Behavioral evidence for cone-based ultraviolet vision in divergent bat species and implications for its evolution

Xuan Fujun,Sun Yi,Zhu Tengteng,Racey Paul,Hu Kailiang,Wang Xuzhong

doi:10.1590/s1984-46702012000200002

Abstract

We investigated the reactions of four bat species from four different lineages to UV light: Hipposideros armiger (Hodgson, 1835) and Scotophilus kuhlii Leach, 1821, which use constant frequency (CF) or frequency modulation (FM) echolocation, respectively; and Rousettus leschenaultii (Desmarest, 1820) and Cynopterus sphinx (Vahl, 1797), cave and tree-roosting Old World fruit bats, respectively. Following acclimation and training involving aversive stimuli when exposed to UV light, individuals of S. kuhlii and C. sphinx exposed to such stimuli displayed conditioned reflexes such as body crouching, wing retracting, horizontal crawling, flying and/or vocalization, whereas individuals of H. armiger and R. leschenaultii, in most cue-testing sessions, remained still on receiving the stimuli. Our behavioral study provides direct evidence for the diversity of cone-based UV vision in the order Chiroptera and further supports our earlier postulate that, due to possible sensory tradeoffs and roosting ecology, defects in the short wavelength opsin genes have resulted in loss of UV vision in CF bats, but not in FM bats. In addition, Old World fruit bats roosting in caves have lost UV vision, but those roosting in trees have not. Bats are thus the third mammalian taxon to retain ancestral cone-based UV sensitivity in some species.

Highlights

Vision is fundamentally important in the animal kingdom, for example in mate choice, communication, and foraging
We investigated the reactions of four bat species from four different lineages to UV light: Hipposideros armiger (Hodgson, 1835) and Scotophilus kuhlii Leach, 1821, which use constant frequency (CF) or frequency modulation (FM) echolocation, respectively; and Rousettus leschenaultii (Desmarest, 1820) and Cynopterus sphinx (Vahl, 1797), cave and tree-roosting Old World fruit bats, respectively
Based on the coevolved theory of vision and hearing of bats (SPEAKMAN 2001, ZHAO et al 2009), the possible evolutionary sensory tradeoffs between shortwave vision and echolocation and changes in roosting ecology are consistent with the results of examination of S opsin among 28 species of bats from these four lineages using immunohistochemistry (MULLER & PEICHL 2005, 2006, MULLER et al 2007, KIM et al 2008, FELLER et al 2009), though the exact spectral tuning of S opsin cannot be directly established

Summary

Introduction

Vision is fundamentally important in the animal kingdom, for example in mate choice, communication, and foraging. WINTER et al (2003) suggested that the possible rod-modulation (beta-band) mechanism for UV light perception in the bats’ eye was still unknown while for other mammals it remained a possibility Because their retinas typically contain only a relatively small population of cones (ca 3% in bats with laryngeal echolocation, even less than 0.5% in Old World fruit bats, MULLER & PEICHL 2005, 2006, MULLER et al 2007, KIM et al 2008), it is difficult to study the nature of cone-based vision in nocturnal mammals (JACOBS et al 2001). The results will indicate the diversity of cone-based UV vision in the order Chiroptera and provide further insight into the evolutionary history of visual capacities of diverse bat species

Methods

Results

Conclusion