Summary The mesopelagic habitat is a vast space that lacks physical landmarks and is structured by depth, light penetration, and horizontal currents. Solar illumination is visible in the upper 1,000 m of the ocean, becoming dimmer and spectrally filtered with depth—generating a nearly monochromatic blue light field 1]. The struggle to perceive dim downwelling light and bioluminescent sources and the need to remain unseen generate contrasting selective pressures on the eyes of mesopelagic inhabitants 2]. Hyperiid amphipods are cosmopolitan members of the mesopelagic fauna with at least ten different eye configurations across the family—ranging from absent eyes in deep-living species to four enlarged eyes in mesopelagic individuals 3–7]. The hyperiid amphipod Paraphronima gracilis has a pair of bi-lobed apposition compound eyes, each with a large upward-looking portion and a small lateral-looking portion. The most unusual feature of the P. gracilis eye is that its upward-looking portion is resolved into a discontinuous retina with 12 distinct groups, each serving one transverse row of continuously spaced facets. On the basis of eye morphology, we estimated spatial acuity (2.5° ± 0.11°, SEM; n = 25) and optical sensitivity (30 ± 3.4 μm2 ⋅ sr, SEM; n = 25). Microspectrophotometry showed that spectral sensitivity of the eye peaked at 516 nm (±3.9 nm, SEM; n = 6), significantly offset from the peak of downwelling irradiance in the mesopelagic realm (480 nm). Modeling of spatial summation within the linear retinal groups showed that it boosts sensitivity with less cost to spatial acuity than more typical configurations.
