Photoreceptor Evolution–from Water Animals to Land Animals

This topic is among the most obvious of “gene-environment interactions” topics…!! 😊 During evolution, when vertebrates first left the water and ventured onto land, they encountered a visual world that was radically different from that of their aquatic ancestors. In order to survive successfully, “new” land species were required to adapt visually, in terms of being able to find food, avoid predators, and sexually reproduce. “The need to see acutely” — represents the environmental pressure; and necessary (and relatively evolutionarily “quick”) changes in visual networks of the eye (and/or brain) — represents the response by genes…

Fish exploit the strong wavelength-dependent interactions of light with water by differentially sending visual image signals from as many as five spectral photoreceptor types into distinct behavioral programs. However, out of the water — the same spectral rules do not apply, and this adaptation required rapid changes in response to this environmental pressure.

Early tetrapods [e.g., Kenichthys from China ~395 million years ago (MYA), Gogonasus & Panderichthys ~380 MYA, and then salamanders with four legs] soon evolved the double cone, a still poorly understood pair of new photoreceptors that increased the “ancestral terrestrial” complement from five to seven photoreceptors. Subsequent non-mammalian lineages differentially adapted this highly parallelized retinal input strategy for their diverse visual ecologies. In contrast, mammals (first appearing ~225 MYA) shed most of their ancestral photoreceptors and converged on an input strategy that is extraordinarily general. In eutherian mammals (i.e., animals born via placenta), including humans, parallelization emerged gradually during evolution, as the visual signal began to traverse the layers of the retina and onwards, into the brain.

Vertebrate vision first evolved in the water, where (for >50 million years) it was consistently based on visual signals from five 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). In the water, these five input streams are probably best thought of as parallel feature channels that deliver distinct types of information to distinct downstream circuits. This is because water absorbs and scatters light in a wavelength-dependent manner (see Fig 1A in attached pdf file), which means that “beyond color,” different spectral photoreceptor channels inherently deliver different types of visual information.

Aquatic visual systems have recently been proposed to evolutionarily reach “answers” that exploit these differences. In this view, photoreceptors represent parallel channels that are differentially wired to drive and/or regulate distinct behavioral programs (see Fig 1B in attached pdf file): 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 stabilization and navigation. Second, ancestral UV cones are used as a specialized 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 water, object vision can be a relatively easy task, because background structure tends to be heavily obscured by an approximately homogeneous aquatic backdrop. At short wavelengths, including in the UV range, this effect can be so extreme that no background is visible at all. Many small fish exploit this fact of physics to find their food. Out of 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. Accordingly, when early would-be tetrapods started to crawl out of the water, strong selection pressures would have favored a functional reorganization of some of these inherited aquatic circuits; 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, which took the “aquatic ancestral” photoreceptor complement of five to a “terrestrial ancestral” complement of seven (see Fig 1 in attached pdf file). The visual systems of all extant tetrapods, including humans, directly descend from this early “terrestrialized” retinal blueprint. However, from there, different descendant lineages have taken this highly parallelized 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 terrestrialized 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’ “heavy lifting” out of the eye and into the brain. Along this path — whether as

cause or consequence — descendant lineages gradually decreased their photoreceptor complements from seven types to six, then five, and eventually to the mere three that we see in eutherians today (see Fig 1C in attached pdf file): Rods (RH), as well as ancestral red (LWS) and UV cones (SWS1).

Primates, including humans, have then taken this eutherian strategy to the extreme: >99.9% of all photoreceptors in our eyes are either rods or ancestral red cones (including both “red-” and “green-shifted LWS variants”), 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 (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 color vision.

However, this “textbook strategy” is far removed from the original aquatic circuit design and probably quite unique to our own lineage. Accordingly, for understanding vision in a general sense, and to understand our own visual heritage, it will be critical to respect the vertebrates’ shared evolutionary past. Here, vision is built on a retinal circuit design that begins with major parallelization — right from the original evolutionary input. 😉😊

DwN

PLoS Biol Jan 22: e3002422

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