Semicircular canals shed light on bottleneck events in the evolution of the Neanderthal clade

Abstract

Revealing the evolutionary processes which resulted in the derived morphologies that characterize the Neanderthal clade has been an important task for paleoanthropologists. One critical method to quantify evolutionary changes in the morphology of hominin populations is through evaluating morphological phenotypic diversity (i.e., disparity) in phylogenetically informative bones as a close proxy to neutral evolutionary processes. The goal of this study is to quantify the degree of disparity in the Neanderthal clade. We hypothesize that a reduction in bony labyrinth disparity is indicative of the underlying genetic variation resulting from bottleneck events. We apply a deformation-based geometric morphometric approach to investigate semicircular canal and vestibule shape of a chronologically broad sample of individuals belonging to the Neanderthal lineage. Our results identify a significant reduction in disparity after the start of Marine Isotope Stage 5 supporting our hypothesis of a late bottleneck, possibly leading to the derived morphology of Late Pleistocene Neanderthals.

Fig. 1. Summary of individuals included in the analyses.

a The geographical and chronological range of the Neanderthal clade individuals and modern humans included in the analysis. The symbols correspond to the n of individuals from each site and are colored as follows: blue = Sima de los Huesos; purple = Krapina; green = late Neanderthals; orange = modern humans. Orange ellipses correspond to the approximated geographical range of the extant modern human assemblage. Age estimates of fossil specimens are provided in Table 1. Background satellite image was downloaded from © Mapbox, © OpenStreetMap, © Maxar and rescaled to fit to figure panel size. b–e Three-dimensional models of the left semicircular canal and vestibule of selected individuals for the four groups considered in the present study.

Fig. 2. Scenarios of phenetic variation along the evolution of the Neanderthal clade.

a Scenario #1: no occurrence of bottleneck events; b Scenario #2: occurrence of an early bottleneck event between Sima de lo Huesos and Krapina populations; c Scenario #3: occurrence of a late bottleneck event after population of Krapina and before late Neanderthals; d Scenario #4: occurrence of both an early and late bottleneck events. The horizontal line is a schematic representation of time with earlier occurring groups on the left and later occurring ones on the right. The thickness of the horizontal bars corresponds to the suggested phenetic variation. Colors are coded as follows: blue = Sima de los Huesos; purple = Krapina; green = late Neanderthals.

Fig. 3. Bivariate scatterplots of a principal component analysis performed on the deformation-fields (raw shape data) obtained from the diffeomorphometric analysis of semicircular canals.

a PC2 vs. PC1; b PC4 vs. PC3. The variance explained by each PC is given within parentheses. 95% confidence ellispes, symbols, and c–f group average shapes (in posterolateral and posteromedial views) are color-coded based on group membership: blue = Sima de los Huesos; purple = Krapina; green = late Neanderthals; orange = modern humans. Source data for this figure can be reproduced using the code and files provided in Supplementary Code 1 and Supplementary Data 3.

Fig. 4. Shape and size differences.

Frequency plots of morphological variance (a) and disparity (b) for each group in the semicircular canal shape space. Bootstrapped group distributions (20,000 bootstraps) were computed based on PC1-19 scores (86.7% of variance) to account for the small number of available specimens for fossil groups. The solid lines represent density curves of the frequencies for morphological variance and disparity values between all possible pairs of individuals within each bootstrapped group. The vertical axis represents the frequency of a given disparity or variance value obtained from the bootstrapping of the sample. Vertical dashed lines correspond to group averages for morphological variance and disparity. c Line plot of pair-wise Euclidean distances for the bootstrapped group distribution (20,000 bootstraps). The solid line corresponds to the second and third quartile; dashed lines represent first and fourth quartiles; black dot shows median of the distribution. d Natural logarithm (ln) of the centroid size of semicircular canals for the individuals included in the analysis. Classic Neanderthals display the largest size variation together with modern humans. Color coding as in Figs. 1 and 3. Source data for this figure can be reproduced using the code and files provided in Supplementary Code 1 and Supplementary Data 3.