Visual ecology of the Australian lungfish (Neoceratodus forsteri)

Visual ecology of the Australian lungfish (Neoceratodus forsteri)

Authors: Nathan S Hart, Helena J Bailes, Misha Vorobyev, N Justin Marshall & Shaun P Collin

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Abstract

Background: The transition from water to land was a key event in the evolution of vertebrates

that occurred over a period of 15–20 million years towards the end of the Devonian. Tetrapods,

including all land-living vertebrates, are thought to have evolved from lobe-finned (sarcopterygian)

fish that developed adaptations for an amphibious existence. However, while many of the

biomechanical and physiological modifications necessary to achieve this feat have been studied in

detail, little is known about the sensory adaptations accompanying this transition. In this study, we

investigated the visual system and visual ecology of the Australian lungfish Neoceratodus forsteri,

which is the most primitive of all the lungfish and possibly the closest living relative to the ancestors

of tetrapods.

Results: Juvenile Neoceratodus have five spectrally distinct retinal visual pigments. A single type of

rod photoreceptor contains a visual pigment with a wavelength of maximum absorbance (λmax) at

540 nm. Four spectrally distinct single cone photoreceptors contain visual pigments with λmax at

366 (UVS), 479 (SWS), 558 (MWS) and 623 nm (LWS). No double cones were found. Adult lungfish

do not possess UVS cones and, unlike juveniles, have ocular media that prevent ultraviolet light

from reaching the retina. Yellow ellipsoidal/paraboloidal pigments in the MWS cones and red oil

droplets in the LWS cones narrow the spectral sensitivity functions of these photoreceptors and

shift their peak sensitivity to 584 nm and 656 nm, respectively. Modelling of the effects of these

intracellular spectral filters on the photoreceptor colour space of Neoceratodus suggests that they

enhance their ability to discriminate objects, such as plants and other lungfishes, on the basis of

colour.

Conclusion: The presence of a complex colour vision system based on multiple cone types and

intracellular spectral filters in lungfishes suggests that many of the ocular characteristics seen in

terrestrial or secondarily aquatic vertebrates, such as birds and turtles, may have evolved in shallow

water prior to the transition onto land. Moreover, the benefits of spectral filters for colour

discrimination apply equally to purely aquatic species as well as semi-aquatic and terrestrial animals.

The visual system of the Australian lungfish resembles that of terrestrial vertebrates far more

closely than that of other sarcopterygian fish. This supports the idea that lungfishes, and not the

coelacanth, are the closest living relatives of the ancestors of tetrapods.