Context-dependent selection and genetic facilitation and constraint on rosette diameter and herbivore resistance across European outdoor common gardens under ambient and reduced precipitation in Fragaria vesca

This study demonstrates that while selection consistently favors larger rosette diameter in *Fragaria vesca* across European environments, evolutionary responses in both growth and herbivore resistance are highly context-dependent, shaped by variable selection pressures and genetic covariances that can either constrain or facilitate adaptation under changing precipitation regimes.

The Gist

Imagine a plant as a small business owner trying to run a successful shop. This owner has a limited budget (energy and water) and two main departments to fund: Growth (expanding the shop, hiring more staff, building a bigger storefront) and Defense (hiring security guards, installing alarms, and buying expensive locks to keep thieves away).

The big question scientists have always asked is: Can you have a big, booming shop and a super-secure one at the same time? Or does spending money on security mean you can't afford to expand?

This paper, studying a wild strawberry plant called Fragaria vesca, goes on a grand adventure across Europe to find the answer. Here is the story of what they discovered, told simply.

The Great European Road Trip

The researchers set up three "test towns" for these strawberry plants:

1. Spain: Hot and dry (like a desert summer).
2. Belgium: Wet and lush (like a rainy garden).
3. Sweden: Cool and home to a lot of hungry bugs (like a busy city with many pickpockets).

In each town, they set up two scenarios:

• The "Normal" Town: Plants got plenty of rain.
• The "Drought" Town: They built little roofs over the plants to block out half the rain, simulating a severe drought.

They grew 16 different "families" of strawberries in each town to see how their unique genetic blueprints handled the stress.

The Two Big Rules of the Game

1. The "Bigger is Better" Rule (Growth)

In almost every single scenario, the plants that grew the biggest (had the largest "rosettes" or leafy circles) were the most successful. They produced the most fruit and the most runners (stolons) to create new baby plants.

• The Analogy: Think of the plant size like the size of a factory. A bigger factory can usually produce more goods.
• The Exception: In the hottest, driest part of Spain in 2022, being too big was a liability. It was like trying to run a massive factory during a power outage; the energy cost was too high. There, the smaller, more frugal plants actually did better.

2. The "Security Guard" Dilemma (Defense)

This is where it gets tricky. The plants' ability to resist being eaten by bugs (their "defense") didn't follow a simple rule. It depended entirely on where they were and what the weather was doing.

• In Sweden (The Bug City): When it was wet, having strong defenses paid off. But when it was dry (drought), having strong defenses became a burden. It was like hiring a security guard during a famine; you can't afford the salary. In the dry Swedish summer, the plants that stopped investing in security and just focused on growing actually survived better.
• The Takeaway: Defense is expensive. If you are already stressed by thirst, you can't afford to pay for security.

The Twist: The "Genetic Handcuffs"

Here is the most fascinating part. The researchers looked at the plants' DNA to see if there was a "genetic handcuff" linking growth and defense.

Imagine the plant's DNA as a set of instructions. Sometimes, the instructions for "Grow Big" and "Build Security" are written on the same page. If you try to change one, the other changes too.

• The Constraint: Sometimes, the DNA made it impossible to be both big and safe. If the plant tried to grow, the genes forced it to become vulnerable. This is a genetic constraint—like trying to run a marathon while wearing a heavy backpack.
• The Facilitation: Sometimes, the genes helped. Being big also made you safer, or being safe helped you grow. This is genetic facilitation—like having a turbocharger that helps both your speed and your fuel efficiency.

The Surprise: These genetic handcuffs or turbochargers didn't work the same way everywhere.

• In Sweden during a drought, the genetic "handcuffs" actually helped the plants evolve to be less defensive and bigger. The environment forced the DNA to let go of the old rules.
• In other places, the genetic rules stayed the same, or didn't matter much.

The Final Lesson: There is No "One Size Fits All"

The main message of this paper is that evolution is not a straight line; it's a chaotic dance.

You cannot predict how a plant will evolve just by looking at its genes or just by looking at the weather. You have to look at the combination of the two.

• A trait that is a "superpower" in a wet, bug-free garden might be a "kryptonite" in a dry, bug-filled forest.
• The genetic rules that bind a plant's traits together can snap or tighten depending on the season and the location.

In simple terms: Nature doesn't have a single rulebook. A strategy that works in Sweden might fail in Spain. The plants that survive are the ones that can read the room, adapt their spending (growth vs. defense), and hope their genetic "blueprint" allows them to make the switch quickly enough.

This study shows us that as our climate changes and gets more unpredictable, plants will face a constant, shifting game of "what works best right now," making it very hard for us to predict exactly how they will change in the future.

Technical Summary

Title

Context-dependent selection and genetic facilitation and constraint on rosette diameter and herbivore resistance across European outdoor common gardens under ambient and reduced precipitation in Fragaria vesca.

1. Problem Statement & Objectives

Plants face a fundamental trade-off between allocating resources to growth (competitive ability, resource acquisition) and defense (herbivore resistance). While this "growth-defense trade-off" is well-documented, the evolutionary dynamics are complex:

• Genetic Architecture: Genetic correlations (pleiotropy or linkage disequilibrium) can either constrain adaptation (if traits are negatively correlated but selection favors both) or facilitate it (if correlations align with selection).
• Environmental Context: These trade-offs and genetic correlations may shift across space and time, particularly under abiotic stressors like drought.
• Fitness Components: In clonal plants, fitness is derived from both sexual reproduction (seeds/fruits) and asexual propagation (stolons), yet few studies analyze how selection acts on these distinct components simultaneously.

Objective: This study aimed to quantify directional and correlational selection on rosette diameter (growth proxy) and herbivore resistance across varying environments (ambient vs. reduced precipitation). It further sought to determine how environment-specific genetic (co)variance matrices (G-matrices) align with selection gradients to predict evolutionary responses ($\Delta z = G\beta$) and identify instances of genetic constraint or facilitation.

2. Methodology

• Study System: Fragaria vesca (woodland strawberry), a perennial clonal plant.
• Experimental Design:
  • Sites: Three outdoor common gardens along a South-North European gradient: Spain (Rascafría), Belgium (Gontrode), and Sweden (Alnarp).
  • Genotypes: 16 wild genotypes collected from distinct populations across the species' European range.
  • Treatments: A split-plot design with two precipitation regimes: Control (ambient) and Reduced Precipitation (50% reduction via rainout shelters).
  • Duration: Two years (2021 and 2022).
  • Replication: ~310 plants per site (total $n=930$), with 10–20 clonal replicates per genotype per treatment.
• Data Collection:
  • Resistance: Measured as the inverse of chewing herbivore damage (leaf area removed). To control for "apparency" (larger plants attracting more herbivores) and latitudinal clines, resistance was adjusted using Generalized Linear Mixed Models (GLMMs) to remove the effects of rosette size and latitude.
  • Growth: Rosette diameter (cm).
  • Fitness Proxies:
    • Sexual: Number of ripe fruits.
    • Asexual: Number of stolons.
• Statistical Analysis:
  • Selection Gradients ($\beta$): Estimated using GLMMs (negative binomial distribution) for fruit and stolon production separately in each environment (Site $\times$ Year $\times$ Treatment). Both directional (main effects) and correlational (interaction) selection were calculated.
  • Genetic (Co)variance ($G$): Estimated using Bayesian bivariate GLMMs to generate environment-specific G-matrices (latent scale converted to observed scale).
  • Evolutionary Response: Calculated using Lande's equation: $\Delta z = G\beta$.
  • Constraint/Facilitation: Quantified by comparing the predicted response with the full G matrix ($RV_1$) versus a diagonalized G matrix with zero covariances ($RV_0$).
    • Facilitation: Covariances increase the response in the direction of selection.
    • Constraint: Covariances reduce the response in the direction of selection.

3. Key Results

• Selection on Growth (Rosette Diameter):

  • Consistent Direction: Selection consistently favored larger rosette diameters for both fruit and stolon production across nearly all environments (11/12 cases).
  • Exception: In Spain (2022, reduced precipitation), selection favored smaller rosettes, likely due to severe drought stress where large size incurs metabolic costs.
  • Evolutionary Response: The predicted response ($\Delta z$) was strongly positive for larger rosettes across all sites, with the strongest response in Belgium (the wettest site).

• Selection on Resistance:

  • Context-Dependent: Selection on resistance was highly variable and often non-significant.
  • Sweden (2021): Higher resistance was favored (associated with more fruits).
  • Sweden (2022, Drought): Lower resistance was favored (associated with more fruits and fewer stolons), suggesting a metabolic cost of defense under water stress.
  • Stolon Production: Higher resistance was consistently associated with fewer stolons in Sweden and Spain (2022), indicating a trade-off where resources allocated to defense reduce clonal propagation.

• Correlational Selection:

  • Generally absent, with few exceptions.
  • Sweden (2022, Drought): Synergistic selection favored plants with both high resistance and large rosettes for fruit production, suggesting that under high herbivory and drought, only plants capable of sustaining both traits succeed sexually.
  • Spain (2022, Drought): Conflicting selection; sexual fitness favored small/low-resistance plants, while asexual fitness favored large/high-resistance plants.

• Genetic Constraints and Facilitation:

  • Significant constraints or facilitation were detected only in Sweden (the site with the highest herbivory) under drought conditions.
  • 2021 (Sweden, Drought): Genetic covariances facilitated the evolution of increased resistance and larger rosettes for fruit production. However, for stolon production, covariances constrained the evolution toward smaller rosettes and reduced resistance.
  • 2022 (Sweden, Drought): The pattern reversed; covariances facilitated the evolution of reduced resistance and increased rosette diameter.
  • Conclusion: The genetic architecture (G-matrix) did not consistently constrain or facilitate evolution; its effect shifted rapidly based on the specific year and reproductive mode.

4. Key Contributions

1. Decoupling Fitness Modes: The study explicitly demonstrates that selection gradients and evolutionary responses can differ significantly between sexual (fruit) and asexual (stolon) fitness components, highlighting the complexity of predicting evolution in clonal plants.
2. Dynamic G-Matrices: It provides empirical evidence that the G-matrix is environment-dependent. The same genetic correlations that facilitate adaptation in one year (2021) can constrain it or reverse direction in the next (2022) under similar stress conditions.
3. Growth-Defense Trade-offs: The results challenge the universality of the growth-defense trade-off. While a trade-off existed for asexual reproduction (high resistance $\to$ low stolons), sexual reproduction in some contexts favored the simultaneous expression of both traits, provided the plant was large enough to support the metabolic cost.
4. Drought Interaction: The study clarifies that drought does not simply suppress defense; it alters the cost-benefit ratio of defense, sometimes favoring reduced resistance to conserve water and resources for growth.

5. Significance

This research underscores the difficulty of predicting evolutionary trajectories under climate change. Because selection gradients and genetic covariances are both highly context-dependent (varying by site, year, precipitation, and reproductive mode), simple models assuming static trade-offs are insufficient.

The findings suggest that standing genetic variation in plant traits may be maintained by fluctuating selection pressures and shifting genetic constraints. For Fragaria vesca, the ability to respond to selection is not a fixed property of the population but a dynamic interaction between the environment and the genetic architecture. This has broad implications for understanding how plant populations might adapt to increasing frequency of extreme weather events (droughts) and changing herbivore pressures.