Evolutionary Mechanisms Of Echolocation And Aggressive Calls In Bats

Acoustic signals mediate a variety of life history events in animals,including resource competition,mate selection and anti-predator defense.It is therefore proposed that acoustic signals play a major role in the maintenance of stability of animal population and community.Why vocalizing animals evolved diverse acoustic signals has been a hot topic in ecology and evolutionary biology,given that understanding the basis of this pattern has far-reaching implications for phenotype evolution and speciation.Echolocating bats are highly specialized mammals that exploit ecological niches at night sky,providing an ideal model for bioacoustic research.In addition to the use of echolocation calls for spatial orientation and foraging,echolocating bats employ aggressive calls to engage in intraspecific competition for food and space resources.Here,we aim to elucidate the evolutionary mechanisms of echolocation and aggressive calls,two common vocalizations given by echolocating bats.We investigated the evolutionary mechanisms underlying echolocation calls among 438 bat species from 19 families worldwide,including Emballonuridae,Craseonycteridae,Rhinopomatidae,Megadermatidae,Nycteridae,Rhinolophidae,Hipposideridae,Myzopodidae,Thypopteridae,Furipteridae,Natalidae,Mystacinidae,Noctilionidae,Mormoopidae,Phyllostomidae,Molossidae,Miniopteridae,Vespertilionidae and Cistugida.Phylogenetic comparative analysis revealed that echolocation call duration was tightly linked to forearm length and phylogenetic components,but was weakly linked to forging niches and climatic factors.Peak frequency was significantly associated with forearm length,foraging niches and phylogenetic components,but was poorly associated with diet and climatic factors.Similarly,call structure was matched to foraging niches and phylogenetic components but not matched to other predictor factors.Based on random forest models,forearm length explained 13.68 — 35.47% of the variation in echolocation call parameters,ecological factors explained 32.31 — 50.70% of the variation,and phylogenetic components explained 47.17 — 68.02% of the variation.Path analyses detected that phylogenetic components determined echolocation call output not only by their direct effects on acoustic parameters,but also by having indirect effects via foraging niches and body size.We repeated the analyses while controlling for body-size effect,removing missing data,using estimated call parameters and alternative phylogenetic tree,each yielding the similar results.We explored the evolutionary mechanisms behind aggressive calls among 31 bat species from Emballonuridae,Rhinolophidae,Hipposideridae,Miniopteridae and Vespertilionidae in China.Analyses showed that the commonly aggressive callsemitted by bats were low-frequency broadband noises.Phylogenetic comparative analysis,combined with linear mixed model,identified that aggressive call duration correlated closely with forearm length and phylogenetic components,but weakly with forging niches and climatic factors.Frequency parameters of aggressive calls(i.e.,peak frequency,minimum frequency and maximum frequency)were tightly linked to forearm length,colony size and phylogenetic components,but were weakly linked to foraging niches and climatic factors.Colony size and phylogenetic components imposed considerable effects on call bandwidth.By contrast,forearm length,foraging niches and climatic factors had no marked effects on call bandwidth.According to hierarchical partitioning algorithm,forearm length accounted for 18.46 — 40.90% of the variance in aggressive call parameters,colony size accounted for 9.85—33.56% of the variance,and phylogenetic components accounted for 4.54 — 22.94% of the variance.We found consistent results after controlling for body-size effect and using alternative phylogenetic components.Using the call dataset spanning 31 bat species above,we assessed the evolutionary mechanisms underpinning echolocation and aggressive calls within a comparative framework.Phylogenetic comparative analysis and linear mixed model suggested that both vocalizations were constrained by forearm length and phylogenetic components.Principal components of echolocation calls were predicted by foraging niches but not by climatic factors and colony size.Principal component of aggressive calls,however,was predicted by colony size but not by foraging niches and climatic factors.According to hierarchical partitioning algorithm,forearm length explained 10.40 — 16.22% of the variation in echolocation call components,and explained 30.49% of the variation in aggressive call component.Foraging niches accounted for 15.33 — 33.27% of the variation in echolocation call components,and phylogenetic components accounted for 38.90—50.02% of the variation.Colony size accounted for 21.54% of the variance in aggressive call component,whereas phylogenetic components accounted for 8.11% of the variance.There were similar results after correcting for body size and using alternative phylogenetic components.Together,these results indicate that:(1)ecological selection,phylogenetic constraint and morphological constraint mold the evolution of bat echolocation calls;(2)phylogeny determines the evolution of bat echolocation calls via multiple,direct and indirect paths;(3)social selection,phylogenetic constraint and morphological constraint are largely responsible for the evolution of bat aggressive calls.Our fingdings demonstrate the adaptive response of bat acoustic signals to foraging niches and social pressures,which expands our knowledge on the emergence of call diversity in nocturnal mammals.This study constitutes the first case to disentangle direct and indirect phylogenetic effects on bat echolocation calls,and to explore the evolutionary mechanisms underlying aggressive calls in bats.We establish a diagnostic frameworkfor testing evolutionary mechanisms of animal vocalizations,laying the basis for further work in other animal taxa.We compile an unprecedented data set that may be applied to assess the sensitivity of bats in response to environmental change,providing a theoretical guide to assign conservation priorities for bat species.