Evolution of Insect Eyes: Tales of Ancient Heritage, Deconstruction, Reconstruction, Remodeling, and Recycling

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SUMMARYObligatory cave species exhibit dramatic trait modifications such as eye reduction, loss of pigmentation and an increase in touch receptors. As molecular studies of cave adaptation have largely concentrated on vertebrate models, it is not yet possible to probe for genetic universalities underlying cave adaptation. We have therefore begun to study the strongly cave-adapted small carrion beetle Ptomaphagus hirtus. For over 100 years, this flightless signature inhabitant of Mammoth Cave, the world's largest known cave system, has been considered blind despite the presence of residual lens structures. By deep sequencing of the adult head transcriptome, we discovered the transcripts of all core members of the phototransduction protein machinery. Combined with the absence of transcripts of select structural photoreceptor and eye pigmentation genes, these data suggest a reduced but functional visual system in P. hirtus. This conclusion was corroborated by a negative phototactic response of P. hirtus in light/dark choice tests. We further detected the expression of the complete circadian clock gene network in P. hirtus, raising the possibility of a role of light sensation in the regulation of oscillating processes. We speculate that P. hirtus is representative of a large number of animal species with highly reduced but persisting visual capacities in the twilight zone of the subterranean realm. These can now be studied on a broad comparative scale given the efficiency of transcript discovery by next-generation sequencing.

Section: Introductionmentioning

confidence: 99%

Phototransduction and clock gene expression in the troglobiont beetlePtomaphagus hirtusof Mammoth cave

Friedrich

Chen

Daines

et al. 2011

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“…Stemmata frequently are not multifaceted like compound eyes, but vary greatly from simple photosensitive organs (such as in many dipterans) to sophisticated camera-type eyes, such as those found in the tiger beetle Cicindela chinensis (Gilbert, 1994;Land and Nilsson, 2002;Toh and Mizutani, 1987;Toh and Mizutani, 1994;Toh and Okamura, 2007). Despite this diversity, careful morphological studies (Paulus, 1979) as well as more recent molecular work (Buschbeck and Friedrich, 2008;Liu and Friedrich, 2004) suggest that stemmata most probably evolved from the most anterior portion of the compound eyes of their hemimetabolous ancestors.…”

Section: Introductionmentioning

confidence: 99%

Spatial distribution of opsin-encoding mRNAs in the tiered larval retinas of the sunburst diving beetle Thermonectus marmoratus (Coleoptera: Dytiscidae)

Maksimovic

Cook

Buschbeck

2009

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SUMMARYLarvae of the sunburst diving beetle, Thermonectus marmoratus, have a cluster of six stemmata (E1-6) and one eye patch on each side of the head. Each eye has two retinas: a distal retina that is closer to the lens, and a proximal retina that lies directly underneath. The distal retinas of E1 and E2 are made of a dorsal and a ventral stack of at least twelve photoreceptor layers. Could this arrangement be used to compensate for lens chromatic aberration, with shorter wavelengths detected by the distal layers and longer wavelengths by the proximal layers? To answer this question we molecularly identified opsins and their expression patterns in these eyes. We found three opsin-encoding genes. The distal retinas of all six eyes express long-wavelength opsin (TmLW) mRNA, whereas the proximal retinas express ultraviolet opsin (TmUV I) mRNA. In the proximal retinas of E1 and E2, the TmUV I mRNA is expressed only in the dorsal stack. A second ultraviolet opsin mRNA (TmUV II), is expressed in the proximal retinas of E1 and E2 (both stacks). The finding that longer-wavelength opsins are expressed distally to shorter-wavelength opsins makes it unlikely that this retinal arrangement is used to compensate for lens chromatic aberration. In addition, we also described opsin expression patterns in the medial retina of E1 and in the non-tiered retina of the lensless eye patch. To our knowledge, this is also the first report of multiple UV opsins being expressed in the same stemma.

“…In some instances they are extremely reduced, in others they have evolved to represent highly sophisticated image-forming chamber eyes. Perhaps the most dramatic and best understood (Buschbeck and Friedrich, 2008) example of reduced stemmata is the Bolwig organ of cyclorrhaphan flies, which lacks image resolution and only has 12 photoreceptors. Although the origin of this organ originally had been questioned, detailed comparative work (Melzer and Paulus, 1989;Paulus, 1989) and the presence of common molecular mechanisms (Friedrich, 2006;Friedrich, 2008) have clarified its compound eye ancestry.…”

Section: Reduced Stemmata and General Considerations For The Evolutiomentioning

confidence: 99%

Escaping compound eye ancestry: the evolution of single-chamber eyes in holometabolous larvae

Buschbeck

2014

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Stemmata, the eyes of holometabolous insect larvae, have gained little attention, even though they exhibit remarkably different optical solutions, ranging from compound eyes with upright images, to sophisticated single-chamber eyes with inverted images. Such optical differences raise the question of how major transitions may have occurred. Stemmata evolved from compound eye ancestry, and optical differences are apparent even in some of the simplest systems that share strong cellular homology with adult ommatidia. The transition to sophisticated single-chamber eyes occurred many times independently, and in at least two different ways: through the fusion of many ommatidia [as in the sawfly (Hymenoptera)], and through the expansion of single ommatidia [as in tiger beetles (Coleoptera), antlions (Neuroptera) and dobsonflies (Megaloptera)]. Although ommatidia-like units frequently have multiple photoreceptor layers (tiers), sophisticated image-forming stemmata tend to only have one photoreceptor tier, presumably a consequence of the lens only being able to efficiently focus light on to one photoreceptor layer. An interesting exception is found in some diving beetles [Dytiscidae (Coleoptera)], in which two retinas receive sharp images from a bifocal lens. Taken together, stemmata represent a great model system to study an impressive set of optical solutions that evolved from a relatively simple ancestral organization.