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

Abstract

SUMMARYHagfish 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.HIGHLIGHTSHagfish eyes are degenerate but not degenerating, i.e. rudimentary but growingRetinal interneurons discovered implying ancestral hagfish had derived retinas & visionDespite lacking pigment, a Retinal Pigmented Epithelium homolog functions in hagfishRevised synapomorphies illuminate the dimly lit origins of vertebrate eye evolutionGRAPHICAL ABSTRACT

A possible origin of the inverted vertebrate retina revealed by physical modeling

“…The amphioxus eye - with its inverted interpreted retina - does not fit directly into the stalk eye hypothesis, unlike the more advanced, bulging eyes of Conodonts (Donoghue, Forey, & Aldridge, 2000). The eye of the Hagfish may represent phase 3 (Figure 2) because it comprises an inverted retina around a vitreous spherical body but has no screening pigment layer (Dong & Allison, 2021). Next, the eye was retracted into the body without maintaining the optic stalk.…”

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

“…Sequences of transcripts are reported in Supplemental file 'eSupp_Transcript_ sequence_ID', and the RNA-Seq data are available from the Dryad Digital Repository: https://doi.org/10.5061/dryad. 79cnp5ht7 [55].…”

Gross anatomy of the Pacific hagfish,Eptatretus burgeri, with special reference to the coelomic viscera

“…In addition, they have many cyclostome-specific features (e.g., lingual apparatus, velum, and mucous cartilage) not found in jawed vertebrates (Janvier, 1996;Oisi et al, 2013), and whether these features are inherited from the common ancestors of vertebrates or are synapomorphies of cyclostomes remains controversial (Yokoyama et al, 2021; also see Sugahara, 2021). The morphology of the hagfishes is regarded to be highly derived, including the degeneration of eyes because of adaptation to the deep sea (Gabbott et al, 2016;Dong & Allison, 2021), and many studies have instead used lampreys as a model for cyclostomes.…”

“…In addition, they have many cyclostome-specific features (e.g., lingual apparatus, velum, and mucous cartilage) not found in jawed vertebrates (Janvier, 1996; Oisi et al, 2013), and whether these features are inherited from the common ancestors of vertebrates or are synapomorphies of cyclostomes remains controversial (Yokoyama et al, 2021; also see Sugahara, 2021). The morphology of the hagfishes is regarded to be highly derived, including the degeneration of eyes because of adaptation to the deep sea (Gabbott et al, 2016; Dong & Allison, 2021), and many studies have instead used lampreys as a model for cyclostomes. However, recent studies have suggested that some lamprey characteristics that had been regarded as ancestral to the cyclostomes, such as the larval-type oral apparatus (Miyashita et al, 2021) and the transformation of the larval endostyle into the thyroid after metamorphosis (Takagi et al, 2022), are in fact the derived state from the acquisition of the ammocoete larval stage.…”