Evolution of gene expression and gene regulation during head development in Drosophila americana and D. novamexicana
Evolution, Anthropology
Final Report Abstract
The morphological diversity present in nature is the result of evolution of developmental programs. Developmental gene regulatory networks (GRNs) need to be highly constraint to ensure functional organ formation. At the same time these networks must be flexible enough to allow natural variation in morphology to occur. Natural variation in traits that are affected by relatively simple GRNs, such as body pigmentation, are well-studied. However, a comprehensive mechanistic understanding of the molecular changes responsible for divergence of complex morphological traits is still largely missing. Therefore, we investigated the genetic architecture of natural variation in eye size and head shape in two groups of closely related Drosophila species. Quantification of natural variation in eye size and head shape in four Drosophila species revealed that D. melanogaster and D. mauritiana (i.e. melanogaster group), as well as D. americana and D. novamexicana (virilis group) differ in eye size due to variation in ommatidia number and larger eyes develop at the expense of head cuticle between the eyes in both species pairs. To gain insights into the molecular and developmental basis of these differences, we integrated multiple unbiased datasets. The combination of genome-wide expression (RNAseq) and chromatin accessibility data (ATACseq) in conjunction with GRN reconstruction revealed the GATA transcription factor Pannier (Pnr) as highly variable central hub gene underlying variation in head morphology between D. melanogaster and D. mauritiana. We functionally validated this finding by showing that experimental modulation of pnr expression in D. melanogaster phenocopies major aspects of eye size and head shape of D. mauritiana. To reveal additional candidate genes, we integrated allele-specific gene expression and quantitative genetics data to unravel a variable GRN module that contains 12 genes with previously unknown functions in head development, as well as multiple genes with known function in this process. Many genes within this network module are expressed in a special cell layer of the developing head, the so called peripodial epithelium. We hypothesize that variable gene expression in this tissue contributes to differences in head morphology between D. melanogaster and D. mauritiana. A combination of genetic crosses, genome wide association studies and population genomics revealed a strong influence of chromosomal inversions on head morphology in D. americana and D. novamexicana. Moreover, we identified 294 candidate genes on the 4th and 5th chromosomes which contribute to morphological differences between the two species. A thorough quantification of cellular and developmental processes throughout head formation showed that differences in eye size between D. americana and D. novamexicana manifest during third larval instar stages. Based on this finding, we generated RNAseq and ATACseq data to reveal tissue- and stage specific candidate genes that were integrated with positional candidate genes from our mapping data to unravel major genes for future functional validation experiments. Overall, we find compelling evidence that the genetic architecture of variation in head morphology between Drosophila species is highly complex. Our data is in line with recent models suggesting that complex traits are influenced by many genes with minor individual impact on the phenotype. We propose that a GRN-centric approach will allow unraveling causative processes underlying natural variation in complex traits.
Publications
- (2019) "Context dependent gene regulation and implications for evolutionary studies." Genes 10(7), 492
Buchberger E, Reis M, Lu T-H, Posnien N
(See online at https://doi.org/10.3390/genes10070492) - (2020). “Multiple loci linked to inversions are associated with eye size variation in species of the Drosophila virilis phylad.” Scientific Reports
Reis M, Wiegleb G, Claude J, Lata R, Horchler B, Ha N-T, Reimer C, Vieira CP, Vieira J, Posnien N
(See online at https://doi.org/10.1038/s41598-020-69719-z) - (2021) “Conserved and Divergent Aspects of Plasticity and Sexual Dimorphism in Wing Size and Shape in Three Diptera." Front. Ecol. Evol. 9:660546
Reis M, Siomava N, Wimmer EA, Posnien N
(See online at https://doi.org/10.3389/fevo.2021.660546) - (2021) “Variation in pleiotropic hub gene expression is associated with interspecific differences in head shape and eye size in Drosophila.” Molecular Biology and Evolution; msaa335
Buchberger E, Bilen A, Ayaz S, Salamanca D, Matas de las Heras C, Niksic A, Almudi I, Torres-Oliva M, Casares F, Posnien N
(See online at https://doi.org/10.1093/molbev/msaa335)
