An official website of the United States government
ABSTRACT Organisms with complex life cycles demonstrate a remarkable ability to change their phenotypes across development, presumably as an evolutionary adaptation to developmentally variable environments. Developmental variation in environmentally sensitive performance, and thermal sensitivity in particular, has been well documented in holometabolous insects. For example, thermal performance in adults and juvenile stages exhibit little genetic correlation (genetic decoupling) and can evolve independently, resulting in divergent thermal responses. Yet, we understand very little about how this genetic decoupling occurs. We tested the hypothesis that genetic decoupling of thermal physiology is driven by fundamental differences in physiology between life stages, despite a potentially conserved cellular stress response. We used RNAseq to compare transcript expression in response to a cold stressor in Drosophila melanogaster larvae and adults and used RNA interference (RNAi) to test whether knocking down nine target genes differentially affected larval and adult cold tolerance. Transcriptomic responses of whole larvae and adults during and following exposure to −5°C were largely unique both in identity of responding transcripts and in temporal dynamics. Further, we analyzed the tissue-specificity of differentially expressed transcripts from FlyAtlas 2 data, and concluded that stage-specific differences in transcription were not simply driven by differences in tissue composition. In addition, RNAi of target genes resulted in largely stage-specific and sometimes sex-specific effects on cold tolerance. The combined evidence suggests that thermal physiology is largely stage-specific at the level of gene expression, and thus natural selection may be acting on different loci during the independent thermal adaptation of different life stages.
more »
« less
The link between gene duplication and divergent patterns of gene expression across a complex life cycle
Abstract The diversification of many lineages throughout natural history has frequently been associated with evolutionary changes in life cycle complexity. However, our understanding of the processes that facilitate differentiation in the morphologies and functions expressed by organisms throughout their life cycles is limited. Theory suggests that the expression of traits is decoupled across life stages, thus allowing for their evolutionary independence. Although trait decoupling between stages is well established, explanations of how said decoupling evolves have seldom been considered. Because the different phenotypes expressed by organisms throughout their life cycles are coded for by the same genome, trait decoupling must be mediated through divergence in gene expression between stages. Gene duplication has been identified as an important mechanism that enables divergence in gene function and expression between cells and tissues. Because stage transitions across life cycles require changes in tissue types and functions, we investigated the potential link between gene duplication and expression divergence between life stages. To explore this idea, we examined the temporal changes in gene expression across the monarch butterfly (Danaus plexippus) metamorphosis. We found that within homologous groups, more phylogenetically diverged genes exhibited more distinct temporal expression patterns. This relationship scaled such that more phylogenetically diverse homologous groups showed more diverse patterns of gene expression. Furthermore, we found that duplicate genes showed increased stage-specificity relative to singleton genes. Overall, our findings suggest an important link between gene duplication and the evolution of complex life cycles.
more »
« less
- Award ID(s):
- 1922720
- PAR ID:
- 10520270
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Evolution Letters
- Volume:
- 8
- Issue:
- 5
- ISSN:
- 2056-3744
- Format(s):
- Medium: X Size: p. 726-734
- Size(s):
- p. 726-734
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract BackgroundDifferences in morphology, ecology, and behavior through ontogeny can result in opposing selective pressures at different life stages. Most animals, however, transition through two or more distinct phenotypic phases, which is hypothesized to allow each life stage to adapt more freely to its ecological niche. How this applies to sensory systems, and in particular how sensory systems adapt across life stages at the molecular level, is not well understood. Here, we used whole-eye transcriptomes to investigate differences in gene expression between tadpole and juvenile southern leopard frogs (Lithobates sphenocephalus), which rely on vision in aquatic and terrestrial light environments, respectively. Because visual physiology changes with light levels, we also tested the effect of light and dark exposure. ResultsWe found 42% of genes were differentially expressed in the eyes of tadpoles versus juveniles and 5% for light/dark exposure. Analyses targeting a curated subset of visual genes revealed significant differential expression of genes that control aspects of visual function and development, including spectral sensitivity and lens composition. Finally, microspectrophotometry of photoreceptors confirmed shifts in spectral sensitivity predicted by the expression results, consistent with adaptation to distinct light environments. ConclusionsOverall, we identified extensive expression-level differences in the eyes of tadpoles and juveniles related to observed morphological and physiological changes through metamorphosis and corresponding adaptive shifts to improve vision in the distinct aquatic and terrestrial light environments these frogs inhabit during their life cycle. More broadly, these results suggest that decoupling of gene expression can mediate the opposing selection pressures experienced by organisms with complex life cycles that inhabit different environmental conditions throughout ontogeny.more » « less
-
Abstract The phenotype of an organism is shaped by gene expression within developing tissues. This shaping relates the evolution of gene expression to phenotypic evolution, through divergence in gene expression and consequent phenotype. Rates of phenotypic evolution receive extensive attention. However, the degree to which divergence in the phenotype of gene expression is subject to heterogeneous rates of evolution across developmental stages has not previously been assessed. Here, we analyzed the evolution of the expression of single-copy orthologs within 9 species of Sordariomycetes Fungi, across 9 developmental stages within asexual spore germination and sexual reproduction. Rates of gene expression evolution exhibited high variation both within and among developmental stages. Furthermore, rates of gene expression evolution were correlated with nonsynonymous to synonymous substitution rates (dN/dS), suggesting that gene sequence evolution and expression evolution are indirectly or directly driven by common evolutionary forces. Functional pathway analyses demonstrate that rates of gene expression evolution are higher in labile pathways such as carbon metabolism, and lower in conserved pathways such as those involved in cell cycle and molecular signaling. Lastly, the expression of genes in the meiosis pathway evolved at a slower rate only across the stages where meiosis took place, suggesting that stage-specific low rates of expression evolution implicate high relevance of the genes to developmental operations occurring between those stages.more » « less
-
Braasch, Ingo (Ed.)Gene duplication is an important process of molecular evolutionary change, though identifying these events and their functional implications remains challenging. Studies on gene duplication more often focus on the presence of paralogous genes within the genomes and less frequently explore shifts in expression. We investigated the evolutionary history of calsequestrin (CASQ), a crucial calcium-binding protein in the junctional sarcoplasmic reticulum of muscle tissues. CASQ exists in jawed vertebrates as subfunctionalized paralogs CASQ1 and CASQ2 expressed primarily in skeletal and cardiac muscles, respectively. We used an enhanced sequence dataset to support initial duplication of CASQl in a jawed fish ancestor prior to the divergence of cartilaginous fishes. Surprisingly, we find CASQ2 is the predominant skeletal muscle paralog in birds, while CASQ1 is either absent or effectively nonfunctional. Changes in the amino acid composition and electronegativity of avian CASQ2 suggest enhancement to calcium-binding properties that preceded the loss of CASQ1. We identify this phenomenon as CASQ2 “synfunctionalization,” where one paralog functionally replaces another. While additional studies are needed to fully understand the dynamics of CASQ1 and CASQ2 in bird muscles, the long and consistent history of CASQ subfunctions outside of birds indicate a substantial evolutionary pressure on calcium-cycling processes in muscle tissues, likely connected to increased avian cardiovascular and metabolic demands. Our study provides an important insight into the molecular evolution of birds and shows how gene expression patterns can be comparatively studied across phylum-scale deep time to reveal key evolutionary eventsmore » « less
-
null (Ed.)Abstract X and Y chromosomes are usually derived from a pair of homologous autosomes, which then diverge from each other over time. Although Y-specific features have been characterized in sex chromosomes of various ages, the earliest stages of Y chromosome evolution remain elusive. In particular, we do not know whether early stages of Y chromosome evolution consist of changes to individual genes or happen via chromosome-scale divergence from the X. To address this question, we quantified divergence between young proto-X and proto-Y chromosomes in the house fly, Musca domestica. We compared proto-sex chromosome sequence and gene expression between genotypic (XY) and sex-reversed (XX) males. We find evidence for sequence divergence between genes on the proto-X and proto-Y, including five genes with mitochondrial functions. There is also an excess of genes with divergent expression between the proto-X and proto-Y, but the number of genes is small. This suggests that individual proto-Y genes, but not the entire proto-Y chromosome, have diverged from the proto-X. We identified one gene, encoding an axonemal dynein assembly factor (which functions in sperm motility), that has higher expression in XY males than XX males because of a disproportionate contribution of the proto-Y allele to gene expression. The upregulation of the proto-Y allele may be favored in males because of this gene’s function in spermatogenesis. The evolutionary divergence between proto-X and proto-Y copies of this gene, as well as the mitochondrial genes, is consistent with selection in males affecting the evolution of individual genes during early Y chromosome evolution.more » « less
