Paleoneurology: a Sight for Four Eyes
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Current Biology Dispatches Paleoneurology: A Sight for Four Eyes Lawrence M. Witmer Department of Biomedical Sciences, Ohio University Heritage College of Osteopathic Medicine, Ohio Center for Ecology and Evolutionary Studies, Athens, OH 45701, USA Correspondence: [email protected] https://doi.org/10.1016/j.cub.2018.02.071 The ‘third eye’ of the pineal complex is a curious component of the vertebrate brain associated with light sensation and melatonin production. A fossil lizard with a ‘fourth eye’ now calls for a reinterpretation of pineal evolution. ‘‘The part of the body in which perhaps few people today subscribe to mediating circadian and seasonal rhythms the soul directly exercises its Descartes’ view of the pineal organ as the via production of the hormone melatonin functions is not the heart at all, or ‘seat of the soul’, it retains an almost [2]. The mammalian pineal organ is the whole of the brain. It is mystical quality in some quarters. Pop complicated enough, but when other rather.a certain very small gland cultural references abound, suggesting vertebrates are taken into account, we now [the pineal organ] situated in the ways (and selling products, of course) to speak of a ‘pineal complex’ involving middle of the brain’s substance.’’ ‘activate the pineal’ with cannabis or multiple organs that emphasize the Rene Descartes, The Passions of ‘harmonic sound wave technology’ to photosensory component. That is, they the Soul, 1649 [1] achieve enlightenment (psychedelic or often are ‘eyes’ with structures spiritual). Fortunately, there is also a rich comparable to the cornea, lens, retina, and It’s perhaps understandable that our scientific literature on the neuroscience visual pigments (opsins) that we typically knowledge of the function and evolution of and clinical neuroendocrinology of the associate with our normal, lateral eyes and the pineal organ has been murky, because, pineal gland, revealing that the organ may which breach the skull to appear on the top as Descartes noted, it is indeed a very have less to do with the soul and of the head [3,4]. In fact, when considering small structure buried deep within the brain enlightenment and more to do with the pineal complex of vertebrates we now of humans and other mammals. Although responding to light/dark cycles and need to distinguish between ‘lateral eyes’ Current Biology 28, R306–R327, April 2, 2018 ª 2018 Elsevier Ltd. R311 Current Biology Dispatches the parapineal gland. The kicker is that there is a huge diversity of extinct tetrapods (land vertebrates), such as the famous sail-backed Dimetrodon, that often show a single large midline parietal foramen in their skull roofs [9–11]. Is this ‘third eye’ opening for a parapineal (parietal) eye or a pineal eye? Both ideas have been proposed [10,12]. Enter Saniwa ensidens, the 49-million- year-old fossil lizard that sparked Smith and colleagues’ [5] re-exploration — and indeed revision — of pineal-complex evolution in this issue of Current Biology. Fossils of this outwardly routine species, a close kin of extant monitor lizards (Varanus), have long been known and have been well studied recently [13,14]. Smith and colleagues [5], however, noticed a couple of specimens that showed something remarkable, which is not one midline opening in the skull roof as in other Figure 1. A four-eyed fossil lizard. lizards, but two. These fragmentary fossil The 49 million-year-old fossils of the extinct monitor lizard Saniwa ensidens uniquely and atavistically display both pineal and parapineal (parietal) eyes on the top of their heads, along with normal lateral specimens had sat in the Yale Peabody eyes. (Digital image based on microCT scan of extant Varanus monitor, modified to reflect the new Museum collection, barely noticed, for findings of S. ensidens [5]; by R. C. Ridgely of WitmerLab at Ohio University.) almost 150 years, but these authors had the insight to wonder whether they were (the eyes with which you’re reading these organs were almost certainly facing a ‘four-eyed’ animal. Indeed, at the words) and ‘median (midline) eyes’ within photosensory at their evolutionary origins end of their exhaustive studies, Smith and or on top of the head. Indeed, the median [6], and remain so to varying extents in the colleagues [5] came to the conclusion that eye formed by a component of the pineal species that retain them today. Indeed, the larger normal-looking parietal foramen complex is widely known as ‘the third eye’ the evolutionary history of the pineal in the front must have been for the [3]. A new paper by Krister Smith and complex is complicated in that some parapineal organ as in other lizards, and colleagues in this issue of Current Biology extant groups (mammals and birds) have the smaller ‘accessory’ foramen behind [5] now presents evidence from a fossil lost the parapineal organ and one extant must have been for the pineal organ. lizard for the first identifiable case of a group (crocodilians) has apparently lost Moreover, the cup-like bone surface on jawed vertebrate with not just a third, but a both components almost entirely [6]. the outer part of the accessory foramen is fourth eye (Figure 1), both of which are part Thus, in most extant vertebrates, the consistent with the presence in life of of the pineal complex, thus shedding new pineal organ is the major component, and cornea- and lens-like structures. In other light, as it were, on the evolution of the its function largely centers on words, Saniwa ensidens had both parietal entire complex. photosensitive neuroendocrine (parapineal) and pineal eyes! Light-sensitive organs (in a broad production of melatonin. This completely unexpected finding has sense, visual organs) are widespread An exception would seem to be lizards. a number of important implications. For among invertebrates and vertebrates, and Most lizards have a prominent and example, there is no longer any debate pineal evolution extends back to the very externally visible ‘third eye’ (with cornea, that it is the parapineal component of the beginnings of vertebrates [6]. The pineal lens, etc.) in the midline of the tops of their pineal complex that forms the parietal eye complex is comprised of a pineal organ heads. This eye traverses an opening in in lizards, and that the parapineal/parietal and a parapineal organ, both of which the center of their bony skull roof, opening should no longer be termed the derive from a portion of the forebrain commonly called the parietal foramen in ‘pineal foramen’ in lizards as it still is called the diencephalon, specifically the which this eye sits (named for the parietal sometimes. It also tips the scales toward epithalamus. Anatomically, the parapineal bones that flank the opening). It turns out the notion that the pineal complex sits in front of the pineal on the midline, that this well-formed third or, as it’s probably is natively a midline system but debates have raged about whether commonly known, parietal eye of lizards is rather than a paired system that got they originally were paired organs (that is, thought to derive from the parapineal evolutionarily tugged into its midline left and right, like the lateral eyes) that organ, and the pineal organ sits behind it alignment. But, although it’s good to clean subsequently diverged in function and more deeply within the bony brain cavity, up the nomenclature and nail down the position [7] or whether they truly were as in other vertebrates [9,10]. So, most original anatomy, the truly remarkable always separate midline structures [8]. extant vertebrate groups emphasize the point is that Saniwa had a photoreceptive Regardless, both pineal and parapineal pineal gland whereas lizards emphasize pineal eye that peered out of the top of its R312 Current Biology 28, R306–R327, April 2, 2018 Current Biology Dispatches head. Such a feature was thought to have 4. Masuda, H., Oishi, T., Ohtani, M., Michinomae, 10. Quay, W.B. (1979). The parietal eye–pineal been lost hundreds of millions of years ago M., Fukada, Y., Shichida, Y., and Yoshizawa, complex. In Biology of the Reptilia, v. 9 T. (1994). Visual pigments in the pineal (Neurology A), C. Gans, R.G. Northcutt, and P. back when the earliest vertebrates with complex of the Japanese quail, Japanese Ulinski, eds. (London: Academic Press), jaws evolved, at which point the pineal grass lizard and bullfrog: pp. 245–406. Immunocytochemistry and HPLC analysis. gland sunk deeper into the brain cavity Tiss. Cell 26, 101–113. 11. Benoit, J., Abdala, F., Manger, P.R., and and lost its eyelike function. In 1893, Rubidge, B.S. (2016). The sixth sense in Belgian paleontologist Louis Dollo 5. Smith, K.T., Bhullar, B.-A.S., Ko¨ hler, G., and mammalian forerunners: variability of the parietal Habersetzer, J. (2018). The only known jawed foramen and the evolution of the pineal eye in formulated the Law of the Irreversibility of vertebrate with four eyes and the Bauplan of South African Permo-Triassic eutheriodont Evolution, which simply states: that which the pineal complex. Curr. Biol. 28, 1101–1107. therapsids. Acta Palaeontol. Pol. 61, 777–789. is lost shall not be regained [15]. Some 6. Ekstro¨ m, P., and Meissl, H. (2003). Evolution 12. Kemp, T.S. (1969). On the functional laws are meant to be broken, and the re- of photosensory pineal organs in new morphology of the gorgonopsian skull. 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