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Vision and Bioluminescence in Cephalopods by Kate Nicole Thomas Department of Biology Duke University Date:_______________________ Approved: ___________________________ Sönke Johnsen, Supervisor ___________________________ Fred Nijhout ___________________________ Susan Alberts ___________________________ William Kier ___________________________ Craig McClain Dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Biology in the Graduate School of Duke University 2018 ABSTRACT Vision and Bioluminescence in Cephalopods by Kate Nicole Thomas Department of Biology Duke University Date:_______________________ Approved: ___________________________ Sönke Johnsen, Supervisor ___________________________ Fred Nijhout ___________________________ Susan Alberts ___________________________ William Kier ___________________________ Craig McClain An abstract of a dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Biology in the Graduate School of Duke University 2018 Copyright by Kate Nicole Thomas 2018 Abstract In the deep pelagic ocean, there are no structures to serve as hiding locations, and visual interactions among animals can occur in all directions. The light environment in the midwater habitat is highly structured due to the scattering and absorption of light. Downwelling daylight dims exponentially, becomes bluer, and gets more diffuse with depth. This structured light environment means that an animal’s depth and viewing direction greatly affect the distances at which it can see visual targets such as potential prey or approaching predators. Additionally, this light environment mediates the visibility of bioluminescent camouflage and signals. My dissertation examines how the midwater light environment affects the ecology and evolution of vision and bioluminescence through an examination of cephalopods, a highly visual group that exhibits a broad diversity of eye adaptations and multiple evolutionary origins of bioluminescence. My research investigates (1) vision and behavior in a deep-sea squid with dimorphic eyes, (2) depth-dependent patterns in cephalopod eye size and visual range, and (3) evolutionary dynamics in bioluminescent cephalopods. First, I examined the function of differently sized and shaped left and right eyes in midwater “cockeyed” squids (Histioteuthis and Stigmatoteuthis) by using in-situ video footage from remotely operated vehicles at the Monterey Bay Aquarium Research Institute to quantify eye and body orientations. I found that the larger left eye points upward toward downwelling daylight and may be useful for spotting silhouettes of potential prey, while the smaller right eye points slightly downward into darkness, and iv may be specialized for detecting bioluminescent flashes. I also found that 65% of adult cock-eyed squids had a yellow pigment in the lens of the larger left eye, which may be used to break the counterillumination camouflage of their prey. Visual modeling showed that the visual gains provided by increasing eye size were much higher for an upward-oriented eye than for a downward-oriented eye, which may explain the evolution of this unique visual strategy. This work has been published (Thomas et al. 2017). Second, I examined the effects of depth and optical habitat on eye scaling across cephalopod species by collecting morphological measurements from 124 species at the Smithsonian Institution’s National Museum of Natural History and constructing a corresponding database of species depth distributions and light habitats from the literature. I then compared absolute and relative eye sizes to body sizes and light habitats and found that cephalopods occupying dim light habitats had significantly higher eye investment than those occupying bright or dark (abyssal) habitats. My results provide evidence for increased investment in eye size with depth through the midwater habitat until dim, downwelling daylight disappears. Finally, I examined the potential effects of the midwater light habitat on evolutionary dynamics among bioluminescent cephalopods using comparative evolutionary methods. I constructed a database of cephalopod daytime depths (as a proxy for light level), body sizes, eye investment, and bioluminescence from published records, then used a published phylogeny and Brownian Motion and Ornstein- v Uhlenbeck likelihood models of continuous character evolution in discrete selective categories to determine a best-fit model of evolution. I found evidence that bioluminescent and non-bioluminescent cephalopods are under different selective regimes with different trait optima for depth, body size, and eye investment. Together, this work shows that the structured, directional light environment of the pelagic midwater realm affects visual ecology at organismal, macroecological, and macroevolutionary levels. vi Dedication For my best friend and longest-serving editor. vii Contents Abstract ......................................................................................................................................... iv List of Tables ................................................................................................................................ xii List of Figures ............................................................................................................................ xiii Acknowledgements .................................................................................................................... xv 1. Introduction ............................................................................................................................... 1 1.1 Project Summary............................................................................................................... 1 1.2 Background ....................................................................................................................... 2 1.3 Study system ..................................................................................................................... 4 2. Two eyes for two purposes: in situ evidence for asymmetric vision in the cockeyed squids Histioteuthis heteropsis and Stigmatoteuthis dofleini ....................................................... 5 2.1 Introduction ....................................................................................................................... 5 2.2 Methods ........................................................................................................................... 10 2.2.1 Study system .............................................................................................................. 10 2.2.2 Eye orientations ......................................................................................................... 11 2.2.3 Posture and body orientations ................................................................................ 12 2.2.4 Lens filtering .............................................................................................................. 13 2.2.5 Depth ........................................................................................................................... 13 2.2.6 Visual modeling ......................................................................................................... 14 2.3 Results .............................................................................................................................. 15 2.3.1 Eye orientations ......................................................................................................... 15 2.3.2 Posture and body orientation .................................................................................. 17 2.3.3 Lens filtering .............................................................................................................. 18 2.3.4 Depth ........................................................................................................................... 19 viii 2.3.5 Visual modeling ......................................................................................................... 20 2.4 Discussion ........................................................................................................................ 22 3. Eye scaling, eye investment, and visual range in cephalopods........................................ 28 3.1 Introduction ..................................................................................................................... 28 3.2 Methods ........................................................................................................................... 32 3.2.1 Morphological Data .................................................................................................. 32 3.2.2 Ecological Data .......................................................................................................... 33 3.2.3 Morphological Scaling Relationships ..................................................................... 34 3.2.4 Effects of Light Habitat on Eye Scaling .................................................................. 35 3.2.5 Visual Modeling ........................................................................................................ 36 3.3 Results .............................................................................................................................. 42 3.3.1 Morphological Scaling Relationships ....................................................................
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