Convergence of specialised behaviour, eye movements and visual optics in the sandlance (Teleostei) and the chameleon (Reptilia)

Abstract

Chameleons have a number of unusual, highly specialised visual features, including telescopic visual optics with a reduced lens power, wide separation of the eye's nodal point from the axis of rotation, a deep-pit fovea, rapid pre-calculated strikes for prey based on monocular depth judgements (including focus), and a complex pattern of partially independent alternating eye movements. The same set of features has been acquired independently by a teleost, the sandlance Limnichthyes fasciatus. Despite its underwater lifestyle, this fish displays visual behaviour and rapid strikes for prey that are remarkably similar to those of the chameleon [1]. In a direct comparison of the two species, we have revealed other, previously unsuspected, similarities, such as corneal accommodation, which was unknown in teleosts, as well as bringing together, for the first time, data collected from both species. The sandlance is the only teleost, among thousands studied, that has corneal refraction, corneal accommodation and reduced lens power, as well as sharing the other specialised optical features seen in chameleons. The independent eye movement pattern in the sandlance is also unusual and similar to that of the chameleon. The selection pressures that have produced this remarkable example of convergence may relate to common visual constraints in the life styles of these two phylogenetically disparate species.

Visual resolution and contrast sensitivity in two benthic sharks

“…Our findings support the existence of a monocularly organised oculomotor system in sharks (Maxwell, 1920;Masseck and Hoffmann, 2008). Monocular organisation is more common in animals with laterally positioned eyes as described for some teleost fishes [sandlance, Lymnichthyes fasciatus, and pipefish, Corythoichthyes intestinalis (Fritsches and Marshall, 2002;Pettigrew et al, 1999)] and the chameleon, Chamaleo chamaleo (Gioanni et al, 1993;Pettigrew et al, 1999). The contralateral placement of the medial rectus motor neurons in the midbrain of sharks differs from most vertebrates, which may allow eye movements to be controlled independently (Graf and Brunken, 1984).…”

Dichoptic Viewing Methods for Binocular Rivalry Research: Prospects for Large-Scale Clinical and Genetic Studies

“…With two independently controlled CCD (charged-couple device) cameras connected, this 'Virtual Chameleon' device enabled two independent (dichoptic) monocular views to be shown on the HMD, thus inducing BR. Such non-conjugate (unyoked) eye movements in humans are analogous to the independent alternating eye movements that have been observed in the chameleon and sandlance (Pettigrew et al, 1999). Indeed, this observation in the sandlance formed part of the basis for proposing a novel neural model of BR (see Ngo et al, 2013).…”

Eye movements in chameleons are not truly independent – evidence from simultaneous monocular tracking of two targets

“…Fritsches and Marshall, 2002;Pettigrew et al, 1999) and birds in which the system allows switching between eye movement patterns.…”

“…In primates, eye movements are conjugate, resulting in the precise alignment of targets on the two foveas, whereas in fish and birds, eye movements are frequently disconjugate. Such differences raise central questions as to the ocular control systems that might govern monocularity, binocularity and the switch from one to the other (von Helmholtz, 1896, cited in Pettigrew et al, 1999 andOtt, 2001). Studies of non-mammalian vertebrates (fish, amphibians, reptiles and birds) suggest that the basic organization of the oculomotor control system is monocular, with separate motor commands to each eye (Kirmse, 1988;Wallman and Pettigrew, 1985;Walls, 1962).…”