A new computational model illuminates the extraordinary eyes of Phronima

Vision in the midwater of the open ocean requires animals to perform visual tasks quite unlike those of any other environment. These tasks consist of detecting small, low contrast objects and point sources against a relatively dim and uniform background. Deep-sea animals have evolved many extraordinary visual adaptations to perform these tasks. Linking eye anatomy to specific selective pressures, however, is challenging, not least because of the many difficulties of studying deep-sea animals. Computational modelling of vision, based on detailed morphological reconstructions of animal eyes, along with underwater optics, offers a chance to understand the specific visual capabilities of individual visual systems. Prior to the work presented here, comprehensive models for apposition compound eyes in the mesopelagic, the dominant eye form of crustaceans, were lacking. We adapted a model developed for single-lens eyes and used it to examine how different parameters affect the model's ability to detect point sources and extended objects. This new model also allowed us to examine spatial summation as a means to improve visual performance. Our results identify a trade-off between increased depth range over which eyes function effectively and increased distance at which extended objects can be detected. This trade-off is driven by the size of the ommatidial acceptance angle. We also show that if neighbouring ommatidia have overlapping receptive fields, spatial summation helps with all detection tasks, including the detection of bioluminescent point sources. By applying our model to the apposition compound eyes of Phronima, a mesopelagic hyperiid amphipod, we show that the specialisations of the large medial eyes of Phronima improve both the detection of point sources and of extended objects. The medial eyes outperformed the lateral eyes at every modelled detection task. We suggest that the small visual field size of Phronima's medial eyes and the strong asymmetry between the medial and lateral eyes reflect Phronima's need for effective vision across a large depth range and its habit of living inside a barrel. The barrel's narrow aperture limits the usefulness of a large visual field and has allowed a strong asymmetry between the medial and lateral eyes. The model provides a useful tool for future investigations into the visual abilities of apposition compound eyes in the deep sea. Author summary How do animals see the world? This is particularly an interesting question when the animal's eyes look very different from our own, or if they inhabit an environment that is visually very different from ours. Biologists approach this question by seeking to determine not only how animal eyes function but also what selective pressures led to the evolution of their eyes. Understanding the eyes of deep-sea animals is particularly intriguing and more challenging than usual because their visual world is so dramatically different from our own and they are inaccessible and therefore hard to study. Understanding their visual capabilities by behavioural or physiological experiments is at best extremely challenging and often impossible. However, modelling of their visual abilities, by combining knowledge about ocular anatomy with information about the way light propagates in the deep sea, is comparatively tractable. Here we present a computational model that predicts the ability of apposition compound eyes (eyes that are widely found in many arthropod invertebrates) to detect salient visual targets in the deep sea between 200 and 700 m below the surface. We use this model specifically to examine the extraordinary 'double eyes' of the midwater hyperiid amphipod Phronima that have perplexed scientists for decades. This allowed us to put forward a new hypothesis about the selective pressures that have led to Phronima's unusual eyes. The predictive model we present here also provides a framework for future assessments of visual performance of apposition compound eyes in other deep-sea animals.

Automated summary

Vision in the midwater of the open ocean is unique and requires animals to have extraordinary visual adaptations. Computational modelling can help us understand the specific visual capabilities of deep-sea animals. The study presents a model to predict the ability of apposition compound eyes to detect visual targets in the deep sea and provides insights into Phronima's unusual eyes.