Award Abstract # 1754332
Collaborative Research: Evolution of long-distance communication in vocal rodents

NSF Org: IOS
Division Of Integrative Organismal Systems
Recipient: MIDWESTERN UNIVERSITY
Initial Amendment Date: July 25, 2018
Latest Amendment Date: July 25, 2018
Award Number: 1754332
Award Instrument: Standard Grant
Program Manager: Jodie Jawor
jjawor@nsf.gov
 (703)292-7887
IOS
 Division Of Integrative Organismal Systems
BIO
 Directorate for Biological Sciences
Start Date: August 1, 2018
End Date: July 31, 2023 (Estimated)
Total Intended Award Amount: $193,774.00
Total Awarded Amount to Date: $193,774.00
Funds Obligated to Date: FY 2018 = $193,774.00
History of Investigator:
  • Tobias Riede (Principal Investigator)
    triede@midwestern.edu
Recipient Sponsored Research Office: Midwestern University
555 31ST ST
DOWNERS GROVE
IL  US  60515-1235
(630)515-6396
Sponsor Congressional District: 06
Primary Place of Performance: Midwestern University
19555 N 59th Ave
Glendale
AZ  US  85308-6813
Primary Place of Performance
Congressional District:
08
Unique Entity Identifier (UEI): XD93A5U66T24
Parent UEI:
NSF Program(s): Animal Behavior
Primary Program Source: 01001819DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s):
Program Element Code(s): 765900
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

Vocal communication is fundamental to the fabric of social life. Animals produce a wide variety of sounds to mediate critical interactions, including advertisement to potential mates and competitors. But why and how do distinct species sound different and what factors contribute to such differences? The widespread importance of acoustic signals in mate recognition and speciation requires a deeper understanding of the causes and consequences of signal divergence. In this project, the physiological mechanisms underlying sound production across an ecologically diverse group of vocal rodents will be studied. The researchers will test the hypothesis that changes in sound production mechanisms are mediated by variation in social organization and spacing. These studies promise to provide important insights into the evolutionary interplay between the physiology of senders, receivers, and their socio-spatial ecologies. The proposal provides training opportunities for a postdoctoral scholar, research technician, and student participants who are underrepresented in science, technology, engineering, and mathematical sciences. In addition, the work develops inquiry-based learning modules that equip middle school classrooms with animals, microphones, and sound analysis software to foster critical thinking skills. The research will be supplemented with outreach at regional events and virtual live streaming of experiments in an indoor animal-tracking arena to allow the public to engage in scientific discovery. Digital audio, video, and morphological specimens will be permanently archived for open access in public repositories.

A central challenge in the study of behavior is connecting functional and mechanistic explanations for the evolution of complex phenotypes. Advertisement vocalizations used in reproductive contexts are among the most diverse and elaborate displays in the animal kingdom, yet understanding of the physiological mechanisms driving acoustic divergence is lacking. The goal of the proposed research is to integrate functional and mechanistic perspectives in senders, receivers, and the environment to understand the evolution of acoustic signals in relation to variation in social organization. Rodents represent over 40% of mammalian diversity and exhibit extreme variation in social structure and space use, even among closely related species. Investigators will leverage the exceptional divergence in social organization and acoustic behavior found in one clade to dissect the sound production mechanisms underlying signal diversification. The work integrates approaches from the field, laboratory, and mesocosm, including high-resolution acoustic recordings and laryngeal morphometrics, auditory electrophysiology, sound propagation experiments, and animal tracking studies to evaluate the socio-spatial context of vocal production. The findings will provide a rich dataset to investigate the evolution of communication systems in relation to variation in social organization, with broad implications for other taxa across all signaling modalities.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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Tobias Riede, Anastasiya Kobrina "Mechanisms of sound production in deer mice (Peromyscus spp.)" Journal of experimental biology , v.225 , 2022 https://doi.org/https://doi.org/10.1242/jeb.243695 Citation Details
Borgard, Heather L and Baab, Karen and Pasch, Bret and Riede, Tobias "The Shape of Sound: a Geometric Morphometrics Approach to Laryngeal Functional Morphology" Journal of Mammalian Evolution , 2019 10.1007/s10914-019-09466-9 Citation Details
Bottasso-Arias, N. and Burra, K. and Sinner, D. and Riede, T. "Disruption of BMP4 signaling is associated with laryngeal birth defects in a mouse model" Developmental Biology , v.500 , 2023 https://doi.org/10.1016/j.ydbio.2023.04.007 Citation Details
Darwaiz, T. and Pasch, B. and Riede, T. "Postnatal remodeling of the laryngeal airway removes body size dependency of spectral features for ultrasonic whistling in laboratory mice" Journal of Zoology , 2022 https://doi.org/10.1111/jzo.13003 Citation Details
Kobrina, Anastasiya and Hidau, Mahendra Kumar and Riede, Tobias and Guthrie, O'neil W. and Pasch, Bret "Agerelated and noiseinduced hearing loss alters grasshopper mouse (Onychomys) vocalizations" Hearing Research , v.404 , 2021 https://doi.org/10.1016/j.heares.2021.108210 Citation Details
Marcela Fernández-Vargas, Tobias Riede "Mechanisms and constraints underlying acoustic variation in rodents" Animal behaviour , v.184 , 2022 https://doi.org/10.1016/j.anbehav.2021.07.011 Citation Details
Riede, Tobias and Coyne, Megan and Tafoya, Blake and Baab, Karen L. "Postnatal Development of the Mouse Larynx: Negative Allometry, Age-Dependent Shape Changes, Morphological Integration, and a Size-Dependent Spectral Feature" Journal of Speech, Language, and Hearing Research , v.63 , 2020 https://doi.org/10.1044/2020_JSLHR-20-00070 Citation Details
Riede, Tobias and Pasch, Bret "Pygmy mouse songs reveal anatomical innovations underlying acoustic signal elaboration in rodents" The Journal of Experimental Biology , 2020 10.1242/jeb.223925 Citation Details
Riede, Tobias and Schaefer, Charles and Stein, Amy "Role of deep breaths in ultrasonic vocal production of Sprague-Dawley rats" Journal of Neurophysiology , v.123 , 2020 10.1152/jn.00590.2019 Citation Details

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

Intellectual Merit

A key challenge in studying social behavior is understanding how it is produced and its evolutionary function. Advertisement vocalizations, especially those used in reproductive contexts, are among the most varied and elaborate displays in the animal kingdom. However, the mechanisms behind these acoustic signals remain poorly understood.

One effective approach is to study model systems, such as rodents, where behaviors could be observed in laboratory settings. By comparing species, researchers could identify evolutionary and developmental features shared with other mammals, including primates.

Rodents comprise over 40% of mammalian species and exhibit significant diversity in social structures, even among closely related species. In this study, we focused on a group of cricetid rodents to investigate the sound production mechanisms behind their varied vocal behaviors. Specifically, we examined species from the Neotominae subfamily, which exhibited diverse vocalizations, from loud, long-distance calls to higher-frequency, lower-amplitude sounds used in close-range interactions.

Understanding how vocal production evolved in relation to ecological needs was crucial. Our findings showed that vocal fold vibrations for long-distance communication are common in Reithrodontomys, Onychomys, and Peromyscus, but a whistle mechanism is used in Baiomys. These differences in vocal production mechanisms contributed to acoustic variation and communication distances. Based on this finding, we suggested that the most recent common ancestor of the Neotominae group likely possessed the ability to produce both types of vocalizations. While Reithrodontomyini and Baiomyini use different mechanisms for long-distance calls, these differences likely contributed to varying communication ranges. The structural diversity of laryngeal morphology and vocal folds in the Neotominae subfamily, along with similarities to human speech production, make cricetid rodents a promising model for exploring the relationship between vocal fold structure and function.

Broader Impact

The Principal Investigator (PI) recruited and trained a diverse group of veterinary and medical students (including four women) and three research associates (all women) in behavioral and anatomical research methods. This training included developing critical thinking and problem-solving skills, which will be valuable in any future career they pursue. These individuals played key roles in research collaborations that contributed to the scientific findings reported above.

During the COVID-19 pandemic, when campus laboratories were closed, the PI and students continued their work through virtual meetings, maintaining engagement and progress.

The PI and lab members presented their findings at local, national, and international conferences and published them in peer-reviewed journals. Students and research associates were included as co-authors in these publications.

Additionally, the PI collaborated with researchers from other institutions to further investigate the value of nontraditional rodent models for studying the human voice.

 


Last Modified: 12/17/2024
Modified by: Tobias Riede

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