📄 evolutionary biology

Conserved transcriptional plasticity, not local adaptation, dominates early climate responses across wild and cultivated apple

This study demonstrates that in both wild and cultivated apples, conserved transcriptional plasticity driven by strong purifying selection constitutes the dominant molecular response to climate variation, while local adaptation relies on distinct, population-specific loci and plays a secondary role.

Original authors: Dadole, R., Chen, X., Sandoval, J., Venon, A., Criado, M., Delpouve, N., Remoue, C., Chollet, S., Hansart, A., Laurens, F., Feugey, L., Kirisits, T., Ursu, T. M., Roman, A., Volk, G. M., Alins, G., Co

Published 2026-07-12

📖 5 min read🧠 Deep dive

CC BY 4.0

Original authors: Dadole, R., Chen, X., Sandoval, J., Venon, A., Criado, M., Delpouve, N., Remoue, C., Chollet, S., Hansart, A., Laurens, F., Feugey, L., Kirisits, T., Ursu, T. M., Roman, A., Volk, G. M., Alins, G., Conde e Silva, N., Avia, K., Bazot, S., Cornille, A. M.

Original paper licensed under CC BY 4.0 (https://creativecommons.org/licenses/by/4.0/). ⚕️ This is an AI-generated explanation of a preprint that has not been peer-reviewed. It is not medical advice. Do not make health decisions based on this content. Read full disclaimer

Imagine apple trees as long-lived travelers trying to survive a rapidly changing world. For years, scientists have debated how these trees handle climate change: do they have a special, unique genetic "survival kit" that evolved specifically for their local neighborhood (local adaptation), or do they just have a super-flexible "Swiss Army knife" that lets them adjust their behavior on the fly no matter where they are (phenotypic plasticity)?

A new study by Dadole and colleagues takes a deep dive into this question using wild and cultivated apples. They set up a massive experiment, growing 1,249 apple seedlings from five different populations (including wild apples from France, Denmark, Romania, and Armenia, plus cultivated apples) inside high-tech climate chambers called "ecotrons." These chambers simulated four distinct European climates. The researchers then watched how the seedlings survived, measured 12 different physical traits (like how fast they grew or how much color their leaves had), and even sequenced the RNA (the genetic instructions being read) of 96 of these seedlings.

The Big Discovery: The "Universal Remote" Wins
The main finding is a bit of a plot twist. The researchers found that climate was the boss. It was the dominant driver of how the trees looked and how their genes behaved. When the temperature or rain changed, almost all the apple populations—whether wild or domesticated—reacted in the exact same way.

Think of it like a universal remote control. No matter which brand of TV (apple population) you have, pressing the "hot weather" button makes them all turn up their volume or change the channel in the same way. The study identified 344 specific genes that acted as this universal remote. These genes turned on or off consistently across all populations when the climate changed. They are like a pre-installed, evolutionarily ancient software update that every apple tree carries to handle stress, nutrient shortages, and cell wall building.

What the Paper Rules Out
The study explicitly argues against the idea that local adaptation (having a unique genetic toolkit for a specific spot) is the main player in these early responses.

It's not about unique local maps: While the researchers did find 217 genetic spots (loci) that seemed linked to temperature and rain gradients, only a tiny subset of these actually showed up in the gene expression data.
It's not about different operating systems: The differences in gene expression between the different apple populations mostly just mirrored their family history (neutral genetic drift), not a special adaptation to their home climate. For instance, the differences in how genes were turned on between populations were so closely tied to how genetically different the populations were from each other that it suggested the changes were just "noise" from their history, not a clever evolutionary strategy.
Domestication didn't break the remote: Even though humans bred cultivated apples (M. domestica) for thousands of years, this "universal remote" program remained intact. Domestication changed some background details (like the amount of "junk" genetic mutations), but it didn't rewrite the core climate-response code.

How Sure Are They?
The authors are very confident about the "universal remote" finding. They measured it directly: 344 genes were consistently responsive across all groups, and statistical tests showed these genes are under "strong purifying selection," meaning nature has been very strict about keeping them unchanged for a long time. They also found that these genes carry fewer harmful mutations than other genes, suggesting they are too important to mess with.

However, their confidence regarding local adaptation is more cautious. They suggest that local adaptation exists but is a "secondary, population-specific layer." They found only a handful of candidate genes (like one specific gene in the Danish population and another in the Romanian one) that showed signs of being locally adapted. They explicitly state that while these signals exist, they are limited and mostly found in wild populations, not the cultivated ones.

The "Mutation Load" Twist
The study also looked at the "genetic baggage" the trees carry. Cultivated apples had a higher ratio of non-synonymous to synonymous mutations (a sign that natural selection is a bit more relaxed in farms than in the wild), but the core climate-response genes remained clean and mutation-free across the board. This suggests that even though farming changed the genetic landscape, the most critical survival genes were protected.

The Bottom Line
In the early stages of climate change, apple trees rely mostly on a shared, flexible, and ancient ability to adjust their genes on the fly, rather than on unique, locally evolved superpowers. While local adaptation is happening in the background for some wild populations, it's the conserved, flexible "Swiss Army knife" of gene expression that is doing the heavy lifting to keep the trees alive. The paper doesn't claim this solves the problem of future climate change, but it provides a clear map of how these trees are currently trying to cope.

Problem Statement
Rapid anthropogenic climate change imposes unprecedented pressure on perennial plant populations, raising critical questions about their capacity to adapt. While plants respond to environmental shifts through phenotypic plasticity (a single genotype producing different phenotypes) and local adaptation (genetic differentiation increasing fitness in native environments), the molecular mechanisms orchestrating these responses—and how they are reshaped by domestication—remain poorly understood. Disentangling plasticity from local adaptation is particularly challenging because demographic history can generate signals resembling adaptation. This study addresses these gaps using the apple (Malus) system, which offers a well-characterized history of domestication and distinct wild relatives (M. domestica, M. orientalis, and M. sylvestris) occupying contrasting climatic niches.

Methodology
The researchers employed an integrative approach combining controlled common-garden experiments, transcriptomics, and population genomics:

Experimental Design: 1,249 seedlings from five populations (cultivated M. domestica, M. orientalis from Armenia, and three M. sylvestris populations from France, Denmark, and Romania) were grown under four simulated European climate regimes (France, Denmark, Romania, Armenia) in climate-controlled ecotrons.
Phenotyping: Of the seedlings, 895 survived and were phenotyped for 12 morphophysiological traits, including growth rates, leaf area, chlorophyll content, flavonoid accumulation, and carbon/nitrogen stoichiometry.
Transcriptomics: RNA sequencing was performed on 96 representative individuals (spanning all population × climate combinations). Differentially expressed genes (DEGs) were identified using the DiCoExpress pipeline, with analyses conducted both on all four treatments and a subset of three (excluding Armenia due to sampling time differences) to ensure robustness.
Genomics: The study integrated RNA-seq data with previously published genome-wide polymorphism data. Analyses included:
- Calculation of neutral genetic differentiation ( $F_{ST}$ ) and absolute divergence ( $D_{XY}$ ) to identify highly divergent loci.
- Estimation of nucleotide diversity ( $\pi_N$ and $\pi_S$ ) and the ratio $\log(\pi_N/\pi_S)$ to assess purifying selection efficiency.
- Quantification of deleterious mutation loads (heterozygous and homozygous).
- Genome-environment association (GEA) analyses (using LFMM and Samβada) on M. sylvestris to link genomic variation to temperature and precipitation gradients.

Key Results

Dominance of Plasticity: Climate treatment was the primary driver of both phenotypic and transcriptional variation. While survival and growth traits varied among populations, most phenotypic responses were shared across lineages, indicating widespread, conserved plasticity.
Conserved Transcriptional Program: The study identified 344 "core" climate-responsive genes that were consistently differentially expressed across all populations and treatments. These genes were enriched for stress responses, nutrient metabolism, and cell wall biosynthesis. Crucially, these genes were under strong purifying selection (low $\pi_N/\pi_S$ ) and accumulated fewer deleterious mutations than background genes.
Limited Local Adaptation: In contrast to the conserved plastic response, signatures of local adaptation were limited. Genome-environment association analyses identified 217 loci associated with climate gradients, but only a subset showed climate-responsive expression. Population-level expression divergence closely mirrored neutral genetic differentiation ( $F_{ST}$ ), suggesting that most transcriptomic differences reflect demographic history rather than adaptive regulatory evolution.
Impact of Domestication: Domestication reshaped the genomic context without disrupting the core climate-response program. Cultivated apples (M. domestica) exhibited relaxed purifying selection (higher $\log(\pi_N/\pi_S)$ ) and a distinct mutation load profile compared to wild relatives, yet they retained the conserved transcriptional plasticity of their wild ancestors.
Population-Specific Signals: While most signals were conserved, some evidence of local adaptation was detected in specific M. sylvestris populations (e.g., French and Romanian), where candidate genes showed concordant signals of expression divergence, genomic differentiation ( $D_{XY}$ outliers), and genotype-environment associations.

Significance and Claims
The paper concludes that early climate responses in apple are primarily mediated by an evolutionarily conserved transcriptional program maintained by strong purifying selection, rather than by rapid, population-specific local adaptation. Local adaptation appears to act as a secondary, population-specific layer that fine-tunes these conserved responses. The study demonstrates that domestication has modified the genomic landscape (diversity patterns and mutation load) but has not fundamentally altered the core molecular toolkit used to respond to climate variation. These findings provide a framework for understanding climate resilience in perennial crops, suggesting that breeding and conservation strategies should prioritize the preservation of these conserved plasticity mechanisms while recognizing the role of lineage-specific adaptation in wild populations. The authors note that while their results strongly support the prevalence of conserved plasticity, determining the long-term adaptive value of these responses requires future long-term field trials linking plasticity to lifetime fitness.

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