Deep evolutionary roots of strepsirrhine primate labyrinthine morphology

Abstract

The cavity system of the inner ear of mammals is a complex three-dimensional structure that houses the organs of equilibrium and hearing. Morphological variation of the inner ear across mammals reflects differences in locomotor behaviour and hearing performance, and the good preservation of this structure in many fossil specimens permits analogous inferences. However, it is less well known to what extent the morphology of the bony labyrinth conveys information about the evolutionary history of primate taxa. We studied this question in strepsirrhine primates with the aim to assess the potential and limitations of using the inner ear as a phylogenetic marker. Geometric morphometric analysis showed that the labyrinthine morphology of extant strepsirrhines contains a mixed locomotor, allometric and phylogenetic signal. Discriminant analysis at the family level confirmed that labyrinthine shape is a good taxonomic marker. Our results support the hypothesis that evolutionary change in labyrinthine morphology is adequately described with a random walk model, i.e. random phenotypic dispersal in morphospace. Under this hypothesis, average shapes calculated for each node of the phylogenetic tree give an estimate of inner ear shapes of the respective last common ancestors (LCAs), and this information can be used to infer character state polarity. The labyrinthine morphology of the fossil Adapinae is close to the inferred basal morphology of the strepsirrhines. The inner ear of Daubentonia, one of the most derived extant strepsirrhines, is autapomorphic in many respects, but also presents unique similarities with adapine labyrinths.

Fig. 1

Landmarks used for geometric morphometric analysis of the bony labyrinth (specimen: Lepilemur ruficaudatus AIM-11054). Grey arrows: anteromedial-to-posterolateral and anterolateral-to-posteromedial directions used to define landmark locations 3–4, 12–14, 16 and 22. The superior-to-inferior direction was used to define landmark locations 5–6, 17–18, 20–21 (see Table 1). Grey line: a simplified version of the medial axis.

Fig. 2

Correlations between molecular distances and corresponding phenetic distances. (A) Graph of size-corrected cranial shape distance vs. molecular distance. (B) Graph of size-corrected bony labyrinth shape distance vs. molecular distance. Black squares: strepsirrhine intra-familial distances; Diamonds: lemuroid inter-familial distances (Cheirogaleidae, Lepilemuridae, Lemuridae and Indriidae). Y: lorisiform inter-familial distance (Lorisidae–Galagidae). Open circles: lemuriform–lorisiform inter-familial distances. Crosses: distances between Daubentonia and Lemuroidea families. Stars: inter-familial distances between strepsirrhines and anthropoids. Red squares: other inter- and intra-familial distances involving at least one non-strepsirrhine taxon. Black regression lines are for strepsirrhine taxa only, red regression lines for all analyzed taxa (see Table S2 for regression summaries).

Fig. 3

Phenetic trees based on inner ear morphology (average labyrinthine shape of taxa). (A) NJ tree reflecting bony labyrinth morphological affinities (size-corrected shape distances) between strepsirrhine families, fossil Adapinae, Tarsius, anthropoids, Scandentia and Dermoptera. (B) UPGMA tree reflecting bony labyrinth morphological affinities (size-corrected shape distances) between strepsirrhine families, fossil Adapinae, Tarsius, anthropoids, Scandentia and Dermoptera. Bootstrap values for 1000 resamplings are given at each node. Lemuroidea families (Cheirogaleidae, Lepilemuridae, Lemuridae and Indriidae) are nested together in both trees, as well as the Lorisiformes (Galagidae and Lorisidae).

Fig. 4

Left bony labyrinth of Daubentonia madagascariensis (A) and Palaeolemur betillei (B). Labyrinths are oriented in superior (left) and lateral (right) views (by convention, the lateral semicircular canal is positioned horizontally). Arrows: in both species, the ampullar part of the posterior canal is fused with the medial part of the lateral canal. Specimens: AIM-ZU AS-1843 (Daubentonia) and Bor-613 (Palaeolemur). Scale bar: 1 mm.

Fig. 5

Principal components analysis (PCA) of labyrinthine shape variation. (A) Graphing the first two components of shape space, PC1 and PC2, shows a common pattern of size-related shape variation (grey arrow approximately parallel to PC1), and major differences in shape between Malagasy primates and lorisiform primates (along PC2). Downward-pointing triangles: Cheirogaleidea; upward-pointing triangles: Lemuroidea; +: Daubentoniidae; X: Galagidae; Y: Lorisidae; stars: Adapinae; Z: Tarsiidae; Red vertical rectangles: Cebidae; Red horizontal rectangles: Cercopithecidae; Red squares: Hominidae; Orange diamonds: Scandentia; Orange circles: Dermoptera. (B) Patterns of labyrinthine shape variation associated with PC1 and PC2, respectively.

Fig. 6

Left bony labyrinths of Cynocephalus volans and Tupaia tana. Arrows: Cynocephalus, as well as extant primates, exhibits a straight superior canal, whereas Tupaia exhibits a curved superior canal. Specimens: AIM-ZU AS-1904 (Cynocephalus) and AIM-ZU 10591 (Tupaia). Scale bar: 1 mm.