Genetic compensation rather than genetic assimilation drives the evolution of plasticity in response to mild warming across latitudes in a damselfly

Swaegers, Janne; Spanier, Katina I.; Stoks, Robby

doi:10.1111/mec.15676

Cited by 23 publications

(30 citation statements)

References 80 publications

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“…Bootstrapping (see Methods) produced very similar proportions of reversions, overshooting and reinforcement across all gene sets, so this bias had minimal impact on our findings (Table S3). Our transcriptome-wide results are consistent with previous studies in animals and microorganisms which generally find that reversion is dominant (Ho & Zhang, 2018;Koch & Guillaume, 2020;Swaegers et al, 2020). However, the subsequent evolutionary response (EC) in many of these genes are likely to be consequences of adaptation (reduced stress/transcriptional disruption in mine populations due to their zinc tolerance, resulting in reversion of ancestral stress responses) rather than it causes (i.e., not directly involved in conferring zinc tolerance).…”

Section: Ancestral Plasticity Is Generally Reversed During Adaptationsupporting

confidence: 89%

“…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).…”

Section: Resultssupporting

confidence: 54%

“…There were six times as many genes with derived plasticity (DP genes) as with constitutive differences between ecotypes (CEC genes). In the literature, there is significant variability across taxa in the ratios of constitutive to plastic differences associated with local adaptation (Josephs et al, 2015;Heckel et al, 2016;Gugger et al, 2017;Passow et al, 2017;Feiner et al, 2018;Gould et al, 2018;Swaegers et al, 2020;Fischer et al, 2021). This may be a function of the degree to which a stressor varies temporally and spatially within a habitat.…”

Section: Rapid Evolution Of Highly Parallel Gene Expression Changesmentioning

confidence: 99%

“…Previous studies have generally found that most ancestral plasticity across transcriptomes is reversed in derived populations, taking expression values further from the new optimum (Ho & Zhang, 2018, 2019Swaegers et al, 2020;Fischer et al, 2021; although see Mäkinen et al, 2016;Mallard et al, 2020). 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).…”

Section: Introductionmentioning

confidence: 99%

“…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).…”

Section: Introductionmentioning

confidence: 99%

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Genetic assimilation of ancestral plasticity during parallel adaptation

Wood

Holmberg

Osborne

et al. 2021

Preprint

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Phenotypic plasticity in ancestral populations is hypothesised to facilitate adaptation, but evidence supporting its contribution is piecemeal and often contradictory. Further, whether ancestral plasticity increases the probability of parallel genetic and phenotypic adaptive changes has not been explored. The most general finding is that nearly all ancestral gene expression plasticity is reversed following adaptation, but this is usually examined transcriptome-wide rather than focused on the genes directly involved in adaptation. We investigated the contribution of ancestral plasticity to adaptive evolution of gene expression in two independently evolved lineages of zinc-tolerant Silene uniflora. We found that the general pattern of reversion is driven by the absence of a widespread stress response in zinc-adapted plants compared to ancestral, zinc-sensitive plants. Our experiments show that reinforcement of ancestral plasticity plays an influential role in the evolution of plasticity in derived populations and, surprisingly, one third of constitutive differences between ecotypes are the result of genetic assimilation of ancestral plasticity. Ancestral plasticity also increases the chance that genes are recruited repeatedly during adaptation. However, despite a high degree of convergence in gene expression levels between independently adapted lineages, genes with ancestral plasticity are as likely to have similar expression levels in adapted populations as genes without. Overall, these results demonstrate that ancestral plasticity does play an important role in adaptive parallel evolution, particularly via genetic assimilation across evolutionary replicates.

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Section: Ancestral Plasticity Is Generally Reversed During Adaptationsupporting

confidence: 89%

Section: Resultssupporting

confidence: 54%

Section: Rapid Evolution Of Highly Parallel Gene Expression Changesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Genetic assimilation of ancestral plasticity during parallel adaptation

Wood

Holmberg

Osborne

et al. 2021

Preprint

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Evolutionary adaptations generally reverse phenotypic plasticity to restore ancestral phenotypes during new environment adaptation in cattle

Jiang,

Zhu,

Zeng

et al. 2024

Ecology and Evolution

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Phenotype plasticity and evolution adaptations are the two main ways in which allow populations to deal with environmental changes, but the potential relationship between them remains controversial. Using a reciprocal transplant approach with cattle adapted to the Tibetan Plateau and adjacent lowlands, we aim to investigate the relative contributions of evolutionary processes and phenotypic plasticity in driving both phenotypic and transcriptomic changes under natural conditions. We observed that while numerous genetic transcriptomic changes were evident during the forward adaptation to highland environments, plastic changes predominantly facilitate the transformation of transcriptomes into a preferred state when Tibetan cattle are reintroduced to lowland habitats. Genes with ancestral plasticity are generally reversed by evolutionary adaptations and show a closer expression level to the ancestral stage in evolved Tibetan cattle. A similar trend was also observed at the phenotypes level, with a majority of biochemical and hemorheology phenotypes showing a tendency to revert to their ancestral patterns, suggesting the restoration of ancestral expression levels is a widespread evolutionary trend during adaptation. The findings of our study contribute to the debate regarding the relative contributions of plasticity and genetic changes in mammal environment adaptation. Furthermore, we highlight that the restoration of ancestral phenotypes represents a general pattern in cattle new environment adaptation.

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Gene expression studies of plastic and evolutionary responses to global warming

Swaegers

Koch

2022

Current Opinion in Insect Science

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Genetic compensation rather than genetic assimilation drives the evolution of plasticity in response to mild warming across latitudes in a damselfly

Cited by 23 publications

References 80 publications

Genetic assimilation of ancestral plasticity during parallel adaptation

Genetic assimilation of ancestral plasticity during parallel adaptation

Evolutionary adaptations generally reverse phenotypic plasticity to restore ancestral phenotypes during new environment adaptation in cattle

Gene expression studies of plastic and evolutionary responses to global warming

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