Research Article

Echolocation in soft-furred tree mice

See allHide authors and affiliations

Science  18 Jun 2021:
Vol. 372, Issue 6548, eaay1513
DOI: 10.1126/science.aay1513

You are currently viewing the abstract.

View Full Text

Log in to view the full text

Log in through your institution

Log in through your institution

New echolocator

Echolocation is a well demonstrated convergent sensory mode in bats and toothed whales. These lineages are not closely related, and this sense might be more broadly distributed than we recognize. Using a suite of approaches, He et al. show that the lineage of soft-furred tree mice (genus Typhlomys) includes multiple echolocators. Clear evidence of the behavioral use of echolocation under fully dark conditions was supported by the convergence of ear bone morphology and hearing-related genes with other echolocating mammals.

Science, aay1513, this issue p. eaay1513

Structured Abstract

INTRODUCTION

Echolocation is a form of orientation behavior in which some animals can assess environments in which vision is ineffective. Echolocating mammals have been recognized for decades, including microbats and toothed whales. Recently, the Chapa soft-furred tree mouse (Typhlomys chapensis) of the rodent family Platacanthomyidae was suggested to echolocate but this was not practically evidenced. There are three other recognized species in the soft-furred tree mice genus (Typhlomys) that share similar ecological and morphological traits, suggesting that echolocation may be a general trait within this genus. In this study, we performed behavioral, morphological, genomic, and functional analyses to test whether echolocation is present across the four species of soft-furred tree mice.

RATIONALE

Echolocation occurs when emitted sonic signals are compared with received signals to facilitate orientation and object identification. This adaptive trait is expected to be reflected at the behavioral, morphological, and molecular levels of the organism. To test whether soft-furred tree mice generally have evolved echolocation, we conducted multiple behavioral experiments to assess the performance of different species in detecting and avoiding obstacles dependent on hearing and examined the anatomical structures of their vocal and hearing apparatus. We further investigated genome-wide convergence in hearing-related genes and the functional convergence of a well-documented echolocation-related gene, prestin, between the soft-furred tree mouse and other known echolocating mammals.

RESULTS

All four recognized soft-furred tree mouse species were capable of emitting regular ultrasonic vocalizations (USVs) with a peak frequency of ~98 kHz. When these mice explored in a cluttered environment and approached an obstacle, they produced USVs with a significantly larger pulse rate. In tests for echolocation, the soft-furred tree mice spent a longer time exploring and emitted more sonic pulses in the sector of the central disk over the escaping platform, consequently dropping to the platform. When their ears were plugged, they lost the preference for the over-platform sector, as shown by exploration time and emitting pluses, and could not land on the platform. The above preference was regained when the earplugs were removed or a plastic tube was inserted into the ear canals. The stylohyal bone fuses with the tympanic bone in soft-furred tree mice, which is an anatomic characteristic previously exclusively observed in laryngeally echolocating bats. By sequencing a high-quality genome of the soft-furred tree mouse, we found a significant genome-wide convergence in hearing-related genes with other echolocating mammals, including the well-documented echolocation-related gene prestin. In vitro experimental analyses also showed a functional convergence of prestin between the soft-furred tree mouse and other echolocating mammals, which was largely contributed by the identified convergent amino acids.

CONCLUSION

Our findings from behavioral experiments, anatomical structures, evolutionary genomics, and gene functional analyses provide strong evidence that soft-furred tree mice are a new echolocating lineage within mammals. The discovery of this echolocating rodent genus suggests that echolocation may be an underappreciated trait in mammals. The genome-wide convergent evolution in hearing-related genes implicates a similar molecular mechanism underlying the origination or elaboration of this complex adaptive phenotype.

Multiple lines of evidence for echolocation in soft-furred tree mice (Typhlomys).

When the soft-furred tree mice explored on a central disk, they spent more time exploring and emitted ultrasonic pulses at a higher rate in the sector over the escaping platform. The stylohyal bone fuses with the tympanic bone in soft-furred tree mice, which was previously observed exclusively in laryngeally echolocating bats. Significant molecular convergence in hearing-related genes and functional convergence of the well-documented echolocation-related gene prestin were found between the soft-furred tree mouse and known echolocating mammals.

Abstract

Echolocation is the use of reflected sound to sense features of the environment. Here, we show that soft-furred tree mice (Typhlomys) echolocate based on multiple independent lines of evidence. Behavioral experiments show that these mice can locate and avoid obstacles in darkness using hearing and ultrasonic pulses. The proximal portion of their stylohyal bone fuses with the tympanic bone, a form previously only seen in laryngeally echolocating bats. Further, we found convergence of hearing-related genes across the genome and of the echolocation-related gene prestin between soft-furred tree mice and echolocating mammals. Together, our findings suggest that soft-furred tree mice are capable of echolocation, and thus are a new lineage of echolocating mammals.

View Full Text

Stay Connected to Science