Variation in daily activity patterns facilitates temporal partitioning of habitat and resources among species. Knowledge of temporal niche partitioning in paleobiological systems has been limited by the difficulty of obtaining reliable information about activity patterns from fossils. On the basis of an analysis of scleral ring and orbit morphology in 33 archosaurs, including dinosaurs and pterosaurs, we show that the eyes of Mesozoic archosaurs were adapted to all major types of diel activity (that is, nocturnal, diurnal, and cathemeral) and provide concrete evidence of temporal niche partitioning in the Mesozoic. Similar to extant amniotes, flyers were predominantly diurnal; terrestrial predators, at least partially, nocturnal; and large herbivores, cathemeral. These similarities suggest that ecology drives the evolution of diel activity patterns.
The genetic mechanisms underlying regressive evolution-the degeneration or loss of a derived trait-are largely unknown, particularly for complex structures such as eyes in cave organisms. In several eyeless animals, the visual photoreceptor rhodopsin
BackgroundAmbient light levels are often considered to drive the evolution of eye form and function. Diel activity pattern is the main mechanism controlling the visual environment of teleost reef fish, with day-active (diurnal) fish active in well-illuminated conditions, whereas night-active (nocturnal) fish cope with dim light. Physiological optics predicts several specific evolutionary responses to dim-light vision that should be reflected in visual performance features of the eye.ResultsWe analyzed a large comparative dataset on morphological traits of the eyes in 265 species of teleost reef fish in 43 different families. The eye morphology of nocturnal reef teleosts is characterized by a syndrome that indicates better light sensitivity, including large relative eye size, high optical ratio and large, rounded pupils. Improved dim-light image formation comes at the cost of reduced depth of focus and reduction of potential accommodative lens movement. Diurnal teleost reef fish, released from the stringent functional requirements of dim-light vision have much higher morphological and optical diversity than nocturnal species, with large ranges of optical ratio, depth of focus, and lens accommodation.ConclusionsPhysical characteristics of the environment are an important factor in the evolution and diversification of the vertebrate eye. Both teleost reef fish and terrestrial amniotes meet the functional requirements of dim-light vision with a similar evolutionary response of morphological and optical modifications. The trade-off between improved dim-light vision and reduced optical diversity may be a key factor in explaining the lower trophic diversity of nocturnal reef teleosts.
Eyes are expected to be adapted to the physical characteristics of the visual environment, yet previous analyses failed to corroborate this observation. We demonstrate that nocturnal, crepuscular/cathemeral, and diurnal activity patterns occupy distinct areas in morphospace and are identified with high accuracies based on a discriminant analysis of visual performance features. Not only nocturnal and diurnal diel activity patterns are reflected in macroscopic morphology of the eyeball, but also the crepuscular/cathemeral patterns. The eyeball morphology of the latter was believed to be undistinguishable between diurnal and nocturnal types. We show that all three categories can be delineated with high accuracies.
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 ...
Nocturnality is widespread among extant mammals and often considered the ancestral behavioural pattern for all mammals. However, mammals are nested within a larger clade, Synapsida, and non-mammalian synapsids comprise a rich phylogenetic, morphological and ecological diversity. Even though non-mammalian synapsids potentially could elucidate the early evolution of diel activity patterns and enrich the understanding of synapsid palaeobiology, data on their diel activity are currently unavailable. Using scleral ring and orbit dimensions, we demonstrate that nocturnal activity was not an innovation unique to mammals but a character that appeared much earlier in synapsid history, possibly several times independently. The 24 Carboniferous to Jurassic non-mammalian synapsid species in our sample featured eye morphologies consistent with all major diel activity patterns, with examples of nocturnality as old as the Late Carboniferous (ca 300 Ma). Carnivores such as Sphenacodon ferox and Dimetrodon milleri, but also the herbivorous cynodont Tritylodon longaevus were likely nocturnal, whereas most of the anomodont herbivores are reconstructed as diurnal. Recognizing the complexity of diel activity patterns in non-mammalian synapsids is an important step towards a more nuanced picture of the evolutionary history of behaviour in the synapsid clade.
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