Abstract

Animal eyes typically possess specialized regions for guiding different behavioural tasks within their specific visual habitat. These specializations, and evolutionary changes to them, can be crucial for understanding an animal's ecology. Here, we explore how the visual systems of some of the smallest flying insects, fungus gnats, have adapted to different types of forest habitat over time (approx. 30 Myr to today). Unravelling how behavioural, environmental and phylogenetic factors influence the evolution of visual specializations is difficult, however, because standard quantitative techniques often require fresh tissue and/or provide data in eye-centric coordinates that prevent reliable comparisons between species with different eye morphologies. Here, we quantify the visual world of three gnats from different time periods and habitats using X-ray microtomography to create high-resolution three-dimensional models of the compound eyes of specimens in different preservation states—fossilized in amber, dried or stored in ethanol. We present a method for analysing the geometric details of individual corneal facets and for estimating and comparing the sensitivity, spatial resolution and field of view of species across geographical space and evolutionary time. Our results indicate that, despite their miniature size, fungus gnats do have variations in visual properties across their eyes. We also find some indication that these visual specializations vary across species and may represent adaptations to their different forest habitats. Overall, the findings demonstrate how such investigations can be used to study the evolution of visual specializations—and sensory ecology in general—across a range of insect taxa from different geographical locations and across time.

Highlights

  • Vision provides essential information for guiding the behaviour of many animals and is often critical for orchestrating both movement through and interactions with their environment [1]

  • To analyse the visual world of fungus gnat species from different geographical locations and evolutionary time periods, we further developed our method such that, rather than requiring volumetric data from specially prepared fresh samples, we are able to analyse the corneal surface of specimens from taxonomic collections in different states of preservation, from naturally preserved specimens that are fossilized in amber or dried and from specimens preserved in ethanol

  • Using our analysis technique based on microCT images of the heads and eyes of insects, we calculated the visual properties of fungus gnat eyes from the three-dimensional structure, shape and size of each individual corneal facet

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Summary

Introduction

Vision provides essential information for guiding the behaviour of many animals and is often critical for orchestrating both movement through and interactions with their environment [1]. Less well understood, factor affecting eye adaptations is the visual environment itself, which may have features that vary dramatically between habitats—consider, for example, the difference in visual information available in a bright open meadow compared with that of a dim cluttered rainforest [2]. To acquire the visual information necessary for guiding behaviour in different environments, animal eyes are likely to have habitat-specific specializations. Knowledge about the relationship between vision and habitat and the evolutionary factors shaping visual specializations is poor, yet it is critical if we are to understand the sensory ecology of different species and to predict if/how they will adapt to and survive both long- and short-term habitat changes

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