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. fish-tetrapod transition | vision | visual ecology | terrestriality | prospective cognition B efore terrestrial vertebrates arose, their ancestors inhabited underwater environments, where vision is highly compromised compared with vision above water. The visual difference between life in water and life above it is comparable with driving fast on a foggy road, where our responses must be rapid and simple, vs. driving in clear daylight conditions, where deliberation over more complex choices is enabled by the vast increase in sensory range. Nonetheless, although an immense quantity of work has been done on the emergence of limbs during the evolution of land vertebrates, how visual capability changed during the transition from water to land has not been explored. In part, this lack of exploration is because computational visual ecology-necessary to interpret the fossil data-has not been combined with early tetrapod paleontology. Through combining these disciplines, here we probe the evolutionary history of the switch in our visual sensory ecology from water to air. Surprisingly, our results show that eyes tripled in size just before full-time life on land evolved. Convergent lines of evidence, including our own, strongly support the hypothesis that a crocodilian ecotype-using the greatly enhanced visual capabilities conferred by vision through air to prey on the bounty of unexploited invertebrates that long preceded the vertebrates onto ...
It is uncontroversial that land animals have more elaborated cognitive abilities than their aquatic counterparts such as fish. Yet there is no apparent a-priori reason for this. A key cognitive faculty is planning. We show that in visually guided predator-prey interactions, planning provides a significant advantage, but only on land. During animal evolution, the water-to-land transition resulted in a massive increase in visual range. Simulations of behavior identify a specific type of terrestrial habitat, clustered open and closed areas (savanna-like), where the advantage of planning peaks. Our computational experiments demonstrate how this patchy terrestrial structure, in combination with enhanced visual range, can reveal and hide agents as a function of their movement and create a selective benefit for imagining, evaluating, and selecting among possible future scenarios-in short, for planning. The vertebrate invasion of land may have been an important step in their cognitive evolution.
Decisions made by mammals and birds are often temporally extended. They require planning and sampling of decision-relevant information. Our understanding of such decision making remains in its infancy compared to simpler, forced choice paradigms. However, recent advances in algorithms supporting planning and information search provide a lens through which we can explain neural and behavioural data in these tasks. We review these advances to obtain a clearer understanding for why planning and curiosity originated in certain species but not others; how activity in the medial temporal lobe, prefrontal and cingulate cortices may support these behaviours; and how planning and information search may complement each other as means to improve future action selection.
4Other than formerly land-based mammals such as whales and dolphins that 5 have returned to an aquatic existence, it is uncontroversial that land animals 6 have developed more elaborated cognitive abilities than aquatic animals. Yet 7 there is no apparent a-priori reason for this to be the case. A key cognitive 8 faculty is the ability to plan. Here we provide evidence that in a dynamic 9 visually-guided behavior of crucial evolutionary importance, prey evading a 10 predator, planning provides a significant advantage over habit-based action 11 selection, but only on land. This advantage is dependent on the massive in-12 crease in visual range and spatial complexity that greeted the first vertebrates 13 to view the world above the waterline 380 million years ago. Our results have 14 implications for understanding the evolutionary basis of the limited ability of 15 animals, including humans, to think ahead to meet slowly looming and distant 16 threats, toward a neuroscience of sustainability. 17 Introduction 18The emergence of vertebrates on to land over 350 million years ago was preceded by a massive 19 increase in visual range when their eyes moved to the top of the head to look over the water 20 surface and tripled in size (1). The optical difference between inland waters-where transitional 21 tetrapods are thought to have emerged-and air resulted in more than a 100-fold increase in 22 visual range, from about a body length to hundreds of body lengths ahead (1, 2). Within the 23 greatly enhanced range of Devonian aerial vision was rich structure provided by vegetation 24 (3) and other terrestrial features, providing complex visual scenes to animals (Supplementary 25 Fig. 1A-B). In this study we will test the hypothesis that for visually guided behaviors, the 26 2 increase in visual range and observed environmental complexity that accompanied the onset of 27 terrestriality advantaged the evolution of neural circuitry for deliberation over multiple futures 28 (4, 5). 29This study builds on investigations into the neural basis of action selection that suggest the ex-30 istence of two competing, distinct, and largely parallel decision making systems: habit-based 31 action selection, and plan-based action selection (6, 7). These two control paradigms have 32 primarily been associated with the lateral striatum and its dopaminergic afferents (8-10) for 33 habit, and the interaction between hippocampus and the prefrontal cortex (nidopallium cau-34 dolaterale in birds (11)) (12-19) for planning. The similarity between lamprey (jawless fish 35 that preceeded mammals by 560 million years) and mammalian basal ganglia in the direct and 36 indirect pathways of the dopamine expressing striatal projection neurons (20-22) suggests that 37 this structure-and thus the habit-based action selection system it supports-evolved very early 38 on in vertebrate evolution. 39 In mammals, planning has been related to the phenomenon of nonlocal spatial representations 40 in hippocampal activity. Two quintessential examples of this phen...
Prior to the vertebrate invasion of land, aquatic vision provided short range sensing with low contrast scenes. Once on land, aerial vision provided a 100-fold increase in range with high contrast scenes. This change in sensory ecology due to emergence onto land may have provided a selective advantage to those animals that were able to imagine alternative action sequences toward distant goals. To explore the relationship between sensory ecology and the utility of planning, we developed a simulation of predator-prey dynamics where we controlled visual range, planning depth, and environmental complexity. Simulations show that for prey with short visual range, increased planning results in a negligible change in survival rate with increased environmental complexity. However, at longer visual ranges, survival rate is strongly correlated with planning depth and environmental complexity, with peak survival rate occurring at high complexity and planning depth. These data suggest that planning is an adaptation to long range sensing enabled by terrestrial habitats 385 million years ago. Our results point to future research into the limitations on our temporal and spatial range of prospective cognition, a possible result of environments in which we have evolved, to raise awareness and create circumventions for looming existential threats.
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