New manuscript up on @Preprints_org today! Here, @wc_ratcliff and I take a theoretical approach to examine the evolution of phototrophy, looking at what it tells us about the evolution of major evolutionary innovations in general. https://www.preprints.org/manuscript/202011.0700/v1

The history of Earth is full of evolutionary innovations that fundamentally changed the world. Some of them happened many times, like the evolution of multicellular creatures from microbes. But some, like the origin of Eukaryotes, only happened once!

Are these singular innovations difficult to invent? Or might they be easy to evolve, but remain singular because they've been suppressed by first-movers? To study this, we looked at an invention that happened exactly twice – phototrophy, the ability to use light for energy.

When a major innovation occurs once, you cannot tell *why*. But with two to work with, you can compare them to each other. It is still a rare invention, but their differences can tell you something about their relationship to each other and other hypothetical similar inventions.

Everything green you’ve ever seen uses oxygenic photosynthesis – but this is just the most successful branch of a diverse set of organisms with machinery in common that uses chlorophyll-containing reaction centers, called *chlorophototrophs*.

But there’s a completely separate invention of the ability to use light. These *retinalophototrophs* use rhodopsin proteins with no common ancestry to chlorophototrophy. Fantastically diverse microbes and fungi all use this machinery, with a purple pigment called retinal.

Chlorophyll and retinal-using machinery could hardly be more different.

Reaction centers are huge proteins that can absorb dim light, capture a lot of energy per photon, need iron, and can be used to build biomass. Rhodopsins need bright light to function, capture only a little energy per photon, don’t need iron, and can only make energy not biomass.

When we ran the math, we discovered that even though chlorophototrophic reaction centers were efficient per unit light, the rhodopsins could be more efficient per unit protein! The same protein investment will give you way more energy in bright light with rhodopsins.

The rhodopsins and reaction centers represent opposite ends of a *tradeoff* between efficiency per unit resource and efficiency per unit investment. Depending on how rich your resources are, one or the other is optimal.

Between this and other attributes, it turns out that the chlorophototrophs and retinalophototrophs perfectly partition the light-using ecological niches between themselves, strongly suggesting that they have co-evolved!

Together, these two forms provide options for phototrophs in all niches. Their exclusivity suggests they have suppressed the evolution of phototrophs that are too similar to themselves, but were unable to suppress things enough unlike themselves, allowing them to stably coexist.

This suggests that the fact that phototrophy evolved just twice over the last 3.5 billion years does not mean it was evolutionarily ‘difficult’, but rather that the breadth of the phototrophic niche is too wide for the first innovator to suppress all future origins.

We explore the most important trade-offs responsible for the stable coexistence of two phototrophic systems, and examine how easy it would be for novel phototrophic systems to evolve (hint: it’s probably pretty easy, there’s a decent amount of photoactive biology out there!).

This has major implications for other rare innovations in Earth's history! Maybe singularities like Eukaryogenesis or life's origin are not difficult leaps but reflect evolutionary priority effects- whoever came first squashed upstarts that take halting steps into their domain.

Importantly, different innovations may have fundamentally different niche breadths. Life, for instance, probably has just one niche on Earth, and the first mover is capable of suppressing poor-performing independent upstarts.

In contrast, other innovations may not be much impacted by evolutionary priority effects: multicellular fungi, plants, and animals all live in different ways, and it’s hard to imagine that the innovation here (multicellularity) would be susceptible to competitive exclusion.

This paper is the result of many sleepless nights reading papers on the fine details of photosynthesis, then realizing that it phototrophy is the only example we have of a dual-singularity, which tell us something interesting about the evolution of innovation more broadly.