Dataset Information

Echolocation call frequency variation in horseshoe bats: molecular basis revealed by comparative transcriptomics.

ABSTRACT: Recently diverged taxa with contrasting phenotypes offer opportunities for unravelling the genetic basis of phenotypic variation in nature. Horseshoe bats are a speciose group that exhibit a derived form of high-duty cycle echolocation in which the inner ear is finely tuned to echoes of the narrowband call frequency. Here, by focusing on three recently diverged subspecies of the intermediate horseshoe bat (Rhinolophus affinis) that display divergent echolocation call frequencies, we aim to identify candidate loci putatively involved in hearing frequency variation. We used de novo transcriptome sequencing of two mainland taxa (himalayanus and macrurus) and one island taxon (hainanus) to compare expression profiles of thousands of genes. By comparing taxa with divergent call frequencies (around 15 kHz difference), we identified 252 differentially expressed genes, of which six have been shown to be involved in hearing or deafness in human/mouse. To obtain further validation of these results, we applied quantitative reverse transcription-PCR to the candidate gene FBXL15 and found a broad association between the level of expression and call frequency across taxa. The genes identified here represent strong candidate loci associated with hearing frequency variation in bats.

SUBMITTER: Sun H

PROVIDER: S-EPMC7542777 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Publications

Echolocation call frequency variation in horseshoe bats: molecular basis revealed by comparative transcriptomics.

Sun Haijian H Chen Wenli W Wang Jiaying J Zhang Libiao L Rossiter Stephen J SJ Mao Xiuguang X

Proceedings. Biological sciences 20200909 1934

Recently diverged taxa with contrasting phenotypes offer opportunities for unravelling the genetic basis of phenotypic variation in nature. Horseshoe bats are a speciose group that exhibit a derived form of high-duty cycle echolocation in which the inner ear is finely tuned to echoes of the narrowband call frequency. Here, by focusing on three recently diverged subspecies of the intermediate horseshoe bat (<i>Rhinolophus affinis</i>) that display divergent echolocation call frequencies, we aim t ...[more]

PMID: 32900318

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Project description:All organisms have specialized systems to sense their environment. Most bat species use echolocation for navigation and foraging, but which and how ecological factors shaped echolocation call diversity remains unclear for the most diverse clades, including the adaptive radiation of neotropical leaf-nosed bats (Phyllostomidae). This is because phyllostomids emit low-intensity echolocation calls and many inhabit dense forests, leading to low representation in acoustic surveys. We present a field-collected, echolocation call dataset spanning 35 species and all phyllostomid dietary guilds. We analyze these data under a phylogenetic framework to test the hypothesis that echolocation call design and parameters are specialized for the acoustic demands of different diets, and investigate the contributions of phylogeny and body size to echolocation call diversity. We further link call parameters to dietary ecology by contrasting minimum detectable prey size estimates (MDPSE) across species. We find phylogeny and body size explain a substantial proportion of echolocation call parameter diversity, but most species can be correctly assigned to taxonomic (61%) or functional (77%) dietary guilds based on call parameters. This suggests a degree of acoustic ecological specialization, albeit with interspecific similarities in call structure. Theoretical MDPSE are greatest for omnivores and smallest for insectivores. Omnivores significantly differ from other dietary guilds in MDPSE when phylogeny is not considered, but there are no differences among taxonomic dietary guilds within a phylogenetic context. Similarly, predators of non-mobile/non-evasive prey and predators of mobile/evasive prey differ in estimated MDPSE when phylogeny is not considered. Phyllostomid echolocation call structure may be primarily specialized for overcoming acoustic challenges of foraging in dense habitats, and then secondarily specialized for the detection of food items according to functional dietary guilds. Our results give insight into the possible ecological mechanisms shaping the diversity of sensory systems, and their reciprocal influence on resource use.

Project description:BackgroundThe hyolaryngeal apparatus generates biosonar pulses in the laryngeally echolocating bats. The cartilage and muscles comprising the hyolarynx of laryngeally echolocating bats are morphologically modified compared to those of non-bat mammals, as represented by the hypertrophied intrinsic laryngeal muscle. Despite its crucial contribution to laryngeal echolocation, how the development of the hyolarynx in bats differs from that of other mammals is poorly documented. The genus Rhinolophus is one of the most sophisticated laryngeal echolocators, with the highest pulse frequency in bats. The present study provides the first detailed description of the three-dimensional anatomy and development of the skeleton, cartilage, muscle, and innervation patterns of the hyolaryngeal apparatus in two species of rhinolophid bats using micro-computed tomography images and serial tissue sections and compares them with those of laboratory mice. Furthermore, we measured the peak frequency of the echolocation pulse in active juvenile and adult individuals to correspond to echolocation pulses with hyolaryngeal morphology at each postnatal stage.ResultsWe found that the sagittal crests of the cricoid cartilage separated the dorsal cricoarytenoid muscle in horseshoe bats, indicating that this unique morphology may be required to reinforce the repeated closure movement of the glottis during biosonar pulse emission. We also found that the cricothyroid muscle is ventrally hypertrophied throughout ontogeny, and that the cranial laryngeal nerve has a novel branch supplying the hypertrophied region of this muscle. Our bioacoustic analyses revealed that the peak frequency shows negative allometry against skull growth, and that the volumetric growth of all laryngeal cartilages is correlated with the pulse peak frequency.ConclusionsThe unique patterns of muscle and innervation revealed in this study appear to have been obtained concomitantly with the acquisition of tracheal chambers in rhinolophids and hipposiderids, improving sound intensity during laryngeal echolocation. In addition, significant protrusion of the sagittal crest of the cricoid cartilage and the separated dorsal cricoarytenoid muscle may contribute to the sophisticated biosonar in this laryngeally echolocating lineage. Furthermore, our bioacoustic data suggested that the mineralization of these cartilages underpins the ontogeny of echolocation pulse generation. The results of the present study provide crucial insights into how the anatomy and development of the hyolaryngeal apparatus shape the acoustic diversity in bats.

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Dataset Information

Echolocation call frequency variation in horseshoe bats: molecular basis revealed by comparative transcriptomics.

Publications

Echolocation call frequency variation in horseshoe bats: molecular basis revealed by comparative transcriptomics.

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