Cochlear Labyrinth Volume in Euarchontoglirans: Implications for the Evolution of Hearing in Primates
Article first published online: 3 DEC 2010
Copyright © 2010 Wiley-Liss, Inc.
The Anatomical Record
Volume 294, Issue 2, pages 263–266, February 2011
How to Cite
Armstrong, S. D., Bloch, J. I., Houde, P. and Silcox, M. T. (2011), Cochlear Labyrinth Volume in Euarchontoglirans: Implications for the Evolution of Hearing in Primates. Anat Rec, 294: 263–266. doi: 10.1002/ar.21298
- Issue published online: 13 JAN 2011
- Article first published online: 3 DEC 2010
- Manuscript Accepted: 28 SEP 2010
- Manuscript Received: 15 MAR 2010
- NSF. Grant Numbers: BCS-0003920, BCS-0129601
- NSERC (Discovery Grants Program – Individual, USRA Grants Program)
- X-ray computed tomography;
Using high resolution X-ray computed tomography data we examined the relationship between cochlear labyrinth volume and body mass in extant, non-primate euarchontoglirans, and in two fossils, to allow for comparison with the results of Kirk and Gosselin-Ildari (2009). Modern primates have significantly higher cochlear labyrinth volumes relative to body mass than other euarchontoglirans, which may be related to a downward shift in the highest and lowest audible frequencies over the course of primate evolution, and to the relative increase in brain size observed in Euprimates. Anat Rec, 2011. © 2010 Wiley-Liss, Inc.
The cochlea is the organ for sound detection, located in the inner ear. It is divided by membranes into three chambers: the scala media, filled with endolymph, and the scala tympani and scala vestibuli, filled with perilymph (Kelly and Chen2009). A recent study by Kirk and Gosselin-Ildari (2009) used the close association that the cochlea forms with its bony labyrinth to measure the cochlear labyrinth volume from skeletal primate specimens using high resolution X-ray computed tomography (CT) data. That study provided evidence that some aspects of the hearing abilities of extinct organisms may be predicted based on cochlear labyrinth volume (see Coleman and Colbert,2010 for a comparable study using cochlear length). The authors did not examine cochlear labyrinth volume in non-primates, however, making it unclear whether the range of variation represented by primates is typical of other mammalian orders.
This study was undertaken to examine the relationship between cochlear labyrinth volume and body mass in three other orders (Scandentia, Dermoptera, and Rodentia) following the method outlined by Kirk and Gosselin-Ildari (2009). All three orders are members of Euarchontoglires, the supraordinal grouping to which primates belong (Murphy et al.,2001; Silcox et al.,2009, 2010; Fig. 1). As such, they may help to reconstruct the primitive anatomy of primates in phylogenetic context. In addition, two fossil specimens from the Late Paleocene (Clarkforkian) of Wyoming were examined: Labidolemur kayi (United States National Museum [USNM] 530208), thought to be a euarchontogliran non-primate (Silcox et al., 2010), and Carpolestes simpsoni (USNM 482354), a stem primate (Bloch and Silcox,2006; Bloch et al.,2007). See Table 1 for the list of species studied.
|Order||Species||Specimen number||Cochlear labyrinth volume (mm3)||Body mass (kg)a|
|Dermoptera||Galeopterus variegatus||USNM 255716||11.6||1.00|
|Cynocephalus volans||USNM 144660||14.5||1.50|
|Rodentia||Glaucomys volans||TMM M-6332||4.7||0.064|
|Idiurus macrotis||CM 69360||1.7||0.030|
|Idiurus zenkeri||LACM 53440||1.5||0.016|
|Sciurus vulgaris||CM 50361||5||0.363|
|Spermophilus beecheyi||CM 65167||6.4||0.600|
|Xerus rutilus||CM 85466||6.3||0.400|
|Scandentia||Ptilocercus lowii||USNM 481105||3.9||0.039|
|Apatotheria||Labidolemur kayib||USNM 530208||3.8||0.074|
|Primates||Carpolestes simpsonib||USNM 482354||2.4||0.100|
Measurements of the cochlear labyrinth volume were taken using high-resolution X-ray CT (μCT) scans of all the specimens, scanned on the OMNI-X high resolution X-ray CT scanner at the Center for quantitative imaging at Pennsylvania State University. These images were 16-bit unsigned data, with a resolution ranging between 0.012 and 0.05 mm (for both slice thickness and interpixel distance). All images containing the cochlear labyrinth were processed, beginning with the basilar gap or round window (whichever came first, depending on the species) to the last slice including the cochlear apex. Using ImageJ software (Rasband,1997–2009), the images were cropped and segmented according to the bounding lines outlined by Kirk and Gosselin-Ildari (2009). These included a line across the gap between the primary and secondary osseous spiral laminae (the basilar gap), and a line from the edge of the oval window, where the stapes is located, to the base of the primary osseous lamina. The modiolus was not included in the cochlear labyrinth volume. In this study, the air-filled space of the cochlear labyrinth was filled with a high threshold color in each slice. Once all slices were processed using this method, the segmented areas were measured using ImageJ, and the cochlear labyrinth volume was calculated by multiplying the areas by the slice thickness. This deviated slightly from the method of Kirk and Gosselin-Ildari (2009), but validation tests confirmed that the two methods produced closely comparable cochlear labyrinth volumes. The segmented slices were also stacked with strip2raw (unpublished DOS program developed by Nathan Jeffrey, University of Liverpool) and used to create a 3D reconstruction in Amira version 3.1.1 (Visage Imaging Inc., 2003; Fig. 2).
For data analysis, both cochlear labyrinth volumes and body mass were log10 transformed to account for the nonlinear, allometric relationship between these two variables (see Gingerich et al.,1982 for a discussion of the importance of using logarithms in studying allometric relationships). Pearson's correlations and linear regression analysis were used to test the association between cochlear labyrinth volume and body mass. Student's t-test was used to test for a statistically significant (α = 0.05) difference between primates and non-primates, for log10 cochlear volume scaled by log10 body mass. All statistical tests were performed using Microsoft Excel 2003.
Results and Discussion
In comparison to these closely related non-primates and to C. simpsoni, modern primates have significantly higher cochlear labyrinth volumes relative to body mass (P < 0.005; Fig. 3). This suggests that an upward shift in relative cochlear volume has occurred over the course of primate evolution. According to Kirk and Gosselin-Ildari (2009), increases in cochlear labyrinth volume may be related to downward shifts in the highest and lowest audible frequencies.
It appears from this small sample that closely related non-primates follow a trend of smaller cochlear labyrinths than living primates. Labidolemur kayi, a fossil specimen, currently classified as a non-primate euarchontogliran, and C. simpsoni, a stem primate, also have small cochleae relative to estimated body mass when compared to the primate distribution. The small cochlea of C. simpsoni is particularly interesting as it would imply that selection for larger cochlear labyrinths did not occur at the basal primate node, but rather may have happened within Euprimates (see also Coleman and Boyer,2008).
Evidence from other stem primates (Gingerich and Gunnell,2005; Silcox et al.,2009;2010) has demonstrated that the increased brain size characteristic of living primates relative to other mammalian orders also evolved within Euprimates, rather than at the basal primate node. Jerison's principle of proper mass, which states that “the mass of neural tissue controlling a particular function is appropriate to the amount of information processing involved in performing the function” (Jerison,1973: 8), would imply that an increase in cochlear labyrinth volume would also result in an increase in the brain tissue associated with the function of the cochlear labyrinth. Consequently, this apparent increase in cochlear volume in Euprimates may be one factor that led to the increase in brain size within the order, along with specializations to other sensory systems such as vision (Kirk,2006).
Kirk and Gosselin-Ildari (2009) concluded from their study that the highest and lowest audible frequencies shift downward as cochlear labyrinth volume increases among primates, as both the high and low frequency limits are significantly negatively correlated with cochlear labyrinth volume. In particular, cochlear labyrinth volume is strongly negatively correlated with the high frequency limit of hearing, even when body mass is held constant. If this is extrapolated to non-primates, then primates may have a lower range of hearing than closely related non-primates (see also Coleman and Boyer,2008), a hypothesis that will require testing with audiograms for the living non-primates. If confirmed, this change in the highest and lowest audible frequencies perceived by primates may have behavioral implications. Some primates use sound as one element in capturing insects; tarsiers, for example, have been known to catch prey with their eyes closed (Niemitz,1979). Here we show that the stem primate C. simpsoni, reconstructed as an omnivorous terminal branch forager (Biknevicius,1986; Bloch and Boyer,2002,2003), had a relatively small cochlear labyrinth volume compared to that of Euprimates (Kirk and Gosselin-Ildari,2009). It is possible that this apparent difference is associated with the evolution of specializations for prey-capture in early Eocene Euprimates. Alternatively, this difference could reflect parallel evolution of increasing cochlear size in multiple lineages of Euprimates, as suggested for increasing brain size (e.g., Kay et al.,2008).
All CT scanning was performed by Ö. Karacan or T. Ryan at the Center for Quantitative Imaging, Penn State University. Thanks to P. Gingerich for access to specimens. Thanks also to two anonymous reviewers, whose comments improved this article. This research was supported by NSF research grants BCS-0003920 (to A. Walker) and BCS-0129601 (to G. Gunnell, P. Gingerich, and JIB), an NSERC USRA grant to SA and an NSERC discovery grant to MTS.
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