scholarly journals Differences in orthodenticle expression promote ommatidial size variation between Drosophila species

2021 ◽  
Author(s):  
Montserrat Torres-Oliva ◽  
Elisa Buchberger ◽  
Alexandra D. Buffry ◽  
Maike Kittelmann ◽  
Lauren Sumner-Rooney ◽  
...  

The compound eyes of insects exhibit extensive variation in ommatidia number and size, which affects how they see and underlies adaptations in their vision to different environments and lifestyles. However, very little is known about the genetic and developmental bases underlying differences in compound eye size. We previously showed that the larger eyes of Drosophila mauritiana compared to D. simulans is caused by differences in ommatidia size rather than number. Furthermore, we identified an X-linked chromosomal region in D. mauritiana that results in larger eyes when introgressed into D. simulans. Here, we used a combination of fine-scale mapping and gene expression analysis to further investigate positional candidate genes on the X chromosome. We found that orthodenticle is expressed earlier in D. mauritiana than in D. simulans during ommatidial maturation in third instar larvae, and we further show that this gene is required for the correct organisation and size of ommatidia in D. melanogaster. Using ATAC-seq, we have identified several candidate eye enhancers of otd as well as potential direct targets of this transcription factor that are differentially expressed between D. mauritiana and D. simulans. Taken together, our results suggest that differential timing of otd expression contributes to natural variation in ommatidia size between D. mauritiana and D. simulans, which provides new insights into the mechanisms underlying the regulation and evolution of compound eye size in insects.

Author(s):  
Elisa Buchberger ◽  
Anıl Bilen ◽  
Sanem Ayaz ◽  
David Salamanca ◽  
Cristina Matas de las Heras ◽  
...  

Abstract Revealing the mechanisms underlying the breath-taking morphological diversity observed in nature is a major challenge in Biology. It has been established that recurrent mutations in hotspot genes cause the repeated evolution of morphological traits, such as body pigmentation or the gain and loss of structures. To date, however, it remains elusive whether hotspot genes contribute to natural variation in the size and shape of organs. Since natural variation in head morphology is pervasive in Drosophila, we studied the molecular and developmental basis of differences in compound eye size and head shape in two closely related Drosophila species. We show differences in the progression of retinal differentiation between species and we applied comparative transcriptomics and chromatin accessibility data to identify the GATA transcription factor Pannier (Pnr) as central factor associated with these differences. Although the genetic manipulation of Pnr affected multiple aspects of dorsal head development, the effect of natural variation is restricted to a subset of the phenotypic space. We present data suggesting that this developmental constraint is caused by the co-evolution of expression of pnr and its co-factor u-shaped (ush). We propose that natural variation in expression or function of highly connected developmental regulators with pleiotropic functions is a major driver for morphological evolution and we discuss implications on gene regulatory network evolution. In comparison to previous findings, our data strongly suggests that evolutionary hotspots are not the only contributors to the repeated evolution of eye size and head shape in Drosophila.


2019 ◽  
Author(s):  
Pedro Gaspar ◽  
Saad Arif ◽  
Lauren Sumner-Rooney ◽  
Maike Kittelmann ◽  
Andrew J. Bodey ◽  
...  

AbstractThe compound eyes of insects exhibit striking variation in size, reflecting adaptation to different lifestyles and habitats. However, the genetic and developmental bases of variation in insect eye size is poorly understood, which limits our understanding of how these important morphological differences evolve. To address this, we further explored natural variation in eye size within and between four species of the Drosophila melanogaster species subgroup. We found extensive variation in eye size among these species, and flies with larger eyes generally had a shorter inter-ocular distance and vice versa. We then carried out quantitative trait loci (QTL) mapping of intra-specific variation in eye size and inter-ocular distance in both D. melanogaster and D. simulans. This revealed that different genomic regions underlie variation in eye size and inter-ocular distance in both species, which we corroborated by introgression mapping in D. simulans. This suggests that although there is a trade-off between eye size and inter-ocular distance, variation in these two traits is likely to be caused by different genes and so can be genetically decoupled. Finally, although we detected QTL for intra-specific variation in eye size at similar positions in D. melanogaster and D. simulans, we observed differences in eye fate commitment between strains of these two species. This indicates that different developmental mechanisms and therefore, most likely, different genes contribute to eye size variation in these species. Taken together with the results of previous studies, our findings suggest that the gene regulatory network that specifies eye size has evolved at multiple genetic nodes to give rise to natural variation in this trait within and among species.


1995 ◽  
Vol 198 (8) ◽  
pp. 1637-1646 ◽  
Author(s):  
C Zollikofer ◽  
R Wehner ◽  
T Fukushi

This study examines the effects of body size variation on the optical properties of the compound eyes of visually guided desert ants belonging to the genus Cataglyphis. Although linear head size may vary by a factor of 2 within conspecific workers and most optical parameters change accordingly, the extent of the visual field remains constant. Comparative measurements carried out on workers of three species (C. albicans, C. bicolor and C. fortis) and on reproductive females and males of one species (C. bicolor) show that the form (size and shape) of the visual field is highly characteristic for each caste/species. A constant visual field is realised by reciprocal scaling rules for the number of ommatidia and the angular spacing of ommatidia. While larger ants have more ommatidia per compound eye, interommatidial angles are reduced accordingly, thus giving rise to a constant visual field. Among conspecific ant workers, the relationship between spatial visual acuity and eye size is similar to that found in interspecific comparisons and reflects optical constraints imposed on the design of the compound eye. Mapping of spatial visual directions onto the compound eye surface reveals a characteristic, inhomogeneous distribution of interommatidial spacing, particularly a foveal band with increased visual acuity in the vertical direction. This 'visual stretch' viewing the horizon is similar to that found in a variety of flying insects. Although, among conspecific workers, both the number of ommatidia and the interommatidial angles vary with varying head size, the overall pattern of interommatidial spacing is maintained so that corresponding positions on the compound eye of small and large individuals look in equivalent directions in space. These findings are in accordance with the observation that the shape of the compound eye surface, as expressed by the radius of curvature along cross sections, is similar in small and large ants.


2020 ◽  
Vol 10 (3) ◽  
pp. 1005-1018 ◽  
Author(s):  
Pedro Gaspar ◽  
Saad Arif ◽  
Lauren Sumner-Rooney ◽  
Maike Kittelmann ◽  
Andrew J. Bodey ◽  
...  

The compound eyes of insects exhibit striking variation in size, reflecting adaptation to different lifestyles and habitats. However, the genetic and developmental bases of variation in insect eye size is poorly understood, which limits our understanding of how these important morphological differences evolve. To address this, we further explored natural variation in eye size within and between four species of the Drosophila melanogaster species subgroup. We found extensive variation in eye size among these species, and flies with larger eyes generally had a shorter inter-ocular distance and vice versa. We then carried out quantitative trait loci (QTL) mapping of intra-specific variation in eye size and inter-ocular distance in both D. melanogaster and D. simulans. This revealed that different genomic regions underlie variation in eye size and inter-ocular distance in both species, which we corroborated by introgression mapping in D. simulans. This suggests that although there is a trade-off between eye size and inter-ocular distance, variation in these two traits is likely to be caused by different genes and so can be genetically decoupled. Finally, although we detected QTL for intra-specific variation in eye size at similar positions in D. melanogaster and D. simulans, we observed differences in eye fate commitment between strains of these two species. This indicates that different developmental mechanisms and therefore, most likely, different genes contribute to eye size variation in these species. Taken together with the results of previous studies, our findings suggest that the gene regulatory network that specifies eye size has evolved at multiple genetic nodes to give rise to natural variation in this trait within and among species.


2020 ◽  
Author(s):  
Elisa Buchberger ◽  
Anıl Bilen ◽  
Sanem Ayaz ◽  
David Salamanca ◽  
Cristina Matas de las Heras ◽  
...  

AbstractRevealing the mechanisms underlying the breath-taking morphological diversity observed in nature is a major challenge in Biology. It has been established that recurrent mutations in hotspot genes cause the repeated evolution of rather simple morphological traits, such as body pigmentation or the gain and loss of structures. To date, however, it remains elusive whether hotspot genes contribute to natural variation in complex morphological traits, such as the size and shape of organs. Since natural variation in head morphology is pervasive in Drosophila, we studied the molecular and developmental basis of differences in compound eye size and head shape in two closely related Drosophila species. We show that differences in both traits are established late during head development and we applied comparative transcriptomics and chromatin accessibility data to identify the GATA transcription factor Pannier (Pnr) as central factor regulating these differences. Although the genetic manipulation of Pnr affected multiple aspects of dorsal head development, the effect of natural variation is restricted to a subset of the phenotypic space. We present data suggesting that this developmental constraint is caused by the co-evolution of expression of pnr and its co-factor u-shaped (ush). We propose that natural variation in highly connected developmental regulators with pleiotropic functions is a major driver for morphological evolution and we discuss implications on gene regulatory network evolution. In comparison to previous findings, our data strongly suggests that evolutionary hotspots do not contribute to the repeated evolution of eye size and head shape in Drosophila.


Development ◽  
1981 ◽  
Vol 61 (1) ◽  
pp. 259-276
Author(s):  
Charles Straznicky ◽  
David Tay

Right compound eyes were formed in Xenopus embryos at stages 32–33 by the fusion of two nasal (NN), two ventral (VV) or two temporal (TT) halves. Shortly after metamorphosis the optic nerve from the compound eye was sectioned and the left intact eye removed. The retinotectal projections from the compound eye to the contralateral and ipsilateral tecta were studied by [3H]proline autoradiography and electrophysiological mapping between 6 weeks and 5 months after the postmetamorphic surgery. The results showed that NN and VV eyes projected to the entire extent of both tecta. In contrast, optic fibre projection from TT eyes, although more extensive than the normal temporal hemiretinal projection, failed to cover the caudomedial portion of the tecta. The visuotectal projections in all three combinations corresponded to typical reduplicated maps to be expected from such compound eyes, where each of the hemiretinae projected across the contralateral and ipsilateral tecta in an overlapping fashion. The rapid expansion of the hemiretinal projections of the compound eyes in the ipsilateral tectum following the removal of the resident optic fibre projection suggests that tectal markers may be carried and deployed by the incoming optic fibres themselves.


Development ◽  
1975 ◽  
Vol 33 (3) ◽  
pp. 775-787
Author(s):  
Joan D. Feldman ◽  
R. M. Gaze

Double-nasal and double-temporal compound eyes were constructed in Xenopus embryos at stages 32 and 37/38. A particular half was removed from the host eye anlage and replaced with the opposite half-eye from the contralateral side of a donor embryo. Control operations consisted of removing a half-eye and replacing it with a similar half from the ipsilateral side of the donor embryo. Whereas in control animals, each half-eye projected its fibres to the appropriate half-tectum, in operated animals each half of the compound eye spread its optic teiminals across the entire rostrocaudal extent of the dorsal tectal surface. The area of tectal surface covered by ganglion fibre terminals was similar in operated animals mapped at successive stages of development to that previously observed in normal animals at equivalent stages. Therefore the factors responsible for the extended distribution of fibre terminals from each half of a compound eye must exist at least from mid-tadpole life, and thereafter be continuously present throughout development.


Development ◽  
1981 ◽  
Vol 66 (1) ◽  
pp. 159-174
Author(s):  
Charles Straznicky ◽  
David Tay

Right compound eyes were formed in Xenopus embryos at tailbud stages by the fusion of two nasal (NN), two temporal (TT) or two ventral (VV) halves. The left eye was kept intact. Two to four weeks after metamorphosis the optic nerve from the intact eye was severed to induce bilateral optic nerve regeneration. The contralateral retinotectal projections from the compound eye and the induced ipsilateral projections from the intact eye to the same (dually innervated) tectum were studied by [3H]proline autoradiography and visuotectal mapping from 3 to 6 months after the postmetamorphic surgery. The results showed that the NN, TT and VV projections, in the presence of optic fibres from the intact eye failed to spread across the whole extent of the dually innervated tectum. Unexpectedly the bulk of the regenerating projection from the intact eye was confined to the previously uninnervated parts of the dually innervated tecta, the caudomedial region in TT, the rostrolateral region in NN and the lateral region in VV eye animals. The partial segregation of the two populations of optic fibres in the dually innervated tectum has been taken as a further indication of the role of fibre-fibre and fibre-tectum interactions in retinotectal map formation.


1992 ◽  
Vol 171 (1) ◽  
pp. 373-393 ◽  
Author(s):  
THOMAS W. CRONIN ◽  
HONG Y. YAN ◽  
KAY D. BIDLE

1. Regional specialization within the triple compound eyes of the gonodactyloid stomatopod Gonodactylus oerstedii (Hansen) was studied by examining how ocular tracking of a small target was affected after occluding vision in particular ommatidial regions with black enamel paint. 2. Complete occlusion of one eye did not prevent the other eye from tracking, indicating that the two eyes act somewhat independently. However, following such treatment, the angular extent over which the seeing eye moved while tracking was reduced. 3. An eye was able to continue tracking a moving target even after occlusion of the anterior tip or after painting over all of its posterior surface except the anterior tip (restricting the visual field to a patch about 40° in diameter). Similarly, occlusion of only the midband, the medial half or the lateral half of an eye did not prevent tracking. 4. Tracking was also possible, although with decreased amplitude, when either the dorsal or the ventral hemisphere was occluded. However, when both the dorsal and ventral hemispheres were occluded, leaving only the midband for vision, the ability of an eye to track was abolished. 5. A computer model was used to investigate whether the midband alone had the potential to direct tracking in our experiments. The model's output predicts that, in spite of its restricted field of view, if the midband is oriented within 20° of the horizontal, an eye could track using the midband alone. Conditions favoring such potential tracking occurred in our experiments, but neither tracking nor targetting movements were observed. 6. We conclude that ommatidia of the dorsal and ventral hemispheres of each compound eye are essential for ocular tracking in G. oerstedii. The midband appears to play no major role in this activity. Note: Present address: Department of Zoology, The University of Maryland College Park, College Park, MD 20742, USA.


2020 ◽  
Vol 6 (49) ◽  
pp. eabc6721
Author(s):  
John R. Paterson ◽  
Gregory D. Edgecombe ◽  
Diego C. García-Bellido

Radiodonts are nektonic stem-group euarthropods that played various trophic roles in Paleozoic marine ecosystems, but information on their vision is limited. Optical details exist only in one species from the Cambrian Emu Bay Shale of Australia, here assigned to Anomalocaris aff. canadensis. We identify another type of radiodont compound eye from this deposit, belonging to ‘Anomalocaris’ briggsi. This ≤4-cm sessile eye has >13,000 lenses and a dorsally oriented acute zone. In both taxa, lenses were added marginally and increased in size and number throughout development, as in many crown-group euarthropods. Both species’ eyes conform to their inferred lifestyles: The macrophagous predator A. aff. canadensis has acute stalked eyes (>24,000 lenses each) adapted for hunting in well-lit waters, whereas the suspension-feeding ‘A.’ briggsi could detect plankton in dim down-welling light. Radiodont eyes further demonstrate the group’s anatomical and ecological diversity and reinforce the crucial role of vision in early animal ecosystems.


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