Adaptive and maladaptive expression plasticity underlying herbicide resistance in an agricultural weed

Abstract

Plastic phenotypic responses to environmental change are common, yet we lack a clear understanding of the fitness consequences of these plastic responses. Here, we use the evolution of herbicide resistance in the common morning glory (Ipomoea purpurea) as a model for understanding the relative importance of adaptive and maladaptive gene expression responses to herbicide. Specifically, we compare leaf gene expression changes caused by herbicide spray to the expression changes that evolve in response to artificial selection for herbicide resistance. We identify a number of genes that show plastic and evolved responses to herbicide and find that for the majority of genes with both plastic and evolved responses, plastic responses appear to be adaptive. We also find that selection for herbicide response increases gene expression plasticity. Overall, these results show the importance of adaptive plasticity for herbicide resistance in a common weed and that expression changes in response to strong environmental change can be adaptive.

Genetic assimilation of ancestral plasticity during parallel adaptation

“…This reveals a significant and widespread disruption to transcription in sensitive plants, consistent with the broad impact of zinc toxicity on cellular processes (Singh et al, 2016). It also indicates that, in general, greater transcriptomic perturbations in ancestral populations exposed to new environments may be driven by general stress responses (Koch & Guillaume, 2020;Swaegers et al, 2020;Josephs et al, 2021;Bittner et al, 2021). 2A).…”

“…This is true for both the identity of the genes and the magnitude of expression shifts. Previous experimental evolution studies in Drosophila, Tribolium and Ipomoea have demonstrated the evolution of gene expression plasticity in response to heterogenous environments within 22-130 generations (Huang & Agrawal, 2016;Koch & Guillaume, 2020;Mallard et al, 2020;Josephs et al, 2021). We demonstrate that this can also occur in wild plant populations in comparable timeframes and is repeatable between independent colonisations of a novel habitat.…”

“…Beneficial plasticity of this kind could be retained in locally adapted populations or genetically assimilated and canalised into constitutive expression differences (Heckel et al, 2016). Alternatively, ancestral plasticity that takes expression levels further away from the new optimum is potentially maladaptive and could hinder adaptation to the novel environment (Velotta et al, 2018;Josephs et al, 2021).…”

“…However, there are examples of ancestral plasticity in particular genes or traits facilitating subsequent adaptation (Scoville & Pfrender, 2010;Levis et al, 2018;Velotta et al, 2018;Wang & Althoff, 2019). Most expression studies on the topic examine transcriptome-wide patterns in ancestrally plastic genes, rarely considering whether genes involved in evolutionary adaptation to the new environment are more likely to have possessed beneficial ancestral plasticity, when compared to the whole transcriptome (Ho & Zhang, 2018;Koch & Guillaume, 2020;Swaegers et al, 2020;Josephs et al, 2021;Fischer et al, 2021;Bittner et al, 2021).…”

Hidden genetic variation in plasticity provides the potential for rapid adaptation to novel environments

“…Furthermore, differential expression in the high fitness genotypes occurred in functional categories associated with plasticity in the closely related high elevation (2,000m+) sister species. These results suggest that adaptation to novel environments requires genotypes that create the most beneficial gene expression profiles (Wang & Althoff 2019;Josephs 2021). This finding contrasts with evidence that adaptation to novel environments involves non-adaptive plasticity in gene expression (Ghalambor et al 2015), or that a lack of genetic variance in gene expression will prevent beneficial responses to novel environments (Oostra et al 2018).…”