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Todd , qai Fg ) hsmjrsiti y okteouinoccurred evolution socket eye in shift primarily major This be 2). to (Fig. understood aquatic the animals of in (here- ”), origin “digited and the after fingers before including happened limbs eye complete have with larger to vertebrates favoring likely change most a is finding: sockets surprising a reveals early bution of sizes socket eye study Methods). relative to and (5) the (Materials method tetrapods of this of landscape variant adaptive Bayesian a the evolu- use by trait We of 4). guided model (3, approach a tion as an process follow (OU) we Ornstein–Uhlenbeck depend the Specifically, that property. tests independence this obser- significance statistical on our conventional losing in disqualifying sizes 2), result socket (1, sample eye our their of in vations animals the incorporat- of evolutionary the approach relationships because statistical needed, is A from information phylogenetic regression). inferred ing animal a socket of by the size eye length in for relative corrected changes of length were evolution (socket compara- length the there phylogenetic governing whether a regime estimate selective Using apply to evolu- phylogeny. then approach 1,000 in we tive of uncertainties distribution, set for tree account a this to generated trees We tionary lengths water– Methods). socket the eye and and bracket skull (Materials par- measurable that time-calibrated have its taxa and a across transition of tetrapodomorph land study assembly 59 our the of of with phylogeny steps start of We sequence disciplines. ent the shows 1 Fig. Terrestriality Before Appeared Eyes Large 1073/pnas.1615563114/-/DCSupplemental at online information supporting contains article This at available 1 is results these reproduce to 10.5281/zenodo.321923. data and Code option. deposition: access Data open PNAS the through online available Freely Submission. Direct PNAS a is article This interest. of conflict no declare paper. authors the The wrote C.D.M. L.S. and and U.M., M.A.M. L.S., and M.A.M., data; tools; analyzed reagents/analytic new contributed T.D.M. research; uhrcnrbtos ...adLS eindrsac;MAM n ..performed L.S. and M.A.M. research; designed L.S. and M.A.M. contributions: Author [email protected]. owo orsodnemyb drse.Eal aie@otwseneuor [email protected] Email: addressed. be may correspondence whom To o re oasot adadeetal,frlf there. life for eventually, and limbs—first land for onto selection forays aiding brief bounty land, for the on to prey line zip opportuni- informational of seeing an provided that away is long- far forwards ties vista” enabled study “buena our The air line, that eyes. larger of hypothesis water for transparency selected the and above higher vision distance just Before vastly like from land. the hunted prey probably where for long at animals limbs head looking these the into land, crocodiles, of fins on top life their the in permanent to modified tripled sides eyes fish the that before from show shifted We and land. size on into living evolved slowly animals fish legged certain ago, years million 385 Starting Significance nlsso h eetv eiesit ihntete distri- tree the within shifts regime selective the of Analysis b eateto ehnclEgneig Northwestern Engineering, Mechanical of Department b PNAS n utsD Mobley D. 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ENGINEERING EVOLUTION PNAS PLUS group in Fig. 2) and ends with the connecting to the last Early tetrapod paleontology ancestor of the very first digited tetrapods, (inferred to have digits) and Acanthostega. During this phase of evolu- Assemble time-calibrated phylogeny of 59 taxa with skull tion, tetrapods entered a new adaptive zone that selected relative and orbit preservation that bracket water-land transition eye socket sizes that were a factor of 1.42–1.53 larger than the ancestral adaptive peak for fish, such as (Fig. 2). Fig. 3 shows the absolute and relative socket sizes for our dataset grouped according to the adaptive zones identified by the anal- 1 ... 59 ysis of selective regime shifts. We refer to the group before the increase in eye socket size as “finned tetrapods” (6). As shown in Fig. 3, there was a near tripling in the mean absolute socket size between the finned and digited tetrapods. We will show below that the enlargement of eye sockets supports the inference that eyes also approximately tripled in size. Create distribution of Measure eye socket and Interestingly, there was a reversion to small eye sockets in a 1,000 phylogenetic trees skull length group of animals that subsequently specialized for life underwa- to account for phylogenetic ter. This group is termed the “adelospondyl-colosteids” (7) (Figs. uncertainty 2 and 3). They have elongated -like bodies with tiny limbs (7, 8) and shrunken eye sockets similar to those of the finned tetrapods. Although there are other animals that are clearly semiaquatic within the digited tetrapods, the adelospondyl- colosteids are unique in the extent of aquatic specialization across the entire group and considered fully aquatic. Our discovery that the evolution of larger eye sockets occurred in animals that were primarily aquatic is in line with other criti- cal conclusions of the past several decades of early tetrapod pale- ontology, which has found that robust limbs evolved in primarily Use computational trait evolution to identify locations of aquatic animals (9, 10) and that fingers and toes evolved in primar- selective regime change across all 1,000 trees (Fig. 2) ily aquatic animals (11). Notably, the increase in eye size starting in the elpistostegalians coincided with a distinct change in the place- ment of eyes in this group. Although placed laterally in the early Computational visual ecology phase of tetrapod evolution, similar to other fish, the eyes moved into a position on the top of the head in this group (Eusthenopteron Compute light fields for Group socket lengths by compared with in Fig. 2). They are on raised “eye brows,” visual environments trait evolution results low bony prominences on the top of the skull (12–14). (Fig. 3) Computational Visual Ecology 1. finned 2. finned-transitional The adaptive landscape analysis in Fig. 2 shows the location and 3. digited magnitude of changes in relative eye socket size but is insufficient 4. digited-aquatic for understanding their possible bases. Larger sockets strongly correlate with larger eyes as shown by data on fish (SI Appendix, Estimating Eye and Pupil Size in Early Tetrapods and Fig. S4), Estimate pupil size for (15), (16), and primates (17). Evidence spanning finned & digited groups such a broad bracket of vertebrates shows that eye socket size in our group of ancient animals reliably captures what their eye size would have been. We can, therefore, estimate that the nearly Compute range, volume and derivatives for viewing threefold increase of absolute eye socket size (Fig. 3) corre- object across conditions using pupil estimates (Fig. 4) sponds to an almost threefold increase in eye size. However, what are these large eyes good for? To better understand the signifi- cance of the increase in eye size, estimates of the functional con- 10 cm disk sequences of these changes across environments that bracket the most likely possibilities (computational visual ecology) (Fig. 1) can be helpful. Larger eyes are strongly correlated with larger pupils (SI Appendix, Estimating Eye and Pupil Size in Early Tetrapods and 10 cm disk Fig. S4), a key variable in estimating visual capability. We selected four measures of visual function that we calculated as a function of pupil size: the distance at which a standard object, a 10-cm black disk, could be seen; the volume of space within which that same object could be seen given an estimate of the field of view; and the gains in both range and volume for a Fig. 1. The sequence of steps within early tetrapod paleontology as well as change in eye size (the derivatives of range and volume mea- computational visual ecology used for generating the results of this study. sures with respect to eye size). These measures were computed for the mean pupil size of the finned and digited groups ±1 SD as estimated from the absolute socket lengths for these groups in a phase of fundamental reorganization of the tetrapod body (Materials and Methods and Fig. 3A). plan. The transitional phase begins with the lineage leading to To make estimates of visual range and volume, we adapted a the last ancestor of the elpistostegalians (the finned transitional model of aquatic visual capability for pelagic fish from Nilsson

E2376 | www.pnas.org/cgi/doi/10.1073/pnas.1615563114 MacIver et al. Downloaded by guest on September 24, 2021 Downloaded by guest on September 24, 2021 upre eetv eiesit,wt soitdfcossgiyn h hnei y oktsz oprdwt h neta eie(eoetegreen the (before regime ancestral the with compared al. size et MacIver socket eye in for. change accounted tetrapods) the are aquatic signifying effects digited size factors log for body of associated brown after (PGLS) with dot) and regression shifts, digited, squares regime least for generalized blue selective phylogenetically transitional, supported from Methods finned residuals and for the yellow (Materials sizes, finned, socket variables for eye (red relative size-corrected circles body The represent trees. time-calibrated 1,000 of sample 2. Fig. vlto n dpielnsaeo eaieeesce iei al erpd umrzn u hlgntccmaaiesuypromdoe a over performed study comparative phylogenetic our summarizing tetrapods early in size socket eye relative of landscape adaptive and Evolution and .Tetikbace niaepstoso well- of positions indicate branches thick The Tetrapods). Early in Length Skull and Orbit of Scaling Appendix, SI PNAS | ulse nieMrh7 2017 7, March online Published 10 -transformed | E2377

ENGINEERING EVOLUTION PNAS PLUS et al. (18), which focused on first-order optical physics, and incor- A 70 porated contrast threshold into this framework. With this change, visual ranges in aquatic and above-water environments can be cal- culated using the same model. The visual system is modeled with 60 two channels: one that only sees an empty background and one that only sees a given target (18) (Materials and Methods and SI Appendix, Computational Visual Sensory Ecology Estimates). For 50 these reasons, our visual range estimates represent a best case scenario for visual detection in the absence of clutter. ~3x To compute the amount of light in the background and the light 40 from the target, we must model the likely visual environments 36 mm of the early tetrapods. Visual range for a given object differs greatly between aquatic and aerial environments, a fact related to 30 their dramatically different attenuation lengths. The attenuation length of a medium is defined as 1/c, where c is the sum of the absorption and scattering coefficients. After a beam of parallel 20 24 mm light rays travels a distance equal to the attenuation length, a frac-

Eye socket length (mm) tion of the light equal to the reciprocal of the base of the natural 14 mm logarithm—≈1/2.71 or 37%—remains at the given wavelength. 10 13 mm Aquatic attenuation lengths—for shorter wavelengths (bluish) that travel the farthest in clear water—vary in oceans from, at most, 24 m for the clearest deep water (19, 20) to meters for 0 coastal oceanic water (18, 20) and vary in freshwater from less than 2 m to a 10th of a meter (21–23). Shallow freshwater B 0.5 are where the majority of early tetrapods emerged (8, 9, 24–26). In dramatic contrast to the ancestral aquatic condition, the atten- 0.4 uation length for similar wavelengths of light in air is 25,000 m (27, 28) ( factor) (SI Appendix, Table S1)—between

) 10,000 and 100,000 times larger than the habitats similar to those

10 0.3 of the early tetrapods. Additional details on the visual ecology calculations are in Materials and Methods and SI Appendix. 0.2 0.20 Our results (Fig. 4) show that visual performance underwent 0.17 a massive increase with the shift from vision through water to vision through air. For the case of daytime viewing horizontally 0.1 in water through finned tetrapod eyes vs. air through digited 0.05 tetrapod eyes, the range increased by well over a factor of 100. 0.02 A conservative estimate of the total volume that our standard 0 object could be sensed within (Materials and Methods)—a more ethologically relevant measure (29, 30)—increases by just under -0.1 2 million times (Fig. 4 A1, A2, C1, and C2 and SI Appendix, row 2 in Table S4). Residual values (log We have performed a large number of sensitivity analyses -0.2 to determine how robust this conclusion is to our assumptions (Materials and Methods, Sensitivity Analyses). These analyses divide into perturbations of our baseline visual environment and -0.3 Digited- Finned Finned- Digited perturbations to our baseline visual . In terms of sen- transitional aquatic sitivity to environment, we note that a large increase in our mea- sures of visual performance occurs regardless of the diel activ- ity patterns of the early tetrapods. Our results are consequently agnostic to whether the increase in eye size was for the gain of sensitivity that this causes for the dim light vision models (- ing to larger range) or because larger eyes in full light lead to Fig. 3. Eye socket lengths across the taxa in Fig. 2 grouped by the regime an increase in acuity (also leading to larger range) (SI Appendix, shift analysis. (A) The mean (horizontal bars) absolute eye socket length of digited tetrapods was three times larger than that of their finned rel- Vision Model Limitations and Sensitivity Analysis and Table S1). atives, with the elpistostegalians (finned-transitional) midway. The dig- Our results are also unaffected by variations in water clarity. In ited tetrapods that returned to life underwater (adelospondyl-colosteids, terms of perturbations to our baseline visual physiology, changes digited-aquatic) reverted to a size similar to that of their finned rela- to a host of factors, including contrast threshold, photoreceptor tives. (B) Relative eye socket size was calculated as residuals from a phy- size, and dark noise level among others, have effects that are well logenetically informed regression of log10-transformed variables (Materi- outside of the range where our conclusions are affected. For the als and Methods) averaged over the full set of 1,000 trees. Positive resid- daylight vision case, these variations are shown in Fig. 4, solid uals indicate eye sockets larger than expected based on skull length, green fill. whereas negative residuals indicate eye sockets smaller than expected. The Bayesian OU results in Fig. 2 show the presence of an adaptive evo- lutionary process and provide estimates of the adaptive peak for each group (horizontal bars). The elpistostegalians entered a new selective are at their respective peak, reflecting a normal evolutionary pattern in regime but are lagging behind, because time was insufficient to accrue which trait values are dispersed around the optimal value. The Bayesian OU enough increases in eye socket size to reach the peak. However, the dig- findings show that there must have been a selective benefit from larger eye ited tetrapods are centered around their adaptive peak, except for the sockets in finned transitional and digited tetrapods, but uncovering its basis adelospondyl-colosteids. As expected for a diverse group, not all tetrapods requires modeling visual performance across likely environments.

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PNAS B1 | ulse nieMrh7 2017 7, March online Published and o uhrnei andfor gained is range much How B2) al S3 Table Appendix, SI D1 y vs. ai multiplier -axis D2). tadepth a at | E2379

ENGINEERING EVOLUTION PNAS PLUS Pederpes

Acanthostega

Tiktaalik

Panderichthys

Eusthenopteron

Fig. 5. A possible evolutionary scenario consistent with our results. Having invaded shallow waters, where the down-welling component of sunlight is sig- nificant, better visual range is obtained with eye sockets moved to the top of the skull, providing upward vision (Fig. 4A1) as shown here for . 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 elpistoste- galians, as shown here for Tiktaalik. Without correction for the differing 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 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 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.

basis of the increase in eye size, it coincides with another aerial with all other things being equal. This bur- change likely to improve energetics. In the transitional elpistoste- den is only slightly eased by the higher extraction efficiency of galians, there is evidence for another major bodily function mov- (43). ing from below to above water: respiration. In this group and It has been suggested that the anatomical features of the later taxa, there was an enlargement of breathing spiracles (also elpistostegalians—enlarged breathing spiracles at the top of the called otic notches) located behind the eyes (green in Fig. 5) skull and eyes on top of the skull on bony prominences—enabled (9, 13, 26, 40). The enlargement of spiracles occurred during a stealthy crocodilian-like predatory behavior (8, 13, 40), in which time of ’s history when oxygen levels trended downward animals are at the surface with their eyes and spiracles just (26, 41). For aquatic animals, the decline of oxygen out of the water, looking at the water–land interface for poten- was exacerbated by the fact that water has 1/30th of the oxygen tial prey to attack from the water (Tiktaalik in Fig. 5). Possible of air, while being 800 times denser (42, 43). Therefore, respi- prey include large terrestrial invertebrates that arrived approxi- ration with water requires 800 × 30 = 24,000 times more mass mately 50 My before vertebrates (33). Interestingly, one group of flux through respiratory tissues per unit of extracted oxygen than these invertebrates, the , developed chemical defense

E2380 | www.pnas.org/cgi/doi/10.1073/pnas.1615563114 MacIver et al. Downloaded by guest on September 24, 2021 Downloaded by guest on September 24, 2021 aIe tal. et MacIver ie atl,adloigvsa tml 5)i rprint the to proportion in (59) Mau- lateral stimuli acoustic, (60). visual looming close-range response and by synapses tactile, the line, activated and of cells, neurons command flexibility of thner the number to limited constrains reactions the involved ultrafast ms), enables (≈4 circuit maneuver stimuli neural escape this the initiate Although to (58). neuron Mauthner and the fish called cell is In escape water. and in by detection preda- reduced predator range between aids short delay that at the 55) , detection (29, after mode” evasion “reactive tor neural would the the of there portion of S4), that infrastructure for Table benefit selective , Appendix reduced been (SI have nocturnality) with (even com- to strategies. time reactive more simplest take the that than strategies pute benefit or control selective complex the prey more furthered toward of have paths would predators, multiple environ- from complex featuring away its (56) with geometry environment: land, our mental onto of Emergence features animals. unpredictable other most with the neces- 55) to not 53, respect (29, (although strategies million-fold enabling mode” mon- sunlight, 1 “deliberative space full complex increased sitating) in of water conditions volume of daylight total that in over the vision line, by water itored the above Making vision Decision of Optimal Temporal/Spatial Affects How large Appendix, with Range (SI strategy, effort mechanical control in behavioral savings different completely a in in later sys- much emerged imaging only . long-range which echolocation, the sensory other is animals of imaging only in lengths) tem evolution The body vision. the 100 aerial with than modality: changed (more limitation long-range percep- This first (ref. deliber- from 496). prey and being stemming p. predators mobile actions actions 55, as of stimuli—such for propor- dynamic sequence of challenging time tion the was requiring of (54) (53) length ated behavior the making driven to decision internally tional serial fashion, with just-in-time-to-act (52) a in Visual to ing Respect with Tetrapods Time Finned in Reaction Range Appendix, (SI of order was length the body ver- prey, on a land were at an which distances viewing lunge from as where habitats a originated, aquatic such tebrates or the in make, predator situation looming to normal the a needs to organism response most an escape the that to sensory respect decisions with extended crucial (51) over behavior making Stimulus-evoked decision ranges. because complex behavior, more animal allows on it effects large has vision Long-range Planning Neural and Reactive Circuits for Vision Long-Range of Implications than 41). more (26, Devonian had the levels in oxygen low , their with Notably, from the rebounded 50). 47–49), in (8, (8, group time adelospondyls spiracles this aquatic some by breathing of purely their exemption (Greererpeton lost possible this tetrapods the also finned of they the of 2), eyes size Fig. the mean the tetrapods did to aquatic revert only when digited Not time of the evolved. also group is it adelospondyl-colosteid Carboniferous unfavor- water, early the to within the oxygen that dissolved interesting tetrapod is low early including energetics, were able land on tebrates supple- significantly 10) (9, (46). movement limbs and by eyes mented larger tension for- land: brief for onto logical suited ays elpis- better certain the seem in that seen adaptations a life and exist tostegalians aquatic resolves fully Hunting for that manner specializations (45). the millipedes between -like predators In vertebrate a (44). deter in Devonian systems these lower today, the in systems smr eairbcm euae yln-ag vision long-range by regulated became behavior more As result can range visual in increase an instances, simple quite In inver- of predation vision-guided aerial and breathing air If s(7 hog eriigasnl ag caliber large single a recruiting through (57) ms ≈6 .Wt hr-ag iulsiuiarriv- stimuli visual short-range With ). .Atrteemergence the After ). in hlgntcpsto sucer emdlteucranycue ypoorly by caused uncertainty better the model on We unclear. focusing is phylogenetic position complete, phylogenetic existing less in is placed taxa. coverage known be stemward can Our that hypotheses. taxa which measurable (72)], most and Gephyrostegidae members (74)] and covers [ Dendrerpetontidae Amniota and group include [Edopoidea total Amphibia the to group crownward total identify the extended , of to well-preserved was used of scope was number phylogenetic the (47) For increase Database To covariance. 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(sensu as (ref. group aquatic such locomotion tetrapod largely members, terrestrial still basal for are more and well-suited thostega, whereas Devonian is 273), Upper that p. terrestri- 8, the of in watcheerid increase shows the occurred transi- the an example, 5) have For land of but tetrapods. to to yet, many Carboniferous assumed Early known water of generally exactly initial preferences is not the ality are The cover tetrapods Tetrapodomorpha. would early the that in Calibration. tion Time select and to Hypothesis, was Phylogenetic Taxa, of Selection Methods and Materials prospec- advantages. of habitat forms this to eventually, that central cognition and been tive terrestriality have may of vision land evolution long-range on the opportunities that the extended information to greatly of provided the 482), channel p. inexpensive activity—that 55, to and (ref. According hypothesis goal-directed resource. vista new buena of the the of exploitation sequence the enable extended would exe- an as weight- of cuting favor adaptations—such as neurobehavioral would bounty adaptations—such limbs—and resources the bearing morphological These of shores. evolving hunting the animals these and on leading was food viewing there awareness, invertebrate long-range water, visual from to of air animals of domain for index ever-expanding account refractive robust to an the more evolved in and mechanics change more optical the Because to while (69). land adjustments 68), onto small 11, forays enabling (9, evolved, hunt- gradually retained and fea- limbs aquatic” be line “primarily to water caused lifestyle tures the This above crocodiles. aquatic like by eyes ing driven likely their was surfacing size eye when tetrapods in between limbs increase digited size big with This in tetrapods evolved. when tripled and lived nearly fish eyes terres- lobe-finned early full that of show evolution the We facilitated triality. afar along from interest- edge opportunities the water’s changes fitness-enhancing the raises seeing anatomical landscape that sensory possibility these ing in envi- before change information tetrapods This the in occurred. early change high- we of dramatic 5) when a Fig. ronment happened was in there what and (summarized how results of fingers light our imagination with fish, our from limbs in transitioned complete central is of toes emergence the Although Conclusion and a (66) within (65). birds (67)—evolved ancestor both reptiles common in in well-studied occur less but to mammals understood plan- of 65)—now components (53, neuronal there- core ning vision, the long-range that hypothesize of we affordance fore, terrestrial this common fully With after recent arose. long most not animals Carboniferous their Late had the in in which ancestor origin (65), developmental mammals same and the hip- birds prospec- the has of on structure dependent forms This are other travel,” pocampus. time imagined like “mental error, are or cognition and possibilities tive trial error future and Vicarious which trial 64). vicarious in (53, by , as in such fitness, behavior that evasion enhance or to pursuit likely for are options multiple consider to able were 63). through up (62, vertebrates in including present amphibians, only are (61), looming of speed ihteeouino utbebancruty eti animals certain circuitry, brain suitable of evolution the With Caerorhachis and PNAS Neopteroplax | ulse nieMrh7 2017 7, March online Published eeecue,bcuetheir because excluded, were Pederpes and u goal Our | Acan- E2381 (Fig.

ENGINEERING EVOLUTION PNAS PLUS understood phylogenetic relationships for the baphetids, colosteids, and work for calculation of the optical stimulus is adapted from Nilsson et al. tristichopterids by forming polytomies. We used the stratigraphic ranges (18), which calculates visual range based on the assumption that there are of the fossils to time-calibrate the phylogeny with the paleotree package two separate channels that view the background and the target, where in R (75) (SI Appendix, Figs. S1, S2). For the basal tetrapodomorphs, strati- channel size is determined by the angular size of the target on the retina graphic range was based on the dating of the corresponding geological for- (given a particular photoreceptor arrangement) for optimal viewing. A tar- mation extracted from recent papers; for digited tetrapods, the Early Tetra- get is said to be visible at a distance if and only if the difference between the pod Database (47) was used. We used the International Chronostratigraphic photons that arrive from the target and the background are greater than Chart (76) to translate to absolute time. Time data were treated as mini- their combined Poisson noise with some reliability coefficient. This relation- mum and maximum bounds on single point dates, which were pulled from ship can be summarized by the equation: a uniform distribution. To account for the uncertainty involved in the exact q stratigraphic ranges, we repeated this process 1,000 times, resulting in a |Ntarget − Nbackground| ≥ R Ntarget + Nbackground , set of 1,000 time-calibrated phylogenies. The time scaling was performed with the “equal” method, which equally allocates time available on deeper where R is the reliability coefficient of 1.96 for 95% confidence, Ntarget branches to resolve the zero branch length problem (75, 77, 78). Polytomies is the number of photons detected arriving from the target/object, and were resolved randomly for each of the 1,000 trees. Nbackground is the number of photons detected arriving from the background. The number of photons detected due to background illumination and due Skull Measurements. Measurements were taken from published drawings to space-light between target and viewer is dependent on target width and images produced by experts in the field. Eye socket length is defined as [T (meters)], distance of object [range; r (meters)], the target’s apparent ˆ −2 −1 −1 the maximum length of the socket, except for in taxa in the digited tetrapod radiance [RO (photons meter second steradian )], background radi- ˆ −2 −1 −1 group featuring antorbital vacuities, for which the major axis of an ellipse ance [Rh (photons meter second steradian )], dilation or constriction fit to the orbit alone was used. We define skull length as the distance from of pupil to adjust for the amount of light [D (meters)], angular size of the the tip of the snout to the caudal margin of the bones at their target on the retina given that each photoreceptor is distributed on a square medial suture. The extracted measurements are shown in SI Appendix, Table array with equal weighting [(πT2)/(r24) (steradian)], and dark noise [false S5. Skull source data (images and drawings) used for measurement are in SI detections; χ (photoisomerizations per rod second−1)] (SI Appendix, Com- Appendix. putational Visual Sensory Ecology Estimates). Based on these dependencies, the numbers of photons detected by the channel viewing only the target Defining Eye Size in a Phylogenetic Comparative Framework. We chose the and the channel viewing only the background become implicit functions of Bayesian implementation of the OU method (5) to assess the adaptive sig- visual range and pupil diameter. Ranges based on this basic model of firing nificance of eye socket size differences in early tetrapods. Specifically, we threshold only account for the physical stimulus that reaches the eye, while analyzed whether the evolution of relative eye socket size includes changes neglecting contrast threshold of the eye. This simplification results in over- in the selective regime that may be congruent with periods of change in the estimating range. To predict the range at which an object becomes invisible, water to land transition. This approach does not require prior classification an observer’s contrast threshold has to be accounted for (80). Contrast fol- −σ(λ)r of samples into categories, which is advantageous given that it is currently lows the same attenuation law as light [CR = COe , where σ(λ) is the difficult to assign early tetrapods into discrete habitat categories. Bayesian extinction coefficient, CR is the apparent observed contrast, and CO is the OU instead agnostically infers whether changes in the selective regime of a actual contrast of the object]. If an object’s apparent contrast at a given trait occurred through evolutionary time and if so, along which branches in range is smaller than the observer’s contrast threshold, the object is said to the phylogeny these changes likely happened. It is also less prone to error invisible. contrast threshold values as a function of apparent lumi- for small phylogenetic comparative datasets (N < 100) than other methods nance and object angular size were taken from prior work (81). These values (79). We multiplied the traits (i.e., residuals from PGLS) by 10 to avoid com- were transformed into functions of apparent luminance, angular resolution, putational issues, because the combination of the small-valued residuals and and angular size of the object, where angular resolution was chosen to be the timespan of more than ≈100 My frequently yielded infinite likelihoods. the diffraction limit, allowing for an implicit pupil diameter and visual range The analysis was performed over the full set of 1,000 time-calibrated phylo- relationship. genies using both PGLS with Brownian Motion and OU correlation structure The 10-cm black disk size was chosen to be ethologically relevant for the residuals. Probabilistic prior settings were set to package defaults (α, σ2), 1- to 2-m body lengths typical of the early tetrapods, but the differences but the expected number of shifts in selective regime was set to 12 with an between aquatic and aerial performance reported here are insensitive to upper limit of 116, the number of branches in the tree. Each branch had the size chosen. We estimated the visual sensory volume (18, 29, 82) for this same prior probability to feature a regime shift anywhere along a branch, object by a spherical sector of specified (from visual range calcula- independent of branch length. The reversible jump Markov chain Monte tions), azimuth, and elevation. For aquatic viewing, we chose an azimuth Carlo simulation was run for 400,000 generations, of which the first 30% of 305◦ [170◦ per eye minus 35◦ binocular overlap typical of fish (83)] and was discarded as burn-in. We evaluated the adequacy of the priors by veri- an elevation of 60◦. For aerial vision, we chose an azimuth of 287◦ [156◦ fying that the estimated parameters were limited to a narrow portion of the for monocular vision and 25◦ binocular overlap typical of crocodile (ref. 84, entire prior distribution, specifically for the mean (α) and SD (σ2). To ensure pp. 293–294)] and an elevation of 30◦. The aerial vertical field of view of that independent chains had converged on similar regions in the parameter 30◦ is similar to the vertically compressed field of view provided by the hori- space, we used two approaches: (i) Gelman’s R for log likelihood, σ2, and α zontal foveal streak in contemporary crocodile eyes (≈33◦) (85), providing a and (ii) a plot of the posterior probabilities for shifts along branches against conservative estimate of aerial volume. We do not incorporate the additive each other, which should fall along a line with a slope of one if conver- effects of eye rotation or head yaw rotation. gence is reached (SI Appendix, Fig. S3). A shift in selective regime along a branch was considered well-supported if its respective posterior probability Optical Properties of Water for Aquatic Vision Estimates. Because early was outside the main distribution of all branches. Four branches with pos- tetrapods predominantly inhabited freshwater rivers, streams, or estuar- terior probabilities of 0.15–0.30 (17.4–34.8 times greater than their priors, ies (8, 9, 24–26), light-field simulations were done in waters with higher respectively) were chosen. These four branches consistently featured well- turbidity and absorption than the clearest ocean water. The Baseline River supported shifts across the entire tree set; branches in randomly resolved model (parameter values; SI Appendix, Table S3) used in Fig. 4 A1–D1 was polytomy regions did not show signatures of selective regime shifts. The selected, such that the attenuation length at 575 nm was between 0.02 choice of type of residuals did not influence the inferred evolutionary pat- and 2.7 m, the span of values for New Zealand and Alaskan rivers and tern of regime shifts. The mean estimate of α is 0.12, indicating a phyloge- lakes (22, 23). For example, the Baseline River model’s attenuation length of netic half-life of 5.79 My (6.33 My for OU residuals). These estimates sug- 0.46 m is around the first quartile of lake values and above the median gest that it took about 12 My to evolve from the ancestral value to the of river values. The water model parameter values were used as input to primary adaptive peak, which is congruent with the timespan of the regime the radiative transfer program HydroLight (version 5.3; Sequoia Scientific, shift zone from the first elpistostegalians to the last ancestor of the digited Inc.) to generate spectral radiance values [L(z, θ, φ, λ)], attenuation coeffi- tetrapods (Fig. 2). cient [c(λ) = a(λ) + b(λ)], and diffuse attenuation coefficient for radiance in the viewing direction [KL(z, θ, φ, λ)] for a water column of depth z = 8 m. Computational Visual Sensory Ecology Estimates. The numerical model for The full moon radiance spectrum (86) was rescaled to give a sea-level irra- both aquatic and aerial vision contains two components: calculation of the diance spectrum (that gives a total irradiance in the 400- to 700-nm band optical stimulus, which can overestimate visual range (particularly in the of 1 × 10−3 Wm−2), which was inputted into HydroLight. For simulation aerial case), and calculation of the effect of contrast threshold. The frame- purposes, it was assumed that the fractional contributions of direct and

E2382 | www.pnas.org/cgi/doi/10.1073/pnas.1615563114 MacIver et al. Downloaded by guest on September 24, 2021 Downloaded by guest on September 24, 2021 1 ireS,CakJ,Hthno R(02 he-iesoa ibjitmblt nthe in mobility Three-dimensional roseae. (2012) Tiktaalik JR Hutchinson of JA, fin Clack and SE, Pierce girdle Pelvic 11. (2014) FA Jenkins EB, Daeschler NH, Shubin 10. 3 ogJ,Gro S(04 h raetse nvrert itr:Apaleobiological A history: vertebrate in step greatest The (2004) MS Gordon JA, Long 13. Panderichthyid of and Description (1991) HP Schultze E, Vorobyeva 12. 4 akeizM ta.(05 aaoniomnso h ieindlmtswt earli- with dolomites Eifelian the light of Palaeoenvironments of (2015) al. estimates et photometer M, Narkiewicz and 24. disk Secchi (1991) J Edmundson J, Koenings 23. pelagic the in ecology visual Computational (2014) S Johnsen E, Warrant DE, Nilsson mam- of origin 18. the predates in Nocturnality (2014) L Schmitz birds. KD, Angielczyk fossil in features 17. performance visual fea- of bony estimates Quantitative associated (2009) L and Schmitz eye 16. the between relationship The (2009) MI Hall 15. fish Panderichthyid The (1985) M Arsenault H, Schultze 14. 2 aisCle J(98 esrn ae lrt ihabakdisk. black a with waters. clarity river water into Measuring (1988) penetration RJ light Davies-Colley Predicting M 22. (2008) Bass ed JW Optics, Nagels of RJ, Handbook water. Davies-Colley of 21. 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Sensitivity source. single no is there because diffuse, 100% as treated aIe tal. et MacIver 3 of irradiance total a spec- give irradiance agreement to an in conditions, photosyn- S was starlight by resulting provided For simulation) trum The (87). sky. the results sunlit of experimental a (result with for radiation as same available of the thetically distribution were angular sky relative moonlit and the moonlight by caused irradiance diffuse .DeclrE,Sui H ekn A(06 eointtao-iefihadthe and fish tetrapod-like Devonian A (2006) FA Jenkins NH, Shubin EB, Univ (Indiana Daeschler Tetrapods of 9. Evolution and Origin The Ground: Gaining (2012) JA Clack 8. of review A (2006) JA Clack M, Ruta 7. .L ,e l 21)Teeris nw tmttao rmteLwrDvna of Devonian Lower the from stem-tetrapod known earliest The (2012) al. et J, Lu interpreting 6. and inferring for method Bayesian novel A (2014) LJ Harmon JC, approach Uyeda modeling A 5. analysis: comparative Phylogenetic . (2004) AA of King analysis MA, comparative Butler the 4. and selection Stabilizing (1997) TF Hansen intervals Confidence 3. present: the predict to past the Using (2000) AR method. Ives comparative T, the Garland and Phylogenies 2. (1985) J Felsenstein 1. vlto ftettao oyplan. body tetrapod the of evolution IN). Bloomington, Press, Scotland. Lothian, West Kirkton, Sci Earth East of Carboniferous Lower the al erpdIchthyostega. tetrapod early USA Sci Acad Natl Proc China. data. comparative phylogenetic from landscapes 63(6):902–918. adaptive of dynamics the evolution. adaptive for Evolution methods. comparative 364. phylogenetic in equations regression for eiwo h s-erpdtransition. fish-tetrapod the of review Associates, Publishing 68–109. (Comstock pp Tetrapods NY), to Ithaca, Relationship Their on Comments with s erpdtakas(oyCosMutis Poland). Mountains, Cross Palaeoecol (Holy trackways turbidity. tetrapod est and color yellow of Effects lakes: 36(1):91–105. 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Acoerelative close Elpistostege—A aaoeg Palaeoclimatol Palaeogeogr 77(5):700–719. mNat Am ntRc(Hoboken) Rec Anat mNat Am rn o Edinb Soc R Trans inlOceanogr Limnol inlOceanogr Limnol IAppendix, SI 125(1):1–15. 155(3):346– t ytBiol Syst were ) SD ±1 1 oe L onde ,Pr ,KwlzkJ Godd J, Kowalczyk implica- J, its Park Y, and Donnadieu fishes DL, polypterid Royer in breathing 41. air Spiracular (2014) al. et JB, Graham potential 40. Action (2014) MR Markham SF, Perry MJ, Moorhead KM, Gilmour JE, Lewis 39. (2016) C Roesier E, Univ Boss (Princeton C, Ecology Mobley Visual (2014) 32. EJ Warrant trade-offs NJ, Marshall Energy-information S, Johnsen (2010) TW, Cronin NA 31. Patankar AA, and Shirgaonkar sensory MA, Omnidirectional Press, (2007) MacIver MA Toronto 30. MacIver of JW, Burdick (Univ ME, Nelson Atmosphere JB, the Snyder Through 29. Vision (1952) Optics, WEK of Handbook Middleton optics. Atmospheric 28. (1995) L Rothman J, Churnside D, Killinger 27. 6 cno ,e l 21)Ti s mrvspromneo otsbtae nmodels in substrates soft on performance improves use Tail (2016) al. et B, McInroe phys- 46. Biochemistry, (diplopoda): millipedes of defenses chemical The (2015) Euramerica: WA Shear of 45. Devonian lower the the from to millipedes Group Juliformian Sister (2006) a HM as Wilson Lungfish Indicates 44. Evidence Physiological (2009) Air-Breathing in ML Respiration Glass of Control 43. and Exchange Gas (2009) FT Rantin ML, Glass 42. evolution the and vision of cost energetic The (2015) EJ Warrant R, Softley evolution D, the Moran on sensory selective 38. a of as processing limitation Energy and (2008) coding SB Laughlin the JE, Niven on constraint 37. a advantage as unique Energy A (2012) (2001) N SB Shashar Laughlin R, to 36. Hanlon eye S, an Johnsen for EJ, required Warrant time DE, the Nilsson of estimate 35. pessimistic A (1994) Myri- S the Pelger of DE, phylogeny Nilsson and record 34. geological The (2010) GD Edgecombe WA, Shear 33. tetrapod the of origin the and breathing, change, climate Devonian (2007) evolution. JA tetrapod Clack Devonian 26. for hypothesis Woodland (2011) GJ Retallack 25. 9 arl 16)Anwfml fCroieosamphibians. Carboniferous of family new A (1969) R tetrapod Carroll of 49. half (2010) first RE The Lombard JR, (2013) Bolt M 48. Sakamoto AM, Dunhill M, Ruta MJ, Benton 47. n h upr fNrhetr nvriydrn ...s3m academic 3-mo M.A.M.’s Foundation during M.A.M.), University Science leave. (to Northwestern National IOB-0846032 of PECASE support by and the funded and M.A.M.) (to partially ear- 1456830 an was IOS-ORG Gallio, on work Grants Marco feedback study. This valuable gave this draft. Wainwright in lier C. used Peter spectra and Paulin, starlight Michael the providing S for thank We versity) Chicago). of control (University of Coates ball reconstruction Michael and the Maryland), coding of with of assistance (University image for for The Uyeda Josef Abraham package. thank bayou also Ian the We S8). and Fig. , Appendix collection (SI example data with tance ACKNOWLEDGMENTS. in provided Analysis. are underwater details nominal Additional our capability. visual decrease always 4 values (Fig. metrics Moreover, alternate substitutions. our in value that viewing alternative to daylight given robust and are water conclusions within Our viewing per- air. only upward was daylight analysis but sensitivity for similarly model formed for computed vision is The performed value. bound is maximum upper the estimate The using bound mm). (1–25 alternative lower diameter all a This pupil diameter. across selecting each pupil 4A1) first Fig. that by corresponding for at the obtained range values for are (e.g., value measure 4 minimum performance the Fig. visual finding in then bounds and lower diameter pupil fill in provided green is The and S2. found was difference percentage the in o eilrsiaini tmtetrapods. stem in respiration aerial for tions rates. firing high at efficiency in trade-off a Neurosci reveal J level organismal the at energetics Princeton). Press, sensing. and movement between fish. electric an in volumes motor 44.1–44.49. Toronto). pp 1, Vol Ed 2nd York), New (McGraw-Hill, M Bass ed feryvrert adlocomotors. land vertebrate early of ecology. and iology . the in of 80(4):638–649. timing the for Implications 161–177. pp Berlin), (Springer, CS Wood LM, Glass eds Vertebrates, Land 99–119. pp Berlin), (Springer, CS Wood LM, Glass eds , 314(9):1259–1283. O and cavefish. Mexican eyeless of systems. sensory of information. . giant in eyes giant for evolve. apoda. 2016. 17, September Accessed www.oceanopticsbook.info. at Available Radiances. group. stem 119(3):235–258. 537–548. Iowa. of the quality. record fossil and Palaeoecol proxies, sampling evolution, 2 rhoo tutDev Struct rcBo Sci Biol Proc siae rmteln-emgohmclmdlGEOCARBSULF. model geochemical long-term the from estimates 34(1):197–201. 372:18–41. nerCm Biol Comp Integr ,i sqiepsil htw r vrsiaigaquatic overestimating are we that possible quite is it A1–D1), urOi Neurobiol Opin Curr x Biol Exp J ice ytEcol Syst Biochem 256(1345):53–58. etakSotShpradOii am o assis- for Carmo Olivia and Schaper Scott thank We Paleontol J e ooti erpdfrom tetrapod colosteid new a hiemstrae, Deltaherpeton c Adv Sci PNAS urBiol Curr 211(11):1792–1804. 39(2-3):174–190. 47(4):510–523. LSCmu Biol Comput PLoS Biol PLoS 11(4):475–480. ca pis ih n aimty Visualizing Radiometry, and Light Optics, Ocean Eusthenopteron 1(8):e1500363. | Science 84(6):1135–1151. 61:78–117. 22(8):683–688. ulse nieMrh7 2017 7, March online Published 5(11):2671–2683. 353(6295):154–158. a Commun Nat rsY(04 ro nlsso CO of analysis Error (2014) Y eris ´ 6(5):e1000769. Acanthostega scuts fJh Merck John of courtesy is neJhsn(ueUni- (Duke Johnsen onke ¨ aaoeg Palaeoclimatol Palaeogeogr IApni,Sensitivity Appendix, SI 5:3022. Table Appendix, SI Palaeontology scuts of courtesy is Paleontol J | mJSci J Am E2383 Geol J 12(4): 2

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