The hidden anatomy of paranasal sinuses reveals biogeographically distinct morphotypes in the nine-banded armadillo ( Dasypus novemcinctus)

Abstract

Background

With their Pan-American distribution, long-nosed armadillos (genus Dasypus) constitute an understudied model for Neotropical biogeography. This genus currently comprises seven recognized species, the nine-banded armadillo ( D. novemcinctus) having the widest distribution ranging from Northern Argentina to the South-Eastern US. With their broad diversity of habitats, nine-banded armadillos provide a useful model to explore the effects of climatic and biogeographic events on morphological diversity at a continental scale.

Methods

Based on a sample of 136 skulls of Dasypus spp. belonging to six species, including 112 specimens identified as D. novemcinctus, we studied the diversity and pattern of variation of paranasal cavities, which were reconstructed virtually using µCT-scanning or observed through bone transparency.

Results

Our qualitative analyses of paranasal sinuses and recesses successfully retrieved a taxonomic differentiation between the traditional species D. kappleri, D. pilosus and D. novemcinctus but failed to recover diagnostic features between the disputed and morphologically similar D. septemcinctus and D. hybridus. Most interestingly, the high variation detected in our large sample of D. novemcinctus showed a clear geographical patterning, with the recognition of three well-separated morphotypes: one ranging from North and Central America and parts of northern South America west of the Andes, one distributed across the Amazonian Basin and central South America, and one restricted to the Guiana Shield.

Discussion

The question as to whether these paranasal morphotypes may represent previously unrecognized species is to be evaluated through a thorough revision of the Dasypus species complex integrating molecular and morphological data. Remarkably, our recognition of a distinct morphotype in the Guiana Shield area is congruent with the recent discovery of a divergent mitogenomic lineage in French Guiana. The inflation of the second medialmost pair of caudal frontal sinuses constitutes an unexpected morphological diagnostic feature for this potentially distinct species. Our results demonstrate the benefits of studying overlooked internal morphological structures in supposedly cryptic species revealed by molecular data. It also illustrates the under-exploited potential of the highly variable paranasal sinuses of armadillos for systematic studies.