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WIREs Dev Biol
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The evolution and development of eye size in flies

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Abstract The compound eyes of flies exhibit striking variation in size, which has contributed to the adaptation of these animals to different habitats and their evolution of specialist behaviors. These differences in size are caused by differences in the number and/or size of ommatidia, which are specified during the development of the retinal field in the eye imaginal disc. While the genes and developmental mechanisms that regulate the formation of compound eyes are understood in great detail in the fruit fly Drosophila melanogaster, we know very little about the genetic changes and mechanistic alterations that lead to natural variation in ommatidia number and/or size, and thus overall eye size, within and between fly species. Understanding the genetic and developmental bases for this natural variation in eye size not only has great potential to help us understand adaptations in fly vision but also determine how eye size and organ size more generally are regulated. Here we explore the genetic and developmental mechanisms that could underlie natural differences in compound eye size within and among fly species based on our knowledge of eye development in D. melanogaster and the few cases where the causative genes and mechanisms have already been identified. We suggest that the fly eye provides an evolutionary and developmental framework to better understand the regulation and diversification of this crucial sensory organ globally at a systems level as well as the gene regulatory networks and mechanisms acting at the tissue, cellular and molecular levels. This article is categorized under: Establishment of Spatial and Temporal Patterns > Regulation of Size, Proportion, and Timing Invertebrate Organogenesis > Flies Comparative Development and Evolution > Regulation of Organ Diversity
Eye size differences in Diptera. (a) The Pipunculid Chalarus and (b) the sheep ked Melophagus ovinus. The eyes of Chalarus comprise more than 4,500 ommatidia (approximately 90,000 cells), while those of Melophagous are formed by about 160 ommatidia (approximately 3,200 cells). The arrows point to its eyes
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Ommatidia can grow to very different sizes. Heads of a Chalarus female (a) and of a Simulium male (b). The eye of Chalarus (a) shows an anterior–posterior gradient of ommatidial size, with the largest ommatidia located anteriorly, at the eye's front. In (b), the dorsal region (“D,” called the “love spot”) harbors much larger ommatidia than the ventral (“V”) half
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Parameters that affect final eye size. (a) Size of the primordium (“P”); (b) Growth rate of progenitor region (represented by arrows); (c) differentiation velocity (arrows); (d) ommatidial size (“s”). below each scheme, the arrow marked with “t” indicates developmental time. Variation in size may require lengthening of developmental time. Progenitor (proliferative area, blue) and differentiating regions (orange). Mechanism A or A and C in combination may explain eye size differences among strains of D. melanogaster (Gaspar et al., 2020; Ramaekers et al., 2019), while a combination of mechanisms B and C may explain differences between strains of D. simulans (Gaspar et al., 2020). Mechanism D is thought to explain the generally larger eyes of some D. mauritiana strains compared to its sibling species (Arif et al., 2013)
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(a) Eye development in Drosophila. From the third instar larval stage (L3) to puparium formation (PF) when ommatidial cells are specified from posterior (Pos) to anterior (Ant) (morphogenetic furrow (MF) (blue line), inner (black) and outer (green) photoreceptor cells). 24 hours after puparium formation (hAPF): inter‐ommatidial pigment cells (IPCs) are rearranged and extra cells removed by programmed cell death (PCD). 40 hAPF: anterior ommatidia are already larger than posterior ommatidia (apical to the photoreceptor cells are the cone cells (blue), primary pigment cells (yellow) and the interommatidial cells (red)). 60 hAPF: formation of the corneal lens is initiated. 96 hAPF: Rhodopsins are expressed. (b) adult ommatidia in cross section: ommatidial diameter (D) and inter‐ommatidial angle (Δϕ)
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Fate map of the eye‐antennal disc compared to the adult eye of Drosophila melanogaster. (a). Eye‐antennal disc at approximately 96 hr after egg laying with the head capsule (blue), antennal (purple), maxillary palp (green), and ocelli and eye (red) primordia indicated. (b). Drosophila head with the adult tissues indicated using the same color scheme
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Comparative Development and Evolution > Regulation of Organ Diversity
Invertebrate Organogenesis > Flies
Establishment of Spatial and Temporal Patterns > Regulation of Size, Proportion, and Timing