There’s been a lot of study into how vertebrates colonised the land, conjuring up lovely visions of our fishy ancestors hauling themselves out onto the mud on stumpy proto-limbs, helped by exciting fossil finds like Tiktaalik. What hasn’t been studied so much is why. It seems obvious – whole new ecological niches to expand into, and a rich abundance of invertebrate life to eat…but how did the animals know this before they got there? Well it may have been because they had evolved eyes sophisticated enough to take a good look at the view…

The evolution of eyes has always fascinated biologists: Darwin discussed how a complex eye could evolve by simple stepwise improvements starting from a simple light sensor (which subsequent work has demonstrated), and the evolution of eyes has even been offered as a reason for the explosion in animal diversity seen 540 million years ago in the Cambrian. Now a new study (full text available) reported in PNAS sheds new light (sorry) on another event that fascinates biologists (and quite a lot of other people): how, or rather why, our fishy ancestors started crawling up onto the land. From the abstract:

The evolution of terrestrial vertebrates, starting around 385 million years ago, is an iconic moment in evolution that brings to mind images of fish transforming into four-legged animals. Here, we show that this radical change in body shape was preceded by an equally dramatic change in sensory abilities akin to transitioning from seeing over short distances in a dense fog to seeing over long distances on a clear day.

They call it the “buena vista” hypothesis, which frankly made me cringe, but it’s a powerful idea, supported by the fossil record and computer simulations. Simply put, the eyes of these proto-tetrapods tripled in size and shifted from the sides to the top of the head, long before any limb modifications took place. The change in size would have had a rather minimal improvement on seeing in the water: but air is far more transparent, and here the improvement in vision would have been significant.

The consequent combination of the increase in eye size and vision through air would have conferred a 1 million-fold increase in the amount of space within which objects could be seen.

The figure below is a summary of what they did: it’s open-access, so you can look up the full data set and figures if you like.

Eyes terra Fig1
Figure 1. From MacIver et al, 2017, PNAS

The anatomy suggests that these animals probably hunted like crocodiles, hanging just below the surface of the water but looking at prey just above the surface of the water, i.e. in air. What they would have seen is a bounty of juicy insect life out there on the land, selecting for further modifications like limbs and behaviour activity to drive them to explore the shoreline and beyond. This is important: nothing is going to evolve limbs unless there is something driving it to do so. Going onto land in hindsight seems logical – but there had to be a behavioural motivation to do so – these animals couldn’t know there was lots of potential food out there; they had to be able to detect it somehow. It seems that adapting to one form of lifestyle – that crocodile-like hunting strategy, opened up the possibility of a whole new way of living.

 

Here’s their model for how it happened:

 

Eyes terra Fig5
Figure 5 From MacIver et al, 2017, PNAS

A possible evolutionary scenario consistent with our results. Having invaded shallow waters, where the down-welling component of sunlight is significant, better visual range is obtained with eye sockets moved to the top of the skull, providing upward vision as shown here for Panderichthys. Possibly driven by low oxygen, animals surfaced near shore to breathe through the spiracles that had also dorsalized to just behind the eyes in the elpistostegalians, as shown here for Tiktaalik. Without correction for the differing refractive index of air, they initially saw blurry outlines of invertebrate fauna that had already been living on land for 50 My. With continued surfacing and selection of the slight changes to lens and cornea to enable a focused image of their quarry, in a small fraction of the 12-My transition from finned to digited tetrapod eye sizes, the full power of long-range vision would have emerged. The strong derivative of visual volume with respect to eye size would have facilitated the observed selection for larger eye size. Simultaneously, selective advantages of limbs with digits over limbs with fins made animals like Acanthostega better suited for longer forays onto land, culminating in more terrestrial forms, such as Pederpes, 30 My after Tiktaalik. The colored portion of the simplified tree marks an evolutionary phase with substantial body plan modifications. Shown in green in Left are the spiracles (what becomes the Eustachian tube) likely used for breathing at the water surface while using aerial vision. Total animal lengths are between 50 cm and 1.5 m and are not drawn to scale. Age spans from 385 My for Eusthenopteron to 355 My for Pederpes.

 

Reference:

MacIver, M.A. et al, 2017. Massive increase in visual range preceded the origin of terrestrial vertebrates. E2375–E2384, vol. 114 no. 12doi: 10.1073/pnas.1615563114

 

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