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. 2024 Jul 2;8(5):726-734.
doi: 10.1093/evlett/qrae028. eCollection 2024 Sep.

The link between gene duplication and divergent patterns of gene expression across a complex life cycle

James G DuBose  1 , Jacobus C de Roode  1
Affiliations

The link between gene duplication and divergent patterns of gene expression across a complex life cycle

James G DuBose et al. Evol Lett. .

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.

Keywords: evolutionary genomics; gene expression; life history evolution; mutations.

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Figures

Figure 1.
Figure 1.
A conceptual diagram showing the hypothesized mechanism of how duplicate gene evolution could lead to divergence in gene expression (and consequently phenotypes) between perceived stages in a complex life cycle. Initially, a given gene has an expression pattern that is relatively uniform throughout an organism’s lifetime. After duplication, the expression patterns of each copy tend to diverge and become more stage-specific. After additional duplication and divergence, expressions tends to diverge and specify even more between copies. This makes the expression at each stage substantially more distinct from other stages, which would result in greater phenotypic divergence between stages if the duplicates functionally diverged as well. This diagram does not show all possible fates of duplicate genes.
Figure 2.
Figure 2.
A depiction of how morphology and transcription change across the D. plexippus lifecycle. (A) Images of each life stage sampled in this study are shown. (B) A principal coordinate analysis plot showing substantial transcriptional divergence between life stages. Each point represents the global gene expression profile of an individual, and closer points indicate more similar gene expression profiles. Axis labels indicate principal coordinate rank and the proportion of variance explained.
Figure 3.
Figure 3.
Phylogenetic distance positively correlates with expression pattern distance in most homologous gene groups. The correlation between phylogenetic and expression distances in a set of (A) Hox homologs and (B) Osiris homologs. In (A) and (B), each point indicates the phylogenetic and expression distance for a pair of genes within the homologous groups. A and B are meant to contextualize the broader analysis, not to lend interpretations about the specific homologous groups used for demonstration purposes. (C) The empirical cumulative density function of correlation coefficients between phylogenetic distance and expression pattern distance across all homologous groups. Values greater than 0 indicate a positive correlation and greater values indicate stronger correlations. Overall, the majority of the distribution (approximately 72%) consists of positive correlations.
Figure 4.
Figure 4.
More phylogenetically diverse homologous groups exhibit more diverse patterns of expression. (A) An example of a less phylogenetically diverse homologous group (a geranylgeranyl diphosphate synthase-like group) showing less diverse patterns of expression. (B) An example of a more phylogenetically diverse group (an arrestin-like group) showing more diverse patterns of expression. (A) and (B) are meant to contextualize the broader analysis, not to lend interpretation about the specific homologous groups used for demonstration purposes. (C) The relationship between phylogenetic and expression pattern diversity across all homologous groups. The solid black line depicts the fit quadratic model, and the light gray area indicates the 95% confidence interval for said model. (D) The relationship between phylogenetic and expression pattern diversity by homologous group size. Each line represents the linear model fit to each homologous group size (only group sizes with five or more replicates were considered in this analysis).
Figure 5.
Figure 5.
The expression patterns of duplicate genes show increased stage-specificity relative to singleton genes. The empirical cumulative density functions of expression specificity values for duplicate (solid line) and singleton (dashed line) genes. Higher expression specificity values indicate increased stage-specificity.
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