Vertebrate features revealed in the rudimentary eye of the Pacific hagfish (Eptatretus stoutii)

Abstract

Hagfish eyes are markedly basic compared to the eyes of other vertebrates, lacking a pigmented epithelium, a lens, and a retinal architecture built of three cell layers - the photoreceptors, interneurons & ganglion cells. Concomitant with hagfish belonging to the earliest-branching vertebrate group (the jawless Agnathans), this lack of derived characters has prompted competing interpretations that hagfish eyes represent either a transitional form in the early evolution of vertebrate vision, or a regression from a previously elaborate organ. Here we show the hagfish retina is not extensively degenerating during its ontogeny, but instead grows throughout life via a recognizable Pax6+ ciliary marginal zone. The retina has a distinct layer of photoreceptor cells that appear to homogeneously express a single opsin of the rh1 rod opsin class. The epithelium that encompasses these photoreceptors is striking because it lacks the melanin pigment that is universally associated with animal vision; notwithstanding, we suggest this epithelium is a homolog of gnathosome Retinal Pigment Epithelium (RPE) based on its robust expression of RPE65 and its engulfment of photoreceptor outer segments. We infer that the hagfish retina is not entirely rudimentary in its wiring, despite lacking a morphologically distinct layer of interneurons: multiple populations of cells exist in the hagfish inner retina that differentially express markers of vertebrate retinal interneurons. Overall, these data clarify Agnathan retinal homologies, reveal characters that now appear to be ubiquitous across the eyes of vertebrates, and refine interpretations of early vertebrate visual system evolution. HIGHLIGHTSO_LIHagfish eyes are degenerate but not degenerating, i.e. rudimentary but growing C_LIO_LIRetinal interneurons discovered implying ancestral hagfish had derived retinas & vision C_LIO_LIDespite lacking pigment, a Retinal Pigmented Epithelium homolog functions in hagfish C_LIO_LIRevised synapomorphies illuminate the dimly lit origins of vertebrate eye evolution C_LI GRAPHICAL ABSTRACT O_FIG_DISPLAY_L [Figure 1] M_FIG_DISPLAY C_FIG_DISPLAY