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From water to land: Evolution of photoreceptor circuits for vision in air [1]

['Tom Baden', 'University Of Sussex', 'Sussex Neuroscience', 'Sussex Center For Sensory Neuroscience', 'Computation', 'Brighton', 'United Kingdom']

Date: 2024-02

Vertebrate vision first evolved in the water, where for more than 150 million years it was consistently based on the signals from 5 anatomically and molecularly distinct types of photoreceptor neurons: rods, as well as ancestral red, green, blue, and UV cones (expressing RH, LWS, RH2, SWS2, and SWS1 opsin, respectively) [1–3]. In the water, these 5 input streams are probably best thought of as parallel feature channels that deliver distinct types of information to distinct downstream circuits [1]. This is because water absorbs and scatters light in a wavelength-dependent manner (Fig 1A), which means that “beyond colour” [1], different spectral photoreceptor channels inherently deliver different types of visual information.

( a ) Split-photo showing a riverine underwater scene and its corresponding view above the surface. Note that below the water, but not above, visual structure rapidly disappears with distance. ( b ) Retinal circuit summary of how ancestral photoreceptor types (cf. Fig 2A ) probably serve as parallel feature channels that differentially drive and/or regulate into distinct sets of behavioural programmes (from ref [ 1 ]). ( c ) Conceptual summary of how early terrestrial vertebrates expanded the 5 ancestral aquatic retinal input channels to 7. Most extant tetrapods use variants of this “ancestral terrestrial” strategy, but mammals gradually shed photoreceptor diversity while offloading visual computations from the retina to the brain. Animal schematics taken from ref [ 122 ].

As argued in a recent perspective [1], aquatic visual systems evolutionarily reached solutions that exploit these differences. In this view, photoreceptors represent parallel channels that are differentially wired to drive and/or regulate distinct behavioural programmes (Fig 1B): First, rods and ancestral red cones are the eyes’ primary brightness sensors. They are used for general purpose vision and to drive circuits for body stabilisation and navigation. Second, ancestral UV cones are used as a specialised foreground system, primarily wired into circuits related to predator–prey interactions and general threat detection. Third, ancestral green and blue cones probably represent an auxiliary system, tasked with regulating rather than driving the primary red/rod and UV circuits.

This ancestral strategy exploits the specific peculiarities of aquatic visual worlds; however, in air the same rules do not necessarily apply. For example, in the water, object vision can be a relatively easy task, because background structure tends to be heavily obscured by an approximately homogeneous aquatic backdrop [4]. At short wavelengths including in the UV range, this effect can be so extreme that no background is visible at all [5]. Many small fish exploit this fact of physics to find their food [5–9]. Above the water, this and many other “ancestral visual tricks” no longer work, because in air, contrast tends to be largely independent of viewing distance: Everything is visible at high contrast [10]. Accordingly, when early would-be tetrapods started to peek out of the water, strong selection pressures would have favoured a functional reorganisation of some of these inherited aquatic circuits, and nowhere is this more evident that at the level of the photoreceptors themselves.

One of the earliest and perhaps most important retinal circuit changes was the emergence of the double cone [1,11], which took the “aquatic ancestral” photoreceptor complement of 5 to a “terrestrial ancestral” complement of 7 (Fig 1C). The visual systems of all extant tetrapods, including humans, directly descend from this early “terrestrialised” retinal blueprint. However, from here, different descendant lineages have taken this highly parallelised retinal input strategy and embarked upon radically different visual paths. Most lineages, including those that led to modern-day amphibians, reptiles, and birds, have retained the terrestrialised ancestral blueprint, modifying upon it to suit their unique visual ecologies. Mammals, however, have ended up on a very different path. Their early synapsid ancestors gradually shifted some of their visual systems’ heavily lifting out of the eye and into the brain. Along this path—whether as cause or consequence—descendant lineages gradually reduced their photoreceptor complements from 7 types to 6, then 5, and eventually to the mere 3 that we see in modern-day eutherians (Fig 1C) [1]: Rods (RH), as well as ancestral red (LWS) and UV cones (SWS1).

Primates including humans have then then taken this eutherian strategy to the extreme: More than 99.9% of all photoreceptors in our eyes are either rods or ancestral red cones (including both “red-” and “green-shifted LWS variants”) [12], the ancestral “general purpose” system of the eye. The remaining 0.1% is what is left of the ancestral UV system, today expressing a blue-shifted variant of the SWS1 opsin [3] (hence often called “blue cones,” not to be confused with ancestral blue cones that express SWS2). In concert, the “three” cone variants drive achromatic vision (although with limited contribution from ancestral UV cones), while in opposition they serve colour vision [13]. However, this “textbook strategy” is far removed from the original aquatic circuit design and probably quite unique to our own lineage [1]. Accordingly, for understanding vision in a general sense, and to understand our own visual heritage, it will be critical to pay homage to vertebrate’s shared evolutionary past. Here, vision is built on a retinal circuit design that begins with major parallelisation right at the input.

From water to air

Following more than 150 million years of aquatic vision, vertebrates started to peek above water surface in the Devonian, some 390 mya [10,14]. This would change everything. In air, water’s strong scatter and absorption of light are essentially gone, and this would have (i) provided more photons for vision overall; (ii) disabled water’s links between spectral content and viewing distance; and (iii) made it possible to see for kilometres rather than metres. The expansion in visual interaction range may have driven the expansion of brain complexity in terrestrial species [15], for example, because this would have turned visual predator–prey interactions from largely fast and reactionary encounters to ones that necessitated long-term planning. However, not only brains became more complex: So did eyes [16] (Fig 2A–2D)!

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TIFF original image Download: Fig 2. Vertebrate photoreceptors over evolutionary time. (a) Summary of vertebrate photoreceptor neurons (bottom) and their typically expressed opsins (top), including the 5 ancestral types (left) and the 3 “new” types that emerged soon after early tetrapods’ colonisation of the land. (b–d) Approximate timeline of vertebrate evolution and key changes in eyes and photoreceptor complements as indicated (cf. Fig 1D). Schematised reconstruction of early tetrapod skull shapes illustrate changing body shapes and eye enlargements (c, based on ref [14], from bottom: Eusthenopteron, Acanthostega, Pederpes). Zebrafish and chicken cone mosaics (d) modified from refs [123] and [124], respectively. https://doi.org/10.1371/journal.pbio.3002422.g002

The eyes of early tetrapods differed from the ancestral aquatic eyes of fish in at least 3 important ways: Eyes were substantially larger [14] (Fig 2C), the previously crystalline cone mosaic of fish [17,18] was replaced with a locally random mosaic [19,20] (Fig 2D), and new types of photoreceptors emerged [11,21,22] (Fig 2A and 2D). The order of these events or their possible interdependencies are difficult to reliably reconstruct today, but all 3 traits emerged before the subsequent split of amphibians, some 340 mya.

Eye enlargement. This transition, which preceded the emergence of well-developed limbs and digits [14], is chiselled into the fossil record: Within only a few million years, early lobe-finned fish transitioned from a swimming form with small eyes, to an “underwater walking” form with large eyes (Fig 2C). Our last fully aquatic ancestors probably lived in the shallows but peeked out of the water in search of food. Invertebrates had colonised the land some 50 million years prior [23], and with no vertebrate predators around, their initial lack of defences [24] would have made for an easy meal. While tetrapod eye enlargement was therefore likely an adaptation for a crocodilian-like lifestyle, it opened the floodgates for much to come.

Shattering the cone mosaic. Many surface dwelling fish have a crystalline cone mosaic with fixed photoreceptor-stoichiometry of 2:2:1:1 for red, green, blue, and UV, and with rods slotted around UV cones [4,17,18] (Fig 2D, left). In species where subsets of cone types are missing the mosaic rearranges accordingly to close any gaps [17,25]. The functional purpose of this crystalline mosaic remains poorly understood; however, it may confer important computational advantages, perhaps not too dissimilar to some of those conferred by the crystalline organisation of crustacean eyes [26], which notably includes insects [27–29]. Conceivably, the mosaic might also be exploited to reliably match “driving” and “regulatory” cone circuits (cf. Fig 1B). In support, in some fish the crystalline lattice propagates onto subsets of horizontal and bipolar cells [17,30]. However, the crystalline solution of fish does not work in air. First, it would lead to spatial oversampling in the periphery, because unlike in water, terrestrial optics cannot simultaneously maintain perfect focus across the entire back of the eye [31]. Second, due to greatly reduced photon scatter and absorption in air, everything is visible with high contrast for as far as the eye can see. Sampling such an environment with a regular cone lattice leads to aliasing [32], which would in turn incapacitate motion circuits. This problem is long recognised in digital photography where it is solved by introducing blur; however, this solution is energy inefficient. In biology, a better option is to break the crystalline arrangement in favour of a locally randomised pattern (Fig 2D, right). This also opened up the possibility to discard the fixed cone stoichiometry in favour of distinct and locally flexible cone ratios that best serve an animal’s specific visual ecology—as is the case in all extant tetrapods [3,20]. And yet, one mystery remains: Extant lobe-finned fishes, the closest living relatives to the aquatic ancestors of tetrapods, have no crystalline mosaic [17,33,34]. The arrangement is also not found in the “preceding” cartilaginous fish or in lampreys [17,35]. The crystalline pattern may therefore be a clade-specific trait of ray-finned fishes that is not ancestral to the tetrapod eye. Alternatively, the crystalline arrangement could have evolved in the common ancestor to all teleosts but have subsequently been lost in extant lobe-finned species, of which there are only 2 small lineages: coelacanth, who live in the deep where light is limiting [36] and where the mosaic breaks also in ray-finned fish [37], and lungfish [33,34], who like early tetrapods routinely peek out of the water.

New photoreceptors. At least 2 new sets of photoreceptor types emerged in early tetrapods: “double cones” [11] and “blue rods” [21,38,39]. Both are present in amphibians but absent in fish, suggesting that their emergence coincided with the first major presence of vertebrates on land. Correspondingly, their purpose is probably related to exploiting new opportunities that presented themselves above the water surface. Of the 2 new photoreceptor systems, double cones probably appeared first. They exist in amphibians [39], reptiles [40,41], birds [11,22], monotremes [42–44], and marsupials [44–46], and therefore probably appeared in a common ancestor to all these lineages: the first tetrapods (Figs 2B and 1C, cf). They are again missing in eutherian mammals [3]. By contrast, blue rods are only present in amphibians [21,38] and therefore probably emerged after their lineage had already diverged from that of subsequent terrestrial species. The origin of double cones is debated, but their anatomical similarity to pairs of ancestral red and green cones in the eyes of fish [18] points at their joint duplication as a likely candidate. Pairs of teleost red and green single cones are also sometimes referred to as double cones [47]; however, this is a historical misnomer: Fish only have 1 set of these cones, while non-eutherian tetrapods have 2: the ancestral set of red and green single cones, plus an independent population of double cones.

Duplicating red/green circuits? Double cones are made up of 2 tightly associated photoreceptors, called the principal and accessory member [11]. In line with its putative origin from the red single cone, the principal member expresses the red LWS opsin, but the same opsin is also usually [48] found in the accessory member [22]. The latter may have resulted from an opsin expression switch from RH2 to LWS. The 2 members of the double cone also differ in their oil droplets [49,50] (see below). Beyond inheriting opsins and morphological characteristics, any newly duplicated cones would presumably also have inherited their ancestors’ postsynaptic circuitry. This would have opened the option to share or take over some of their original functions. In agreement, just like red and green single cones, the 2 members of the double cone feed into mutually independent horizontal and bipolar cell circuits [11]. Conceivably, the ancestral one-size-fits-all strategy of using red cones to drive most of vision could therefore now be broken into 2 independent circuits, each with their own regulatory system. This in turn would have enabled individual specialisation of the 2 circuits for different sets of visual tasks. One of these tasks, at long last, might have been the emergence of a dedicated system for colour vision as we think of it today.

Co-option of ancestral single cones for terrestrial colour vision? This view is supported by observing phylogenetic patterns in photoreceptor oil droplets—small optical elements that are positioned immediately in front of cones’ light sensitive outer segments [49]. Oil droplets are common in vertebrates, from lobe-finned fish to marsupials, and again absent in eutherians. Moreover, some ray-finned fish have ellipsosomes, which though developmentally distinct, appear functionally reminiscent of oil droplets [51]. In general, oil droplets can serve many functions, but one of them is spectral sharpening [49,52,53]. By mixing coloured pigments into the oil, the droplets can be used as filters that restrict a cone’s spectral sensitivity. This limits spectral overlap between cones and thereby increases colour resolution. However, this sharpening comes at the cost of reduced light sensitivity, which means that it is not possible to simultaneously optimise the same photoreceptor for high signal to noise greyscale vision and for spectrally narrow colour vision. Prior to the emergence of double cones, this trade-off would have precluded ancestral red cones from using oil droplets (or ellipsosomes) in this way, and correspondingly, all teleosts [49] except lungfish [33,34] use them for non-spectral tasks. Conversely, oil droplets are often heavily pigmented in red cones of amniotes, while double cone droplets remain at most weakly pigmented, and sometimes absent [49,52,53]. Together, this hints that double cones, led by the principal member and regulated by the accessory member, took over some of the original roles of the long wavelength system in supporting high acuity spatiotemporal tasks [54]. This could have freed up the use of single cones for spectral vision. In agreement, most diurnal birds retain the full complement of ancestral single cones, and these cones’ interplay with oil droplets leads to the probably most highly resolved colour vision system among vertebrates [22,49,52,53] (Fig 3A and 3B). Double cones are theoretically not needed for this task [54]. Among single cones, any surviving opponency of ancestral green and blue circuits [55] would no longer be overly useful for estimating distance in air [1,10,56], and similarly, their requirements for regulating motion circuits likely changed [57]. This would have opened the possibility to co-opt some of their existing, spectrally nuanced retinal and central circuits for new functions, such as colour vision. Likewise, some of the ancestral functions of UV cones, such as prey capture, are less applicable in air, and probably opened further options for spectral specialisations. A decreased dependence on single cones for supporting achromatic vision, alongside the no longer fixed stoichiometry as necessitated in fish, would have allowed retinal circuits to reduce their relative abundances, including of their postsynaptic circuits. For example, in chicken only around 20% of cones are ancestral blue- or UV cones [19], and these feed into fewer than 10% of bipolar cells [11], down from more than half in zebrafish [58]. This reduction in short wavelength contributions to retinal circuits is pervasive across terrestrial species and taken to the extreme in our own eye: Fewer than 0.1% of photoreceptors in the human retina are ancestral UV cones, and only a single type of bipolar cell specifically represents their signals [59,60]. PPT PowerPoint slide

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TIFF original image Download: Fig 3. Retinal circuits of nonmammalian tetrapods. (a) Conceptual retinal wiring schema of diurnal birds and reptiles, illustrating how double cones might fit into the circuit blueprint inherited from fish (cf. Fig 1B). While double cones might partially take over greyscale functions of the ancestral red system, existing and new interactions between single cone circuits might have increasingly been coopted for colour vision. (b) Spectral sensitivity functions of chicken cones with oil droplets included (based on ref [125]). (c) Mean spike rates of 2 functionally identified ganglion cell clusters from poultry chick retina in response to a time-accelerating full field chirp stimulus as indicated (mod. from ref [65]). (d) As (a), but for frogs, who lost ancestral green cones (RH2) but evolved “blue rods.” Potentially, blue rods serve functions similar to those served by ancestral blue cones of fish, however at lower light levels. https://doi.org/10.1371/journal.pbio.3002422.g003

Double cones took over (some of) achromatic vision. While single cones potentially specialised for colour vision, double cones may have specialised for high acuity spatiotemporal vision [54,61]. In chicken, they co-wire with rods [11], the ancestral remit of red single cones [58,62]. Double cones are usually also the largest and most numerous cone types, which maximises their potential for temporal and spatial resolution, respectively [63]. In support, birds generally have some of the fastest eyes of any vertebrate [64], and the spectral tuning of birds’ fastest retinal output channels (Fig 3C) is consistent with a primary drive from a red opsin expressing cone [65]. However, the extent to which these fast channels are driven by red single and/or double cones remains unknown. It is also unclear if the principal and accessory members of the double cone work jointly (as suggested by their intimate coupling), in mutual opposition (as hinted by their putative ancestry), or both. Despite their pervasive presence across vertebrates, from frogs [39] to kangaroos [44], systematic data on the function of double cones and their downstream circuits remains close to nonexistent. Moreover, despite the newfound potential for differentially specialising red circuits, some important aspects of ancestral red single cones for driving achromatic vision must have been retained: First, diurnal raptors have the highest spatial resolution of any vertebrate, but in most species, this is achieved without the use of double cones which are systematically absent from their foveae [66]. Second, eutherian mammals lost the double cone, but they can see perfectly fine. If double cones would have completely taken over general-purpose greyscale vision in the ancestors of eutherian mammals, our own eyes today would probably be covered in double cones, not red single cones.

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