Four camera eyes in the earliest vertebrates from the Cambrian

Vertebrate vision is mainly accommodated by a pair of lateral image-forming camera eyes and is facilitated in non-mammalian vertebrates by a dorsal pair of photoreceptive organs, the endocrine pineal complex (pineal and parapineal organs)1. The pineal complex shares a common genetic and embryologic basis with the lateral eyes, both of which are derived from evaginations during the development of diencephalon2. Despite widely heralded as the third eye in crown vertebrates3, the nature of the pineal complex and hypothesised visual capability in early vertebrates2 remains unknown. Here we describe in two species of myllokunmingids, the earliest known fossil vertebrates (c.a. 518 Million Years Ago, Mya), two pigmented features situated between the lateral eyes and interpret these as pineal/parapineal organs. In both myllokunmingid species, the pineal complex bears abundant melanin-containing melanosomes that are identical to those in the retinal pigment epithelium (RPE) in the lateral eyes, and a distinctive, regular ovoid structure that is interpreted as a lens. Our results reveal the lateral eyes and pineal complex in myllokunmingids likely functioned as camera eyes capable of image formation. As such we propose that four camera eyes are a vertebrate ancestral character, corroborating hypotheses regarding the deep homology between eyes and pineal complex.