Evolution of Large Eyes in Stromboidea (Gastropoda): Impact of Photic Environment and Life History Traits

Abstract

Eyes within the marine gastropod superfamily Stromboidea range widely in size, from 0.2 to 2.3 mm, the latter being the largest known eyes of any gastropod. However, the evolutionary pressures underlying this variation remain unknown. Here, we use the wealth of material available in museum collections to explore the impact of ecological factors that affect light availability (ocean depth, turbidity and diel activity) on the evolution of eye size and structure within Stromboidea. We construct the most taxonomically extensive phylogeny of Stromboidea to date as a framework to investigate these relationships. Our results suggest that depth is a key light-limiting factor in stromboid eye evolution; here, increasing water depth is correlated with increasing aperture width relative to lens diameter (p = 0.043), and therefore an increasing investment in sensitivity in dim light environments. In the clade containing all large-eyed families (Strombidae, Rostellariidae and Seraphsidae), cathemeral species had wider eye apertures relative to lens sizes than diurnal species (p = 0.002), thereby prioritising sensitivity over resolution. These cathemeral species also had smaller body sizes than diurnal species (p = 0.002); this may suggest that animals with smaller shells are more vulnerable to shell-crushing predators, and therefore avoid the higher predation pressure experienced by animals active during the day. Within the large-eyed stromboid clade, ancestral state reconstruction estimates that absolute eye size increased above 1 mm twice independently. Due to the high energetic investment associated with large eye sizes, this repeated increase in eye size suggests that higher performance vision is important in behavioural tasks within these families. In addition, we note that species with more robust escape responses tend to have larger eyes than those that do not: for example, strombids have 1.79 times the eye size that would be expected from their body size (based on Stromboidea as a whole) and are known to display either a rapid escape response from an approaching predator or withdrawal into the shell. By contrast, the small-eyed xenophorids have 0.59 times the expected eye size, and are only known to withdraw when threatened.