The evolution of condition-dependent self-fertilisation

This paper demonstrates through population-genetic modeling that selection favors condition-dependent self-fertilization, where high-condition individuals self-fertilize and low-condition individuals outcross, thereby generating stable within-population variation in mating systems and reducing mutation load.

The Gist

Imagine a world of plants that are both male and female at the same time. These "hermaphrodite" plants have a big choice to make every time they reproduce: Do I mate with a neighbor (outcrossing), or do I mate with myself (self-fertilization)?

For decades, scientists thought this choice was hardwired in a plant's DNA. They believed a species was either a "selfer" (always mates with itself) or an "outcrosser" (always mates with others), or perhaps a "mixer" that does both at a fixed rate.

But this new paper by Thomas Lesaffre, John Pannell, and Charles Mullon suggests something much more dynamic is happening. They propose that plants are actually smart decision-makers that adjust their mating strategy based on how "healthy" they feel.

Here is the story of their discovery, explained with some everyday analogies.

1. The Problem: The "Bad Genes" Burden

Every living thing carries some "junk" in their genetic code—harmful mutations.

• Healthy plants have very few of these bad genes.
• Sickly plants are carrying a heavy load of bad genes.

If a plant with a heavy load of bad genes mates with itself, those bad genes get doubled up, and the offspring are likely to be weak or die. This is called inbreeding depression. However, if a healthy plant mates with itself, it's actually a great deal: it guarantees reproduction and passes on its good genes without the risk of "junk" mixing in.

2. The Old Theory vs. The New Idea

The Old Theory: Evolution picks a fixed strategy. If inbreeding is bad, the whole population becomes outcrossers. If it's good, they all become selfers.
The New Idea (Condition-Dependent Selfing): Plants can sense their own "condition" (how much genetic junk they are carrying).

• The Healthy Plant: "I feel great! I have clean genes. I'll mate with myself to lock in my success."
• The Sickly Plant: "I feel terrible. I'm full of bad genes. If I mate with myself, my kids will suffer. I need to find a partner with good genes to fix my family tree."

3. The "Escape Hatch" Analogy

The authors use a brilliant metaphor to explain why sickly plants should avoid selfing. Imagine you are trapped in a sinking ship (a genetic background full of bad mutations).

• Staying on the ship (Selfing): If you stay, you go down with the ship. Your genes die out.
• Jumping into a lifeboat (Outcrossing): If you jump into a lifeboat (mate with a healthy neighbor), you might get rescued. Even if you are a bit damaged, you can recombine your genes with a healthy partner and survive.

The paper shows that evolution favors a rule where healthy plants stay on the ship (self), and sickly plants jump into the lifeboat (outcross).

4. What Happens in the Population?

This creates a fascinating mix within a single field of plants:

• Some plants are selfing 100% of the time.
• Some are outcrossing 100% of the time.
• Most are somewhere in between, depending on their health.

This explains why we see "mixed mating" in nature. It's not that the plants are confused; it's that they are customizing their strategy based on their personal genetic health. This actually helps the whole population because the sickly plants are constantly "purging" their bad genes by outcrossing, while the healthy ones spread their good genes efficiently.

5. The Plot Twists: Weather and Pollen

The researchers also tested what happens when things get messy in the real world:

• The Weather Factor (Environmental Noise): Imagine a plant is genetically healthy, but it's growing in a drought. It looks "sick" because of the weather, even though its genes are fine.

  • Result: If the weather is too unpredictable, the plant gets confused. It might think, "I look sick, so I should outcross," even though it's actually healthy. This confusion makes the "smart strategy" harder to evolve, but it doesn't stop it completely.

• The Pollen Discount (The Cost of Selfing): When a plant mates with itself, it often uses up pollen that it could have sent to a neighbor. This is like a store giving a discount to a customer who buys from their own shelf, but losing a sale to a competitor.

  • Result: If the cost of selfing is high (pollen discounting), the "all-or-nothing" strategy changes. Instead of a sharp switch (Healthy = Self, Sick = Outcross), the plants develop a smooth gradient. A plant might self a little bit if it's okay, but outcross more if it's really sick. It becomes a sliding scale rather than a light switch.

The Big Takeaway

This paper changes how we view plant reproduction. Instead of seeing mating systems as rigid genetic rules, we should see them as flexible, plastic responses.

Just like a human might choose a healthy diet when they feel energetic but might need a doctor's help when they feel weak, these plants adjust their mating habits based on their internal "health check." This flexibility allows nature to maintain a rich diversity of mating styles within a single population, keeping the species resilient against the constant threat of bad genes.

Technical Summary

1. Problem Statement

The evolution of mating systems in hermaphroditic organisms (plants and animals) is a central problem in evolutionary biology. Classical theory posits that selfing rates are genetically fixed and determined by a balance between the transmission advantage of selfing and inbreeding depression (the fitness cost of expressing deleterious recessive mutations). This theory predicts a "threshold effect": populations should evolve toward either complete outcrossing or complete selfing, making mixed mating (intermediate selfing rates) evolutionarily unstable.

However, empirical observations show widespread variation in selfing rates within populations and individuals often exhibit plasticity in mating behavior. While some plasticity (e.g., delayed selfing) is understood, the evolution of condition-dependent selfing—where individuals adjust their selfing rate based on their physiological or genetic "condition" (specifically their deleterious mutation load)—has not been theoretically explored. The authors ask: Does natural selection favor individuals in good genetic condition to self-fertilize while those in poor condition outcross? How does this plasticity affect mutation load, and is it robust to environmental noise and pollen discounting?

2. Methodology

The authors employed a combination of analytical population genetics and individual-based simulations to model the evolution of condition-dependent selfing.

• Two-Locus Model (Analytical):

  • Locus 1 (Condition): A diallelic locus with a wild-type allele ($A$) and a deleterious allele ($a$). Genotypes $AA$, $Aa$, and $aa$ have different fitness/condition levels ($\phi$).
  • Locus 2 (Modifier): A locus controlling the selfing rate ($\alpha$) conditional on the genotype at the condition locus. The modifier encodes specific selfing rates for each genotype ($\alpha_{AA}, \alpha_{Aa}, \alpha_{aa}$).
  • Analysis: The authors derived selection gradients to determine the evolutionary stability of different selfing strategies. They analyzed the equilibrium frequency of the deleterious allele under linear and arbitrary relationships between condition and selfing.

• Polygenic Model (Individual-Based Simulations):

  • Condition: Modeled as the cumulative effect of $L$ unlinked loci, where deleterious mutations reduce individual condition multiplicatively.
  • Plasticity Mechanism: Instead of a single modifier locus, the authors used a gene regulatory network (GRN) architecture (inspired by the Wagner model). The network takes individual condition as an input and outputs a selfing rate. This allows the evolution of complex, non-linear reaction norms without pre-specifying their shape.
  • Extensions: The model was extended to include:
    1. Environmental Heterogeneity: Adding an environmental noise term to individual condition to test if it obscures the link between genotype and phenotype.
    2. Pollen Discounting: Modeling the trade-off where increased selfing reduces the amount of pollen exported for outcrossing.

3. Key Contributions

• Theoretical Framework: The paper provides the first theoretical framework demonstrating that condition-dependent selfing is an evolutionarily stable strategy (ESS) driven by a "genetic escape" mechanism.
• Mechanism Identification: It identifies that selection favors positive condition dependence (high-condition individuals self, low-condition individuals outcross) because outcrossing allows alleles at the modifier locus to escape deleterious genetic backgrounds via recombination.
• Polygenic Realism: By using GRNs and polygenic backgrounds, the study moves beyond simplified two-locus models to show that these dynamics hold in realistic, complex genetic architectures.
• Ecological Constraints: The study quantifies how environmental noise and pollen discounting modify the shape of the evolved reaction norm, shifting it from a step-function to a continuum.

4. Key Results

A. Evolution of Positive Condition Dependence

• Escape Strategy: In a population where other genotypes are selfing, deleterious homozygotes are "trapped" in a lineage doomed to extinction due to high mutation load. A modifier allele that promotes outcrossing in these individuals allows them to recombine onto a wild-type background, effectively "escaping" the deleterious load.
• Equilibrium Strategy: The population evolves toward a strategy where:
  • High-condition genotypes (e.g., $AA$) evolve complete selfing ($\alpha \approx 1$).
  • Low-condition genotypes (e.g., $aa$) evolve complete outcrossing ($\alpha \approx 0$).
  • This creates a step-wise reaction norm.
• Mutation Load Reduction: This strategy significantly reduces the population's mutation load compared to fixed selfing rates. By purging deleterious alleles more efficiently in selfing lineages while allowing outcrossing to rescue low-condition individuals, the mean condition of the population increases.

B. Polygenic Background

• Simulations with $L=1000$ loci confirmed that the two-locus results hold in a polygenic context.
• The evolved reaction norm is a sharp threshold: individuals above a certain condition threshold self-fertilize; those below outcross.
• This plasticity maintains substantial within-population variation in realized selfing rates, explaining the prevalence of mixed mating systems.

C. Impact of Environmental Fluctuations

• When condition is influenced by environmental noise (e.g., soil quality), the correlation between genotype and phenotype weakens.
• Moderate Noise: Condition dependence still evolves but is less stable.
• Strong Noise: The evolution of condition dependence is hindered. Populations may fail to evolve the strategy, or evolve it only to lose it repeatedly, as environmental noise causes high-genetic-quality individuals to appear "low condition" and outcross unnecessarily, or vice versa.

D. Impact of Pollen Discounting

• Pollen discounting (the cost of selfing in terms of lost male reproductive success) alters the shape of the reaction norm.
• Weak Discounting: Results in the step-wise strategy (all-or-nothing).
• Strong Discounting: Favors a gradual, continuous increase in selfing rate with condition. As selfing increases, the cost of lost pollen export rises sharply. High-condition individuals can afford to self more, but the trade-off prevents them from reaching 100% selfing, creating a continuum of mating phenotypes rather than a binary split.

5. Significance and Implications

• Maintenance of Mixed Mating: The study offers a novel explanation for the persistence of mixed mating systems in nature. Instead of requiring complex spatial or temporal heterogeneity, simple condition-dependent plasticity can generate stable variation in selfing rates within a single population.
• Purging Efficiency: Condition-dependent selfing acts as a highly efficient purging mechanism. It concentrates selfing (and thus homozygosity) in individuals that can tolerate it, while protecting the population's genetic integrity by forcing low-condition individuals to outcross.
• Broader Evolutionary Context: The "genetic escape" mechanism likely applies beyond selfing. It suggests that in dioecious species, individuals in poor condition might evolve to disperse further or avoid inbreeding more strictly than those in good condition.
• Empirical Predictions: The authors propose testable hypotheses:
  • In species with herkogamy (separation of anthers and stigma), individuals in better condition should exhibit reduced herkogamy (higher selfing).
  • Experimental crosses should reveal a negative correlation between a parent's selfing rate and the inbreeding depression observed in its offspring.

In conclusion, this paper demonstrates that condition-dependent selfing is a robust evolutionary strategy that reduces mutation load and maintains mating-system diversity, challenging the classical view that selfing rates are fixed genetic traits.