Inferring the Retinal Anatomy and Visual Capacities of Extinct Vertebrates
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Rowe, M.P. 2000. Inferring the Retinal Anatomy and Visual Capacities of Extinct Vertebrates. Palaeontologia Electronica, vol. 3, issue 1, art. 3: 43 pp., 4.9MB. http://palaeo-electronica.org/2000_1/retinal/issue1_00.htm Copyright: Society of Vertebrate Paleontologists, 15 April 2000 Submission: 18 November 1999, Acceptance: 2 February 2000 INFERRING THE RETINAL ANATOMY AND VISUAL CAPACITIES OF EXTINCT VERTEBRATES M.P. Rowe ABSTRACT One goal of contemporary paleontology is the resto- other terrestrial vertebrates because of the loss of ana- ration of extinct creatures with all the complexity of tomical specializations still retained by members of form, function, and interaction that characterize extant most all tetrapod lineages except eutherian mammals. animals of our direct experience. Toward that end, much Consequently, the largest barrier to understanding vision can be inferred about the visual capabilities of various in extinct animals is not necessarily the nonpreservation extinct animals based on the anatomy and molecular of relevant structures, but rather our deep and largely biology of their closest living relatives. In particular, unrecognized ignorance of visual function in modern confident deductions about color vision in extinct ani- animals. mals can be made by analyzing a small number of genes M.P.Rowe. Department of Psychology, University of in a variety of species. The evidence indicates that basal California, Santa Barbara, CA, 93106, USA. tetrapods had a color vision system that was in some ways more sophisticated than our own. Humans are in a KEY WORDS: eyes, photopigments, dinosaurs, per- poor position to understand the perceptual worlds of ception, color Palaeontologia Electronica—http://www-odp.tamu.edu/paleo 1 PLAIN LANGUAGE SUMMARY: We can deduce that extinct animals had particular (in animals that have them) probably sharpen the spec- soft tissues or behaviors via extant phylogenetic brack- tral tuning of photoreceptors and thus enhance per- eting (EPB, Witmer 1995). Application of EPB entails ceived color contrasts (Bowmaker et al. 1997). the recognition of two extant lineages that diverged ear- Eutherian mammals also lack double cones and the lier and later, respectively, from the extinct organisms' mosaics of these structures found in a variety of other lineage (Figure 1). Parsi- vertebrates (Walls 1942). Double cones and their mosa- mony indicates that a char- ics have been known for roughly 100 years, but no com- acter or character-state pelling theory explains the utility of such anatomical shared by each of two lin- arrangements. Comparative anatomy and EPB allow eages existed in their most reasonable inferences about which extinct animals had recent common ancestor double cones and mosaics, but these inferences do not (MRCA). Thus, unless sub- help us to understand these animals because we do not sequently lost in particular know how double cones are used by living animals. lineages, the character or state was also present in all Much of our perceptual world is built upon what our other descendants of the eyes report to us. Indeed, much of the primate cerebral MRCA including those whose extinction left no direct cortex is devoted to deciphering signals from the retina evidence of the character. The EPB method can be (Felleman and Van Essen 1991). However, the primate applied using DNA sequences as proxies for the pro- visual system evolved from one that was secondarily teins that those sequences encoded. Results of the search simplified from a more complex state (as indicated by for genes that code for opsins - the proteins that signal the apparent loss of oil droplets, double cones, and some the detection of light in retinal photoreceptors - suggest that the MRCA of the two major bony fish radiations opsins). Hence our visual worlds are probably very dif- had four different opsin genes (Bowmaker 1998). Many ferent from those of animals that never underwent this tetrapods retained all four genes whereas the basal euth- simplification. Psychologists have recognized for some erian mammals apparently retained only two (Jacobs time that what we perceive is a reconstruction of the 1993). By newly deriving a third opsin, our ancestors world around us. This reconstruction strongly depends endowed us with a color vision system approaching, but upon the characteristics of our sense organs. Biologists not equaling, the system probably retained by most are only beginning to appreciate the significance of this Mesozoic tetrapods. Many animals also have oil drop- insight when studying the behavior of other animals lets screening the light-sensitive parts of their photore- (Bennett, et al. 1994). Hopefully, paleobiologists will ceptors (Walls 1942). Again eutherian mammals are not lag behind neobiologists in reaching this under- aberrant in showing no trace of these structures which standing. INTRODUCTION As a historical science, paleontology readily presents of view and area of stereoscopic overlap can be deter- questions that cannot be answered via empirical meth- mined from physical measurements of its skull (Stevens ods. For instance, paleobiologists wishing to understand 1997, Coates 1998). Preservation of the lenses of trilo- how an extinct animal viewed its surroundings have bite eyes provides enough detail to indicate the acuity of infrequent access to tissues that mediated visual percep- their bearers' vision (Fordyce and Cronin 1989, Fordyce tion. Soft tissue preservation is a rare occurrence even and Cronin 1993), and a few cranial endocasts provide within the set of rare occurrences in which anything at detail on the relative sizes of different brain regions in all is preserved from an animal that lived long ago. skulls that have been particularly well preserved (e.g., Needless to say, even when fragments of fossilized soft Stensiö 1927 in Gould 1988; Rogers 1998; Brochu, per- tissue are found they are non-functional. sonal commun., 1999; and Paleoneurology: the Study of Brain Endocasts of Extinct Vertebrates on the Univer- On the other hand, the fossil record has been rela- sity of Wisconsin site Comparative Mammalian Brain tively generous to those pursuing answers to particular Collections). questions about perception. Farlow (1994) addressed questions about tyrannosaur lifestyle with simple geo- Here I follow a different approach. I wish to explore metrical considerations about the position of their eyes the visual capacities of extinct animals via extant phylo- relative to the ground. Similarly, an animal's total field genetic bracketing (EPB, Witmer, 1995) the method Palaeontologia Electronica—http://www-odp.tamu.edu/paleo 2 described in Figure 1. Whereas Witmer (1995) inferred biology and electrophysiology - have rendered other that Tyrannosaurus rex had eyeballs, I will go further parts of his treatise hopelessly inadequate. Relevant to out on the limb and infer what sorts of receptors it had the latter parts, I will here describe some of the newer within those eyeballs. data and its potential relevance to paleontology. I will Gordon Walls (1942) compiled much of what we also highlight some of the former areas where the rela- know about comparative visual anatomy in vertebrates tive paucity of newer information suggests we should be almost 60 years ago. In many areas Walls' treatise still focusing efforts to fill the holes in our understanding of represents the envelope of our knowledge, but revolu- organisms past and present. tions in some areas of science - particularly molecular FUNDAMENTALS OF VISION The production of a neural image of the light con- ated, the retinal is in a con- verging upon an animal figuration named 11-cis to begins with the focusing of denote the orientation of the that light onto a sheet of bonds around the eleventh receptors. Figure 2 depicts a carbon atom (Figure 5). generalized bird eye. In ter- When the chromophore restrial animals most of the absorbs a photon, an elec- focusing power of the eye is tronic rearrangement may occur, which results in a rota- at the air/cornea interface. In aquatic vertebrates the tion of the constituent atoms around the eleventh carbon refractive index of the cornea is similar to that of the bond. This isomerization of the chromophore causes a water in which it is immersed, and hence most of the change in the shape of the opsin, and in its new configu- focussing power is provided by the lens. In either case, ration, the opsin behaves as an enzyme. light impinging upon the eye from particular directions is redirected to particular locations on the retina, the tis- The rate at which the sue lining the inside of the eye. Within the retina are reaction catalyzed by the photoreceptors, cells specialized for transducing relative opsin occurs sets the rate at light intensities into neurochemical signals that can be which the photoreceptor passed along to the central nervous system. releases neurotransmitters to other retinal neurons. Figure 6 shows the absorption The Molecular Basis of Phototransduction probability of a typical ver- Figure 3 contains a draw- tebrate photopigment as a function of wavelength and, ing of a cross-section of a essentially, the absorption spectrum of a photoreceptor human retina showing the as well, since in most cases, all of the opsin molecules position and orientation of within a given photoreceptor are chemically identical. the photoreceptors. Figure 4 Neglecting some nuances diagrams the photoreceptor such as adaptation processes outer segments, where light (that are quite important for is absorbed and transduced visual function but are not in vertebrates. important for the arguments presented here) the rate at The outer segments con- which opsins are catalyzing sist of sets of disks stacked within a photoreceptor can like pancakes and con- be determined by integrating the product of the quantal structed of lipid bilayers. Embedded in the disk mem- flux through the photoreceptor's outer segment and the branes are large numbers of photopigment molecules. photopigment's absorption spectrum as shown in Figure Each photopigment consists of a chromophore 6B. covalently bound to a protein called an opsin.