10] functional head size (PGLMM: β = −18.97, CI = −27.06 to −10.98, PMCMC < 0.001) (Supplementary Table 5)
We revealed that poorer high frequency hearing sensitivity was predictive of shallower spectral slopes in forest mammal vocalisations
Summary
Signal characteristics and sensory systems are predicted to co-evolve according to environmental constraints, this hypothesis has not been tested for acoustic signalling across a wide range of species, or any mammal sensory modality. Selection could favour high frequency hearing sensitivity for optimal sound localisation in dense forests with poor visibility, for avoiding predation and localising prey, which would help to counteract the attenuation of higher frequencies that occurs in forest environments[16,17,18] and facilitate more effective vocal communication. The latter contention is plausible because functionally relevant information is often encoded across a wide frequency range in vocalisations, and not just limited to the lower, or lowest frequencies with the most acoustic energy. The dimensions and tissue properties of the supra-laryngeal vocal tract (which comprises the pharyngeal, oral and nasal cavities) determine the formant frequency values and bandwidth in the call spectra[19]
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