Evolutionary rates provide genomic insights into convergent and lineage-specific evolution in carnivorous plants
Abstract
Carnivorous plants (CPs) are striking examples of convergent evolution across ecological, morphological, and molecular scales, making them ideal systems for investigating genomic adaptation to extreme environments. While genomic studies have shown that gene family expansion and functional recruitment underlie key carnivorous traits, the effects of these transitions on rates of sequence evolution remain incompletely understood. Here, we present a comparative framework to examine evolutionary rate shifts across 30 carnivorous and non-carnivorous eudicots in over 12,000 gene families. After normalizing for genome-wide background effects, analysis of branch-lengths and evolutionary rate covariation (ERC) detected both lineage-specific and convergent acceleration in CPs for genes associated with stress response, stimulus signaling, and light perception. Accelerated genes often belong to expanded families and show relaxation of purifying selection pressure. Despite the limited number of specific genes or gene families showing convergent acceleration across CP lineages, we find strong convergence at the functional level. Distinct sets of accelerated genes in each CP lineage are enriched for similar functional pathways, particularly light and hormone responses. ERC network analysis identifies a stress- and stimulus-responsive gene community with lineage-specific acceleration in Sarraceniaceae species and moderate acceleration in other CP lineages. Hub genes in this network are also co-expressed in a distantly related non-CP model system, suggesting repeated co-option of an ancestral regulatory module for carnivorous functions. Together, our results show that convergent genomic rate accelerations in CPs primarily involve functionally equivalent or similar but lineage-distinct genes, shaped by gene duplication, relaxed selection, and co-option of stress-response networks.
Significance Statement
Investigations of carnivorous plant (CP) evolution over the last decade have produced a large amount of genomic data that has yet to be fully explored. Using existing genomes and transcriptomes from five independently evolved CP lineages and their non-carnivorous relatives, we compared how rapidly different genes change to identify both shared and lineage-specific shifts associated with carnivory. We show that CP lineages frequently speed up evolution in genes involved in similar biological functions, such as responses to stress, light, and hormones. Using evolutionary rate covariation analysis, we also identify groups of genes that appear to have evolved together and been repurposed for carnivory from ancestral stress- and stimulus-response functions. These findings complement earlier work on gene family expansion in CPs and demonstrate that examining patterns of evolutionary rate can reveal new insights into how complex traits like carnivory evolve.
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