Microhabitat partitioning correlates with opsin gene expression in coral reef cardinalfishes (Apogonidae)

Abstract

1. Fish are the most diverse vertebrate group, and they have evolved equally diverse visual systems, varying in terms of eye morphology, number and distribution of spectrally distinct photoreceptor types, visual opsin genes and opsin gene expression levels.2. This variation is mainly due to adaptations driven by two factors: differences in the light environments and behavioural tasks. However, while the effects of largescale habitat differences are well described, it is less clear whether visual systems also adapt to differences in environmental light at the microhabitat level.3. To address this, we assessed the relationship between microhabitat use and visual system features in fishes inhabiting coral reefs, where habitat partitioning is particularly common.4. We suggest that differences in microhabitat use by cardinalfishes (Apogonidae) drive morphological and molecular adaptations in their visual systems. To test this, we investigated diurnal microhabitat use in 17 cardinalfish species and assessed whether this correlated with differences in visual opsin gene expression and eye morphology.5. We found that cardinalfishes display six types of microhabitat partitioning behaviours during the day, ranging from specialists found exclusively in the water column to species that are always hidden inside the reef matrix.6. Species predominantly found in exposed microhabitats had higher expression of the short-wavelength-sensitive violet opsin (SWS2B) and lower expression of the dim-light active rod opsin (RH1). Species of intermediate exposure, on the other hand, expressed opsins that are mostly sensitive to the blue-green central part of the light spectrum (SWS2As and RH2s), while fishes entirely hidden in the reef substrate had a higher expression of the long-wavelength-sensitive red opsin. 7. We also found that eye size relative to body size differed between cardinalfish species, and relative eye size decreased with an increase in habitat exposure.8. Retinal topography did not show co-adaptation with microhabitat use, but data suggested co-adaptation with feeding mode.9. We suggest that, although most cardinalfishes are nocturnal foragers, their visual systems-and possibly those of other (reef) fishes-have also adapted to the light intensity and the light spectrum of their preferred diurnal microhabitats. | Functional EcologyLUEHRMANN Et AL.

Seeing the rainbow: mechanisms underlying spectral sensitivity in teleost fishes

“…Therefore, cichlids living at clearer sites in the center of a lake express shorter-wavelength opsins whereas those living nearby in more murky riverine sites have longer-wavelength opsins Wright et al, 2019). On coral reefs, cardinalfish that live above the corals in the 'blue' water column express shorter-wavelength opsins, whereas those that live in dimmer 'reddish' coral caves express longer-wavelength opsins (Luehrmann et al, 2020). Similarly, opsin expression in guppies varies between different watershed populations (Sandkam et al, 2015b) and even between populations with high versus low predation (Sandkam et al, 2015a).…”

“…Understanding the role of the environment or indeed the microenvironment in altering visual sensitivities is important (Luehrmann et al, 2020;Marshall et al, 2003;Munz and McFarland, 1977). All visual detection and discrimination tasks must be performed within the context of the local light environment.…”

Marine artificial light at night: An empirical and technical guide

“…Table 1 presents optical sensor analogues that best resemble organisms' visual system to quantify its photosensitivity. An animal's photosensory system is closely linked to its photic environment (Land & Nilsson, 2012) down to the scale of variations in the (micro)habitat (Luehrmann et al, 2020), its ecology (e.g. coastal/inter-or subtidal; sessile/mobile; benthic/demersal/pelagic) and activity pattern (diurnal/crepuscular/nocturnal/cathemeral; Schmitz & Wainwright, 2011).…”

Sex differences in behavioural and anatomical estimates of visual acuity in the green swordtail, Xiphophorus helleri

“…However, aside from the environment, several other ecological factors, such as feeding mode ( de Busserolles et al, 2014 , 2021 ; Luehrmann et al, 2020 ), predator detection ( Collin and Pettigrew, 1988a ), competition ( Stieb et al, 2019 ) and signalling traits ( Parker et al, 2017 ), may also contribute to the evolution of specific retinal topography patterns. In the Ambon damselfish, Pomacentrus amboinensis , for example, the higher density of RGCs in the dorso-temporal part of the retina that extends centrally ( Parker et al, 2017 ) may enhance their ability to discriminate the species-specific fine facial markings of their conspecifics ( Siebeck, 2004 ; Siebeck et al, 2010 ).…”

“…These specializations, which provide higher acuity in a specific part of the visual field, are usually classified into two main types, ‘areas’ and ‘streaks’, where the increase in cell density is concentric or elongated across the retinal meridian, respectively. Variability in the type of specialization and its localization often correlates with the ecology and behaviour of a particular species and has been shown in fish to vary with habitat type, feeding ecology, predator or conspecific detection, and life stage ( Collin and Pettigrew, 1988a , b ; de Busserolles et al, 2014 , 2021 ; Luehrmann et al, 2020 ; Shand et al, 2000 ; Stieb et al, 2019 ; Tettamanti et al, 2019 ).…”