Massive increase in visual range preceded the origin of terrestrial vertebrates

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. Measurements of eye sockets and simulations of their evolution show that eyes nearly tripled in size just before vertebrates began living on land. Computational simulations of these animal's visual ecology show that for viewing objects through water, the increase in eye size provided a negligible increase in performance. However, when viewing objects through air, the increase in eye size provided a large increase in performance. The jump in eye size was, therefore, unlikely to have arisen for seeing through water and instead points to an unexpected hybrid of seeing through air while still primarily inhabiting water. Our results and several anatomical innovations arising at the same time suggest lifestyle similarity to crocodiles. 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 "buena vista" hypothesis that our data suggest is that seeing opportunities from afar played a role in the subsequent evolution of fully terrestrial limbs as well as the emergence of elaborated action sequences through planning circuits in the nervous system.

Keywords: fish–tetrapod transition; prospective cognition; terrestriality; vision; visual ecology.

Fig. 1.

The sequence of steps within early tetrapod paleontology as well as computational visual ecology used for generating the results of this study.

Fig. 2.

Evolution and adaptive landscape of relative eye socket size in early tetrapods summarizing our phylogenetic comparative study performed over a sample of 1,000 time-calibrated trees. The circles (red for finned, yellow for finned transitional, blue for digited, and brown for digited aquatic tetrapods) represent body size-corrected relative eye socket sizes, the residuals from phylogenetically generalized least squares regression (PGLS) of log₁₀-transformed variables (Materials and Methods and SI Appendix, Scaling of Orbit and Skull Length in Early Tetrapods). The thick branches indicate positions of well-supported selective regime shifts, with associated factors signifying the change in eye socket size compared with the ancestral regime (before the green dot) after body size effects are accounted for.

Fig. 3.

Eye socket lengths across the taxa in Fig. 2 grouped by the regime shift analysis. (A) The mean (horizontal bars) absolute eye socket length of digited tetrapods was three times larger than that of their finned relatives, with the elpistostegalians (finned-transitional) midway. The digited tetrapods that returned to life underwater (adelospondyl-colosteids, digited-aquatic) reverted to a size similar to that of their finned relatives. (B) Relative eye socket size was calculated as residuals from a phylogenetically informed regression of log₁₀-transformed variables (Materials and Methods) averaged over the full set of 1,000 trees. Positive residuals indicate eye sockets larger than expected based on skull length, whereas negative residuals indicate eye sockets smaller than expected. The Bayesian OU results in Fig. 2 show the presence of an adaptive evolutionary process and provide estimates of the adaptive peak for each group (horizontal bars). The elpistostegalians entered a new selective regime but are lagging behind, because time was insufficient to accrue enough increases in eye socket size to reach the peak.However, the digited tetrapods are centered around their adaptive peak, except for the adelospondyl-colosteids. As expected for adiverse group, not all tetrapods are at their respective peak, reflecting a normal evolutionary pattern in which trait values are dispersed around the optimal value. The Bayesian OU findings show that there must have been a selective benefit from larger eye sockets in finned transitional and digited tetrapods, but uncovering its basis requires modeling visual performance across likely environments.

Fig. 4.

Visual performance in and out of water. Aquatic vision is estimated using the Baseline River water type defined in SI Appendix, Table S3 at a depth of 8 m. The object is a black 10-cm-diameter disk. (A1 and A2) Maximum distance that the object can be seen in water and air, respectively, under various lighting conditions. Note that visual range scales proportionately to target size. For a 1-cm disk in daylight, the aerial range decreases to 139.3 m assuming mean pupil size for digited tetrapods and 54.7 m for the mean pupil size of finned tetrapods (data not shown). (B1 and B2) How much range is gained for an increase in pupil size? Note that the y-axis multiplier is 100 times larger in B2. (C1 and C2) Total volume within which the standard object is visible. Note that the y-axis multiplier is 1 million times larger in C2. (D1 and D2) How much volume is gained for an increase in pupil size? Note that the y-axis multiplier is 1 million times larger in D2. For the aerial plots, the aquatic values are shown but imperceptible. Uncertainty for the daylight condition (green fill) was calculated by using alternative values for the vision model (Materials and Methods) and is not shown for other conditions for clarity. SD is here only for showing the distribution of estimated pupil sizes; it cannot be used in this context for ascertaining significance because of shared ancestry (details are in the text). *Red horizontal bars show $\pm$1 SD of pupil sizes from the mean (dotted vertical lines) estimated for the eye sockets of finned tetrapods. **Blue horizontal bars and vertical lines are for the digited tetrapods.

Fig. 5.

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 (Fig. 4A1) 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 (33) 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 (34) 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.