Evolutionary Biology of Hearing

For well over 100 years, investigators have pondered questions regarding the evolutionary origin of the vertebrate ear and about how the ear evolved from its most primitive form to that found in modern mammals. The earliest ideas for the origin of the ear, called the acousticolateralis hypothesis, suggested that the ear evolved from the lateral line (reviewed in Popper et al., 1992). A variety of studies suggested a series of evolutionary changes from the primitive ear to that of modern mammals (see van Bergeijk, 1967). More recent investigators, and particularly those using modern anatomical and physiological methods, now suggest that while the ear and lateral line may share a common ancestor, these are two distinct systems that are unrelated in terms of one giving rise to the other (see Popper et al., 1992). Moreover, we now know that regions of the ear evolved multiple times in the course of vertebrate history, much as very similar ears evolved multiple times in the evolution of invertebrates (e.g., Hoy, 1992; Popper and Fay, 1997; Fay and Popper, 2000, Christensen-Dalsgaard and Carr, 2008).

The diversity of ear structures and auditory systems among vertebrates is extraordinarily large, and very few data are available even now that help us answer questions related to the evolution of the auditory system. At the same time, it is likely that we may learn more about evolution of sensory systems from studying the auditory system than from any other sensory system. The reason for this is simple. There is a potential wealth of information about evolutionary changes in the ear lying in the fossil record - something that is not available for any other vertebrate sensory system (e.g., Clack, 2012). Moreover, the comparative material available for each of the different levels of the vertebrate auditory system (from periphery to CNS) is far richer than for any other sensory system. In essence, the very fact that the ear may have evolved multiple times (see Fritzsch, 2014) provides a rich body of comparative data upon which to evaluate evolution of the ear.

Unique and important information about the basic mechanisms of hearing come from research on diverse species. Often specific questions regarding human auditory function can be approached and answered by selecting a species for study that allow exploration of the auditory system in ways that are not easy to accomplish in humans. Clearly, the science of hearing and auditory neuroscience has benefited greatly from the comparative approach and from viewing animals in the context of their evolutionary relationships.

Some examples of basic research in non-mammalian species that have driven the field include:

  1. 1. The study of nucleus laminaris in birds has improved understanding of sound localization in mammals, and helps explain how and why localization of low-frequency sounds is not easy for patients with a single cochlear implant (see Middlebrooks et al., 2005).
  2. 2. The finding that interrupted or altered auditory feedback slows the degradation of birdsong leaves no doubt about the importance of auditory feedback in speech production (see Mooney, 2004).
  3. 3. The finding that hair cells regenerate in birds opened the possibility that hair cells can be made to regenerate in mammals (reviews in Meyer & Corwin 2008; Oesterle & Stone 2008).Studies on turtles, frogs, and birds have formed the basis for understanding the biophysics of hair cells because their hair cells survived more easily in vitro than mammalian hair cells (reviewed in Hudspeth 2014).
  4. 4. Studies on turtles, frogs, and birds have formed the basis for understanding the biophysics of hair cells because their hair cells survived more easily in vitro than mammalian hair cells (reviewed in Hudspeth 2014).
  5. 5. Mice and zebrafish are the major models for studying the genetics of hearing loss (e.g., Shalit & Avraham 2008).
  6. 6. Studies of mice have shown acceleration of age-related hearing loss by early noise exposure (Kujawa and Lieberman, 2006).

Studies of comparative and evolutionary biology of hearing at UMD

Our training program is a joint effort of 17 Core Faculty (Table 2) from four departments in three colleges at UMD and a Core Faculty member from the University of Maryland School of Medicine, Baltimore. Our faculty share a common research interest in hearing as well as a common interest in the insights derived from comparative hearing and the evolution of hearing. Our research questions range from the cellular and molecular structure of the ear to aging in the auditory system. Our labs use experimental approaches that range from molecular biology to psychoacoustics to imaging. Organisms studied include insects, fish, amphibians, reptiles, birds, non-human mammals, and humans. The breadth of experimental approaches and subjects, combined with a common interest among investigators in comparative evolutionary issues, provides opportunities for research training at the graduate and postdoctoral levels that, we believe, exists nowhere else. We combine our research training with outstanding professional training in the hearing sciences.

The major goal of our program is to produce auditory neuroscientists who understand the diversity of hearing mechanisms and the evolution of the auditory system so that they are able to identify appropriate models to ask questions of fundamental importance central to the function of the auditory system in health and in disease. Examples include understanding of hair cell repair and regeneration using fish and birds; (e.g., Dooling and Hertzano labs); understanding mechanisms of sound source localization (Carr, Goupell and MacLeod labs); new views of cortical plasticity and function (Kanold, Fritz and Shamma), and exploring aging in the auditory system (e.g., Gordon-Salant, Anderson and Kuchinsky). Our theme of the comparative and evolutionary biology of hearing follows naturally from the work of our Core Faculty.

Our location in the greater Washington DC area provides unique training opportunities for our students through collaborations with investigators in other programs and groups. The most important of these for our students involves collaborations with NIDCD, University of Maryland Baltimore, the Walter Reed National Military Medical Center, and Children’s National Medical Center in DC. Of particular importance is our relationship with NIDCD, where a number of intramural faculty are adjunct professors in the NACS program. This partnership fosters close collaborative research training opportunities for doctoral and postdoctoral students that involve strong interactions between co-mentors at both institutions. The collaboration also provides significant additional opportunities for training of doctoral and postdoctoral students in areas of greatest strength at NIDCD, including molecular biology, cellular biology, and communication disorders. The NIDCD faculty open their labs for specialized training and research opportunities for trainees who are doing their primary work at UMD, and may also serve as co-mentors for these students. UMD faculty reciprocate and open their labs to NIDCD trainees from programs other than UMD.