Eye-Size Variability in Deep-Sea Lanternfishes (Myctophidae): An Ecological and Phylogenetic Study

Abstract

One of the most common visual adaptations seen in the mesopelagic zone (200–1000 m), where the amount of light diminishes exponentially with depth and where bioluminescent organisms predominate, is the enlargement of the eye and pupil area. However, it remains unclear how eye size is influenced by depth, other environmental conditions and phylogeny. In this study, we determine the factors influencing variability in eye size and assess whether this variability is explained by ecological differences in habitat and lifestyle within a family of mesopelagic fishes characterized by broad intra- and interspecific variance in depth range and luminous patterns. We focus our study on the lanternfish family (Myctophidae) and hypothesise that lanternfishes with a deeper distribution and/or a reduction of bioluminescent emissions have smaller eyes and that ecological factors rather than phylogenetic relationships will drive the evolution of the visual system. Eye diameter and standard length were measured in 237 individuals from 61 species of lanternfishes representing all the recognised tribes within the family in addition to compiling an ecological dataset including depth distribution during night and day and the location and sexual dimorphism of luminous organs. Hypotheses were tested by investigating the relationship between the relative size of the eye (corrected for body size) and variations in depth and/or patterns of luminous-organs using phylogenetic comparative analyses. Results show a great variability in relative eye size within the Myctophidae at all taxonomic levels (from subfamily to genus), suggesting that this character may have evolved several times. However, variability in eye size within the family could not be explained by any of our ecological variables (bioluminescence and depth patterns), and appears to be driven solely by phylogenetic relationships.

Vertical distribution and diurnal migration of atlantid heteropods

“…Seapy (1990) found that larger species offshore of Oahu migrated to deeper waters during the daytime. Similar trends of larger taxa with depth have been found in other mesopelagic zooplankton (Dai et al 2017), and larger eyes relative to body size are thought to in crease photon capture (and hence detection of predators and prey) in deeper dwelling mesopelagic fishes (de Busserolles et al 2013). …”

Retinal Ganglion Cell Distribution and Spatial Resolving Power in Deep-Sea Lanternfishes (Myctophidae)

“…L. alatus and L. parvicauda, indicating a higher acuity in the centro-lateral visual field thereby allowing the fish to perceive signals in a large part of its monocular field of view, suggesting that these species are visual generalists. In addition to the generalist specialization, L. parvicauda does not appear to possess a very sensitive visual system due to its relatively small eyes [de Busserolles et al, 2013] and low summation ratios (around 20: 1 in the peak area and 50: 1 in the periphery) compared to other myctophids (i.e. M. brachygnathum 200: 1 in the peak area and 500: 1 in the non-specialized region) [de Busserolles et al, 2014b;this study].…”

“…Furthermore, most species possessing an elongated area are also known to be surface migrants and have been recorded in the first few metres of water at night (i.e. Myctophum sp., Symbolophorus sp., D. laternatus [de Busserolles et al, 2013]), where a weak visual horizon would be formed by the downwelling light emitted by the moon and stars or by the air-water interface, explaining the need for a streaklike elongated area in these species.…”

“…photophores and luminous organs) thought to play several different roles (camouflage, distraction, illumination and intra-and inter-specific communication) [Case et al, 1977;Edwards and Herring, 1977]. Myctophids also show marked intra-and interspecific variation in the depths they occupy [Karnella, 1987], their migration patterns [Watanabe et al, 1999] and the location of their luminous organs [Nafpaktitis and Nafpaktitis, 1969;Paxton, 1972;Nafpaktitis et al, 1977Nafpaktitis et al, , 1978Zahuranec, 2000;Herring, 2007;de Busserolles et al, 2013]. Recently, marked differences in the visual system of this large group of fishes have been revealed [de Busserolles et al, 2013[de Busserolles et al, , 2014a, including large variations in photoreceptor distribution across the retina [de Busserolles et al, 2014b].…”

Spectral Tuning in the Eyes of Deep-Sea Lanternfishes (Myctophidae): A Novel Sexually Dimorphic Intra-Ocular Filter

“…Like most mesopelagic fishes, lanternfishes (Myctophidae) possess several visual adaptations for life in the mesopelagic zone that serve to increase the sensitivity of the eye and optimise photon capture [de Busserolles et al, 2013[de Busserolles et al, , 2014a. Lanternfishes generally lack cones and possess a single rod photoreceptor class with a peak spectral absorption tuned to the blue-green region of the visible spectrum [Partridge et al, 1992;Douglas and Partridge, 1997;Turner et al, 2009].…”