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

Abstract

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.

Molecular Evolution of Spider Vision: New Opportunities, Familiar Players

“…However, it is more likely that arachnid eyes evolved from the expansion of individual ommatidia for the following reasons. First, the photoreceptor arrays of spider secondary eyes (Blest et al, 1980;Land and Barth, 1992) do not show remnants of ommatidial borders, as is often observed for eyes that have evolved from the fusion of multiple ommatidia (Nilsson and Modlin, 1994;Buschbeck, 2014). Second, in scorpions, which also have median (principal) and lateral (secondary) eyes, the latter are highly variable in number, composed of zero to five pairs (Loria and Prendini, 2014).…”

“…In principle, there are two ways in which ancestral compound eyes can lead to image-forming camera-type eyes: fusion of multiple units that together give rise to a single eye, or enlargement of individual units that then each become image forming. Both transitions have been observed within stemmata, the larval eyes of holometabolous insects (for review, see Buschbeck, 2014). Examples of stemmatal formation by combined fusion and expansion also exist, such as in the flour beetle Tribolium castaneum (Herbst, 1797) (Liu and Friedrich, 2004).…”

Serial electron microscopic reconstruction of the drosophila larval eye: Photoreceptors with a rudimentary rhabdomere of microvillar-like processes

“…Where do the microvillar-like processes of Drosophila larval PRCs fall into the wide spectrum of apical membrane processes observed among different animal phyla? According to the existing developmental and genetic evidence, larval stemmata observed in holometabolous insects, including Drosophila, are homologous to the ommatidia of adult compound eyes, a proposition that has been well documented and discussed in previous works (Paulus, 1986(Paulus, , 1989Melzer and Paulus, 1989;Friedrich, 2013;Buschbeck, 2014). Microvilli of ommatidial rhabdomeres, including those of larval stemmata described for other species, are of extremely uniform diameter, orientation and high packing density, with neighboring microvilli stacked right next to each other (Arikawa et al, 1990;Hardie and Raghu, 2001;Fain et al, 2010).…”

“…As opposed to the compound adult eyes, which are large, modular arrays of small groups of photoreceptors (ommatidia) shielded by a pigment cell layer, stemmata are simpler eyes comprised of single or small groups of ommatidia; in many cases, these ommatidia are fused together into larger complexes of tens to hundreds of receptor cells joined together in a single photosensitive epithelium capped by a lens ("fusionsstemma"; (Melzer and Paulus, 1989). It has been proposed that stemmata are homologous to the posterior-most ommatidia of primitive (hemimetabolous) insects (Melzer and Paulus, 1989;Paulus, 1989;Friedrich, 2003Friedrich, , 2011Liu and Friedrich, 2004;Buschbeck, 2014). In these, a dorsal domain of the embryonic head ectoderm becomes specified as the eye field, from which photoreceptors and other retinal cell types develop in a posterior to anterior temporal gradient (Friedrich, 2003).…”

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“…The eyes of animals are classified into two major systems, single-chamber eyes and compound eyes (Buschbeck, 2014). The anatomy of compound eyes is well known in several insect species, but a limited amount of information is available from a small number of crustacean species (Alkaladi and Zeil, 2014;Buschbeck, 2014).…”