scholarly journals Variation in pleiotropic hub gene expression is associated with interspecific differences in head shape and eye size in Drosophila

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.

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.


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.


2020 ◽  
Author(s):  
Ting-Ru Mao ◽  
Ye-Wei Liu ◽  
Madhava Meegaskumbura ◽  
Jian Yang ◽  
Gajaba Ellepola ◽  
...  

ABSTRACTEpitomized by the well-studied Astyanax mexicanus, cavefishes provide important model organisms to understand adaptations in response to divergent natural selection. However, the spectacular Sinocyclocheilus diversification of China, the most diverse cavefish clade in the world harboring nearly 75 species, demonstrate evolutionary convergence for many traits, yet remain poorly understood in terms of their morphological evolution. Here, using a broad sample of 49 species representative of this diversification, we analyze patterns of Sinocylocheilus evolution in a phylogenetic context. We categorized species into morphs based on eye-related condition: Blind, Micro-eyed (small-eyed), and Normal-eyed and we also considered three habitat types (Troglodytic – cave-restricted; Troglophilic – cave-associated; Surface – outside of caves). Geometric morphometric analyses show Normal-eyed morphs with fusiform shapes being segregated from Blind/Micro-eyed (Eye-regressed) morphs with deeper bodies along the first principal component (“PC”) axis. The second PC axis accounts for shape complexity related to the presence of horns. Ancestral character reconstructions of morphs suggest at least three independent origins of Blind morphs, each with different levels of modification in relation to the typical morphology of ancestral Normal-eyed morphs. Interestingly, only some Blind or Micro-eyed morphs bear horns and they are restricted to a single clade (Clade B) and arising from a Troglodytic ancestral species. Our geophylogeny shows an east-to-west diversification spanning the Pliocene and the Pleistocene, with Troglodytic species dominating karstic subterranean habitats of the plains whereas predominantly Surface species inhabit streams and pools in hills to the west (perhaps due to the scarcity of caves). Integration of morphology, phylogeny and geography suggests Sinocyclocheilus are pre-adapted for cave dwelling. Analyses of evolutionary rates suggest that lineages leading to Blind morphs were characterized by significant rate shifts, such as a slowdown in body size evolution and a 3.3 to 12.5 fold increase in the evolutionary rate of eye regression. Furthermore, body size and eye size have undergone reversals, but horns have not, a trait that seem to require substantial evolutionary time to form. These results, compared to the Astyanax model system, indicate Sinocyclocheilus fishes demonstrate extraordinary morphological diversity and variation, offering an invaluable model system to explore evolutionary novelty.


Nature Plants ◽  
2016 ◽  
Vol 2 (11) ◽  
Author(s):  
Xiangchao Gan ◽  
Angela Hay ◽  
Michiel Kwantes ◽  
Georg Haberer ◽  
Asis Hallab ◽  
...  

Abstract Finding causal relationships between genotypic and phenotypic variation is a key focus of evolutionary biology, human genetics and plant breeding. To identify genome-wide patterns underlying trait diversity, we assembled a high-quality reference genome of Cardamine hirsuta, a close relative of the model plant Arabidopsis thaliana. We combined comparative genome and transcriptome analyses with the experimental tools available in C. hirsuta to investigate gene function and phenotypic diversification. Our findings highlight the prevalent role of transcription factors and tandem gene duplications in morphological evolution. We identified a specific role for the transcriptional regulators PLETHORA5/7 in shaping leaf diversity and link tandem gene duplication with differential gene expression in the explosive seed pod of C. hirsuta. Our work highlights the value of comparative approaches in genetically tractable species to understand the genetic basis for evolutionary change.


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.


Author(s):  
Vivek Philip Cyriac ◽  
Ullasa Kodandaramaiah

Abstract Many species possess warning colourations that signal unprofitability to predators. Warning colourations are also thought to provide prey with a ‘predator-free space’ and promote niche expansion. However, how such strategies release a species from environmental constraints and facilitate niche expansion is not clearly understood. Fossoriality in reptiles imposes several morphological limits on head and body size to facilitate burrowing underground, but many fossorial snakes live close to the surface and occasionally move above ground, exposing them to predators. In such cases, evolving antipredator defences that reduce predation on the surface could potentially relax the morphological constraints associated with fossoriality and promote morphological diversification. Fossorial uropeltid snakes possess varying degrees of conspicuous warning colourations that reduce avian predation when active above ground. We predicted that species with more conspicuous colourations will exhibit more robust body forms and show faster rates of morphological evolution because constraints imposed by fossoriality are relaxed. Using a comparative phylogenetic approach on the genus Uropeltis, we show that more conspicuous species tend to have more robust morphologies and have faster rates of head-shape evolution. Overall, we find that the evolution of warning colourations in Uropeltis can facilitate niche expansion by influencing rates of morphological diversification.


2011 ◽  
Vol 356 (1) ◽  
pp. 266
Author(s):  
William Rogers ◽  
Kristen Davis ◽  
Joe Salomone ◽  
Thomas Williams

2017 ◽  
Vol 284 (1857) ◽  
pp. 20170921 ◽  
Author(s):  
Corentin Bochaton ◽  
Salvador Bailon ◽  
Anthony Herrel ◽  
Sandrine Grouard ◽  
Ivan Ineich ◽  
...  

Fossil remains provide useful insights into the long-term impact of anthropogenic phenomena on faunas and are often used to reveal the local (extirpations) or global (extinctions) losses of populations or species. However, other phenomena such as minor morphological changes can remain inconspicuous in the fossil record depending on the methodology used. In this study, we used the anole of Marie-Galante Island ( Anolis ferreus ) in Guadeloupe (French, West Indies) as a model to demonstrate how the morphological evolution of an insular lizard can be tracked through the Pleistocene/Holocene climatic transition and the recent anthropization of the island. We used a fossil assemblage of nearly 30 000 remains and a combination of anatomical description, traditional morphometry and geometric morphometrics. These fossils are attributed to a single taxon, most likely to be A. ferreus on the basis of morphological and morphometric arguments. Our results show the disappearance of a distinct (sub)population of large specimens that were about 25% larger than the modern representatives of A. ferreus . We also demonstrate an apparent size stability of the main fossil population of this species since the Late Pleistocene but with the possible occurrence of a reduction in morphological diversity during the Late Holocene. These results highlight the impact of anthropic disturbances on a lizard whose morphology otherwise remained stable since the Late Pleistocene.


2014 ◽  
Vol 281 (1781) ◽  
pp. 20133120 ◽  
Author(s):  
Thomas A. Stewart ◽  
W. Leo Smith ◽  
Michael I. Coates

Adipose fins are appendages found on the dorsal midline between the dorsal and caudal fins in more than 6000 living species of teleost fishes. It has been consistently argued that adipose fins evolved once and have been lost repeatedly across teleosts owing to limited function. Here, we demonstrate that adipose fins originated repeatedly by using phylogenetic and anatomical evidence. This suggests that adipose fins are adaptive, although their function remains undetermined. To test for generalities in the evolution of form in de novo vertebrate fins, we studied the skeletal anatomy of adipose fins across 620 species belonging to 186 genera and 55 families. Adipose fins have repeatedly evolved endoskeletal plates, anterior dermal spines and fin rays. The repeated evolution of fin rays in adipose fins suggests that these fins can evolve new tissue types and increased structural complexity by expressing fin-associated developmental modules in these new territories. Patterns of skeletal elaboration differ between the various occurrences of adipose fins and challenge prevailing hypotheses for vertebrate fin origin. Adipose fins represent a powerful and, thus far, barely studied model for exploring the evolution of vertebrate limbs and the roles of adaptation and generative biases in morphological evolution.


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