Abstract
The degree to which molecular and morphological loss of function occurs synchronously during the vestigialization of traits is not well understood. The mammalian vomeronasal system, a sense critical for mediating many social and reproductive behaviors, is highly conserved across mammals. New World Leaf-nosed bats (Phyllostomidae) are under strong selection to maintain a functional vomeronasal system such that most phyllostomids possess a distinct vomeronasal organ and an intact TRPC2, a gene encoding a protein primarily involved in vomeronasal sensory neuron signal transduction. Recent genetic evidence, however, shows that TRPC2 is a pseudogene in some Caribbean nectarivorous phyllostomids. The loss-of-function mutations suggest the sensory neural tissue of the vomeronasal organ is absent in these species despite strong selection on this gene in its mainland relatives, but the anatomy was unknown in most Caribbean nectarivorous phyllostomids until this study. We used diffusible iodine-based contrast-enhanced computed tomography (diceCT) to test whether the vomeronasal and main olfactory anatomy of several phyllostomid species matched genetic evidence of function, providing insight into whether loss of a structure is linked to pseudogenization of a molecular component of the system. The vomeronasal organ is indeed rudimentary or absent in species with a disrupted TRPC2 gene. Caribbean nectar-feeders also exhibit derived olfactory turbinal morphology and a large olfactory recess that differs from closely related bats that have an intact vomeronasal organ, which may hint that the main olfactory system may compensate for loss. We emphasize non-invasive diceCT is capable of detecting the vomeronasal organ, providing a feasible approach for quantifying mammalian chemosensory anatomy across species.
Highlights
Vestigial structures are commonly observed across animals, but the molecular and morphological underpinnings of the process of trait loss through time is not well understood (Fong et al, 1995; Lahti et al, 2009)
The vomeronasal organ is clearly visible in the diffusible iodine-based contrast-enhanced computed tomography (diceCT) scans of Artibeus jamaicensis (Figures 2A, 3A)
The vomeronasal epithelium and lumen can be distinguished in diceCT scans
Summary
Vestigial structures are commonly observed across animals, but the molecular and morphological underpinnings of the process of trait loss through time is not well understood (Fong et al, 1995; Lahti et al, 2009). Selection may be relaxed on senses that no longer contribute to fitness, and sensory organs may become vestigial (Fong et al, 1995). Comparative analyses of the molecular and morphological components of sensory systems can clarify these mechanisms of relaxed selection, as they provide insight into when shifts in selection may have occurred. We integrated molecular and morphological evidence for loss of function, connecting the process of pseudogenization of genes and vestigialization of morphology
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