Krister T. Smith, Bhart-Anjan S. Bhullar, Gunther KÃhler & JÃrg Habersetzer (2018)
The Only Known Jawed Vertebrate with Four Eyes and the Bauplan of the Pineal Complex.
Current Biology (advance online publication)
An extinct monitor lizard had an atavistic pineal eye behind the third eye
This fourth eye confirms that the third eye in lizards is a parapineal derivative
The evolution of the pineal shows not only parallel reductions but also elaboration
The lizard third eye might not be a good model for the third eye of other tetrapods
The pineal and parapineal organs are dorsal outpocketings of the vertebrate diencephalon that play key roles in orientation and in circadian and annual cycles. Lampreys are four eyed in that both the pineal and parapineal form eyelike photosensory structures, but the pineal is the dominant or sole median photosensory structure in most lower vertebrate clades. The pineal complex has been thought to evolve in a single direction by losing photosensory and augmenting secretory function in the transitions from three-eyed lower vertebrates to two-eyed mammals and archosaurs. Yet the widely accepted elaboration of the parapineal instead of the pineal as the primary median photosensory organ in Lepidosauria (lizards, snakes, and tuataras) hints at a more complex evolutionary history. Here we present evidence that a fourth eye re-evolved from the pineal organ at least once within vertebrates, specifically in an extinct monitor lizard, Saniwa ensidens, in which pineal and parapineal eyes were present simultaneously. The tandem midline location of these structures confirms in a striking fashion the proposed homology of the parietal eye with the parapineal organ and refutes the classical model of pineal bilaterality. It furthermore raises questions about the evolution and functional interpretation of the median photosensory organ in other tetrapod clades.