The influence of photoreceptor size and distribution on optical sensitivity in the eyes of lanternfishes (Myctophidae)

Fanny de Busserolles; John L Fitzpatrick; N Justin Marshall; Shaun P Collin

doi:10.1371/journal.pone.0099957

The influence of photoreceptor size and distribution on optical sensitivity in the eyes of lanternfishes (Myctophidae)

PLoS One. 2014 Jun 13;9(6):e99957. doi: 10.1371/journal.pone.0099957. eCollection 2014.

Authors

Fanny de Busserolles¹, John L Fitzpatrick², N Justin Marshall³, Shaun P Collin⁴

Affiliations

¹ The School of Animal Biology and The UWA Oceans Institute, The University of Western Australia, Crawley, Australia; Red Sea Research Centre, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia.
² Centre for Evolutionary Biology, School of Animal Biology, The University of Western Australia, Crawley, Australia; Computational and Evolutionary Biology, Faculty of Life Sciences, University of Manchester, Manchester, United Kingdom.
³ Sensory Neurobiology Group, Queensland Brain Institute, University of Queensland, Brisbane, Australia.
⁴ The School of Animal Biology and The UWA Oceans Institute, The University of Western Australia, Crawley, Australia.

Abstract

The mesopelagic zone of the deep-sea (200-1000 m) is characterised by exponentially diminishing levels of downwelling sunlight and by the predominance of bioluminescence emissions. The ability of mesopelagic organisms to detect and behaviourally react to downwelling sunlight and/or bioluminescence will depend on the visual task and ultimately on the eyes and their capacity for detecting low levels of illumination and intermittent point sources of bioluminescent light. In this study, we investigate the diversity of the visual system of the lanternfish (Myctophidae). We focus specifically on the photoreceptor cells by examining their size, arrangement, topographic distribution and contribution to optical sensitivity in 53 different species from 18 genera. We also examine the influence(s) of both phylogeny and ecology on these photoreceptor variables using phylogenetic comparative analyses in order to understand the constraints placed on the visual systems of this large group of mesopelagic fishes at the first stage of retinal processing. We report great diversity in the visual system of the Myctophidae at the level of the photoreceptors. Photoreceptor distribution reveals clear interspecific differences in visual specialisations (areas of high rod photoreceptor density), indicating potential interspecific differences in interactions with prey, predators and/or mates. A great diversity in photoreceptor design (length and diameter) and density is also present. Overall, the myctophid eye is very sensitive compared to other teleosts and each species seems to be specialised for the detection of a specific signal (downwelling light or bioluminescence), potentially reflecting different visual demands for survival. Phylogenetic comparative analyses highlight several relationships between photoreceptor characteristics and the ecological variables tested (depth distribution and luminous tissue patterns). Depth distribution at night was a significant factor in most of the models tested, indicating that vision at night is of great importance for lanternfishes and may drive the evolution of their photoreceptor design.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Eye / metabolism*
Fishes / metabolism*
Photoreceptor Cells / metabolism*

Grants and funding

This work was funded by the Australian Research Council (Discovery grant to SPC, the Deep-Australia Linkage Grant to NJM and SPC, and a Postdoctoral Fellowship to JLF) and the West Australian State Government (SPC). FdB was supported by a Scholarship for International Research Fees (SIRF) and a University International Stipend (UIS) at the University of Western Australia. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.