Research in various fields of evolutionary biology has shown that divergence in gene expression is a key driver for phenotypic evolution. An exceptional contribution of cis-regulatory divergence has been found to contribute to morphological diversification. In the light of these findings, the analysis of genome-wide expression data has become one of the central tools to link genotype and phenotype information on a more mechanistic level. However, in many studies, especially if general conclusions are drawn from such data, a key feature of gene regulation is often neglected. With our article, we want to raise awareness that gene regulation and thus gene expression is highly context dependent. Genes show tissue- and stage-specific expression. We argue that the regulatory context must be considered in comparative expression studies.
Revealing the mechanisms underlying the breathtaking 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. As 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 coevolution of expression of pnr and its cofactor 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 suggest that evolutionary hotspots are not the only contributors to the repeated evolution of eye size and head shape in Drosophila.
Background: Pleuropodia are limb-derived glandular organs that transiently appear on the first abdominal segment in embryos of insects from majority of "orders". They are missing in the genetic model Drosophila and little is known about them. Experiments carried out on orthopteran insects 80 years ago indicated that the pleuropodia secrete a "hatching enzyme" that digests the serosal cuticle to enable the larva to hatch, but evidence by state-of-the-art molecular methods is missing. Results: We used high-throughput RNA-sequencing to identify the genes expressed in the pleuropodia of the locust Schistocerca gregaria (Orthoptera). First, using transmission electron microscopy we studied the development of the pleuropodia during 11 stages of the locust embryogenesis. We show that the glandular cells differentiate and start secreting just before the definitive dorsal closure of the embryo and the secretion granules outside the cells become more abundant prior to hatching. Next, we generated a comprehensive embryonic reference transcriptome for the locust and used it to study genome wide gene expression across ten morphologicaly defined stages of the pleuropodia. We show that when the pleuropodia have morphological markers of functional organs and produce secretion, they are primarily enriched in transcripts associated with transport functions. They express genes encoding enzymes capable of digesting cuticular protein and chitin. These include the potent cuticulo-lytic Chitinase 5, whose transcript rises just before hatching. Unexpected finding was the enrichment in transcripts for immunity-related enzymes. This indicates that the pleuropodia are equipped with epithelial immunity similarly as barrier epithelia in postembryonic stages.Conclusions: These data provide transcriptomic support for the historic hypothesis that pleuropodia produce cuticle-degrading enzymes and function in hatching. They may also have other functions, such as facilitation of embryonic immune defense. By the genes that they express the pleuropodia are specialized embryonic organs and apparently an important though neglected part of insect physiology.
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.
18 19 Pleuropodia are limb-derived vesicular organs that transiently appear on the first 20 abdominal segment of embryos from the majority of insect "orders". They are 21 missing in the model Drosophila and little is known about them. Experiments
1The size and shape of an organism is tightly controlled during embryonic and 2 postembryonic development to ensure proper functionality. However, in the light of the 3 breath-taking diversity of body forms observed in nature, developmental processes must have 4 evolved to allow evolutionary changes in adult morphology. Therefore, gene regulatory 5 networks (GRNs) that orchestrate organ development are mostly constrained, but nodes and 6 edges within such networks must change to give rise to morphological divergence. Identifying 7 such tuning nodes remains a major challenge in evolutionary developmental biology. Here, we 8 combined comparative transcriptomics and chromatin accessibility data to study 9 developmental differences leading to natural variation in compound eye size and head shape 10 in the two closely related Drosophila species D. melanogaster and D. mauritiana. We show that 11 variation in expression of the GATA transcription factor Pannier (Pnr) is associated with 12 extensive remodeling of the transcriptomic landscape during head development. Since U-13 shaped (Ush), a co-factor of Pnr, is involved in the same regulatory context, we argue that 14 variation in expression of both factors may be a driver of divergence in head morphology. 15Applying functional genetics and geometric morphometrics we confirmed that manipulation of 16 pnr expression in D. melanogaster largely phenocopies D. mauritiana dorsal head shape and 17 ommatidia number. Therefore, we propose that the regulatory module composed of Pnr and 18 Ush represents a tuning node within the otherwise highly conserved GRN underlying head 19 development in Drosophila. 20 21 developmental GRNs allows gaining new insights into constrained and variable developmental 1 processes, respectively. 2One approach to reveal tuning nodes is first to identify genetic variants associated with 3 morphological diversity and then in a second step to establish regulatory interactions of genes 4 affected by those variants. However, variation in complex morphological traits is influenced by 5 many genetic loci with small effect sizes, which are spread throughout various genomic 6 locations 23-25 . For instance, mandible and craniofacial shape differences between mouse 7 strains are influenced by various loci located on most of the chromosomes [26][27][28][29] . Similarly, 8 studies in Drosophila revealed that loci on several chromosomes contribute to differences in 9 eye size and head shape [30][31][32] . These examples corroborate the complexity of the genetic 10 architecture of such traits and highlight the difficulty to determine individual causative 11 molecular changes. 12As an alternative, we propose to first identify tuning nodes within the GRN governing 13 the development of a variable morphological trait. We assume that variation in the expression 14 or function of putative tuning nodes (e.g. genes coding for transcription factors) directly affects 15 the expression of downstream target genes (i.e. "gene modules" 33 ). Candidate tuning nodes 16 can then ...
Adaptive memories are formed in the face of a fundamental tension: extracting commonalities across experiences to generate novel inferences (i.e., generalization), while simultaneously forming separate representations of similar events (i.e., memory specificity). Theoretical memory models suggest that specific experiences are initially encoded as hippocampus-dependent episodic memories and slowly become amenable to generalization through consolidation. Post-learning sleep facilitates such consolidation processes. However, generalization can also occur rapidly during wakefulness. Contemporary models propose that rapid generalization relies on the retrieval of specific episodes. In a sample of 141 four- to eight-year-old children, we investigated whether (i) age differentially relates to generalization and memory specificity, (ii) generalization is contingent on different aspects of past experiences, and (iii) the effect of a sleep-filled delay on generalization and memory specificity differs across age. We found age-related differences in generalization and memory specificity, with improvements with age being more pronounced in generalization than in memory specificity. Unlike prior evidence in adults, children’s generalization success was contingent on retrieving specific object conceptual properties and on inter-object semantic proximity, but not on perceptual attributes or surrounding contexts. Further, older children were more likely to retain general and specific aspects of memory after an overnight delay. However, age-related gains differed across memory functions: Compared to younger children, older children showed greater gains in generalized, but not in specific memories. These findings reveal those aspects of past experiences upon which children draw when creating inferences, and suggest that the effects of sleep on generalization and memory specificity interact with age.
Memories enable the retrieval of specific events in the past while building generalizable knowledge that guides inference in new situations. According to a prominent conceptualization, serving both of these adaptive functions requires pattern separation, pattern completion, and generalization as distinct sets of complementary component processes. It is not known whether these three processes are separable in early childhood or whether they originally represent a single dimension of memorability that differentiates in middle childhood. Based on a selection of13 memory tasks, we will address this question though hypothesis-guided tests of differences in the factor structure of memory performance between younger and older groups of children (two groups, 48–59 versus 72–83 months of age, n = 120per group) using structural equation modeling. The results of this study will pave the way for a process-based and systemic understanding of memory development during childhood.
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