Continuous and Regular Expansion of a Distributed Visual System in the Eyed ChitonTonicia lebruni

Abstract

Chitons have a distinctive armature of eight articulating dorsal shells. In all living species, the shell valves are covered by a dense array of sensory pores called aesthetes, but in some taxa, a subset of these are elaborated into lensed eyes, which are capable of spatial vision. We collected a complete ontogenetic series of the eyed chiton Tonicia lebruni to examine the growth of this visual network, and found that it expands continuously as eyes are added at the margin during shell growth. Our dataset ranged from a 2.58 mm juvenile with only 16 eyes to adults of 25-31 mm with up to 557 eyes each. This allowed us to investigate the organization and potential constraints therein of these sensory structures and their development. Chiton eyes are constrained to a narrowly defined region of the shell, and data from T. lebruni indicate they are arranged roughly bilaterally symmetrically. We found deviations from symmetry of up to 10%, similar to irregularity reported in some other animals with multiplied eyes.Distances separating successive eyes indicate that, while shell growth slows during the life of an individual chiton, eyes are generated at regular time intervals. Although we could not identify a specific eye-producing tissue or organ, we propose that the generation of new eyes is controlled by a clock-like mechanism with a stable periodicity.The apparent regularity and organization of the chiton visual system is far greater than previously appreciated. This does not imply the integration of shell eyes to form composite images, but symmetry and regular organization could be equally beneficial to a highly duplicated system by ensuring even and comprehensive sampling of the total field of view.

Variation in eye abundance among scallops reveals ontogenetic and evolutionary convergence associated with life habits

“…To our knowledge, few studies have investigated allometric predictors for distributed visual systems so far. For example, eyes are formed at regular time intervals during the life span of the chiton Tonicia lebruni , resulting in hundreds of eyes in large, adult animals (Sigwart and Sumner‐Rooney 2021). However, the relationship between eye number and eye size is largely unexplored in distributed visual systems, leaving open questions regarding possible patterns and trade‐offs.…”

“…Consequently, the capacity to operate at lower light intensities and contrasts is not only advantageous to respond to predators without causing false alarms but also to obtain spatial information (Land 1968). For example, the regular organization of eyes on the shell plates of chitons is likely associated with an even and comprehensive sampling of the total field of view (Sigwart and Sumner‐Rooney 2021).…”

“…2020; Sumner‐Rooney et al. 2020; Sigwart and Sumner‐Rooney 2021). Unlike paired, cephalic eyes, distributed visual systems prompt unique questions regarding network properties beyond those of individual photoreceptor organs (Bok et al.…”

“…First, in many distributed visual systems, new optical units are added at regular time intervals as the body grows (Sigwart and Sumner‐Rooney 2021). This condition suggests an allometric relationship, generally defined by how a phenotypic trait scales with body size at different biological levels (Gould 1966; Cheverud 1982).…”

“…Distributed visual systems have attracted recent attention in investigating the functional link between ecology and evolution (Birk et al 2018;Audino et al 2020;Sumner-Rooney et al 2020;Sigwart and Sumner-Rooney 2021). Unlike paired, cephalic eyes, distributed visual systems prompt unique questions regarding network properties beyond those of individual photoreceptor organs (Bok et al 2017).…”