Male-biased sexual selection persists across contrasting habitats in a dioecious plant

This study demonstrates that despite habitat degradation altering pollinator interactions, male-biased sexual selection persists in the dioecious plant *Silene dioica*, with anthropogenic environments specifically intensifying selection on male floral traits while maintaining consistent selection on female fertility-related traits.

The Gist

Imagine a bustling dance hall where the music is played by insects (pollinators) and the dancers are plants. In this dance, the goal is to find a partner to pass on your genes. This study looks at a specific type of plant called Silene dioica (a red campion), which is unique because it has separate "male" and "female" plants, much like humans.

The researchers wanted to know: Does the environment change the rules of the dance? Specifically, they compared plants dancing in quiet, natural forests versus those dancing in noisy, human-made landscapes (like roadsides and farms).

Here is the story of their findings, broken down with some everyday analogies:

1. The Setting: The Forest vs. The City

The scientists set up six dance floors: three in deep forests and three in "anthropogenic" (human-altered) areas.

• The Expectation: They thought the "city" dance floors would be chaotic. They expected fewer insects (dancers) and that the plants would struggle to find partners.
• The Reality: Surprisingly, the "city" wasn't that empty. While the rate of visits per flower was slightly lower (because the city plants had huge, flashy displays that distracted the insects), the overall quality of the "dance" (pollination) was just as good as in the forest. The insects were still doing their job well.

2. The Female Dancers: The "Resource Managers"

Think of the female plants as event planners. Their job is to host the party and make sure there are enough seats (ovules) for the guests.

• What they needed: They didn't need a million guests; they just needed enough to fill the seats. Once the seats are filled, having more guests doesn't help the event planner get more "points."
• The Result: In both forests and cities, the female plants were selected based on how many "seats" they had (how many flowers and ovules they produced).
• The Twist: In the city, the selection for having more flowers was actually stronger. But this wasn't because the city was empty; it was because the city plants varied wildly in size. The "biggest" planners stood out more in the city crowd. Crucially, having more dance partners didn't help the females produce more seeds. Once the job was done, extra partners were just extra noise.

3. The Male Dancers: The "Salesmen"

Now, think of the male plants as salesmen trying to sell as much product (pollen) as possible.

• The Strategy: Unlike the event planners, the salesmen never feel like they have "enough" customers. Every new customer is a potential sale.
• The Result: The study confirmed a classic rule of biology: Male success is all about how many partners they find. The more female plants a male "danced" with, the more offspring he had. This held true in both the forest and the city.
• The City Challenge: In the city, the "salesmen" faced a different pressure. The study found that male plants with a specific trait—a deeper flower cup (calyx height)—were more successful in the city.
  • The Analogy: Imagine the city is a windy, noisy street. To sell your product, you need a better "grip" on the customer. A deeper flower cup acts like a better grip, ensuring the insect grabs the pollen and doesn't drop it. In the quiet forest, a simple handshake was enough, but in the city, you needed a firm handshake to win the sale.

4. The Big Takeaway: The "Male Bias" Persists

The most important lesson from this paper is that nature's rules for men and women (or male and female plants) stay different, even when the environment changes.

• Females are limited by their own resources (how many seeds they can make). They don't get "richer" just because they have more partners.
• Males are limited by their ability to find partners. They get "richer" (more offspring) the more partners they find.

Even when the environment gets tough (like in human-altered landscapes), this fundamental difference remains. The males are still the ones fighting harder to attract attention and secure as many partners as possible, while the females are focused on managing the resources they already have.

Summary in One Sentence

Even when the "dance floor" changes from a quiet forest to a busy city, the female plants focus on making sure their "seats" are full, while the male plants keep fighting to find as many new dance partners as possible, proving that the pressure to "win" the mating game is still much stronger for the males.

Technical Summary

1. Problem Statement and Research Context

The study addresses a gap in evolutionary ecology regarding how land-use change and habitat degradation affect sex-specific sexual selection in plants.

• Theoretical Background: Sexual selection theory predicts that male reproductive success is more constrained by mate acquisition (pollinator visits) than female success, which is often limited by resources. Consequently, selection on attractive floral traits should be stronger in males.
• The Conflict: Anthropogenic disturbances (e.g., agriculture, urbanization) often reduce pollinator density. Theory suggests that under pollen limitation, female reproductive success becomes equally dependent on mate acquisition, potentially equalizing selection pressures between sexes or altering the strength of selection on floral traits.
• Knowledge Gap: Most empirical studies focus on female reproductive success (seed production) or hermaphroditic species. There is a lack of comprehensive data on how habitat variation alters selection patterns in dioecious species (separate male and female individuals) and whether male-biased sexual selection persists under environmental stress.

2. Methodology

The researchers conducted a field study on the dioecious plant Silene dioica (Red Campion) across six populations in Northern France.

• Study Design:

  • Habitats: Three populations in forest habitats (low anthropogenic impact, >90% natural) and three in anthropogenic habitats (agricultural/urban, >40% human-modified).
  • Sampling: 50 male and 50 female plants were tagged per population (600 total). Surrounding plants were clipped to ensure controlled pollination dynamics.
  • Duration: A 10-day monitoring period during peak flowering.

• Data Collection:

  • Floral Traits: Measured corolla width, calyx height, number of open flowers, gamete count (ovules for females, pollen grains for males).
  • Pollinator Metrics: Recorded visitation rates and diversity (Hymenoptera, Diptera, etc.) across 12 sessions per population.
  • Pollination Service Quality: A hand-pollination experiment using potted plants (Open vs. Hand-pollinated) to test for pollen limitation in both habitats.
  • Reproductive Success (RS):
    • Females: Estimated via total seed production (fruits × seeds/fruit).
    • Males: Estimated via paternity analysis using microsatellite markers on 4,800 offspring. A spatially explicit mating model estimated the number of seeds sired by each male.
  • Mating Success: Estimated via categorical paternity assignment (number of unique sexual partners).

• Statistical Analysis:

  • Selection Gradients: Calculated using Lande & Arnold regression (relative RS vs. standardized traits).
  • Structural Equation Modeling (SEM): Used to disentangle direct effects of traits on RS versus indirect effects mediated through mating success.
  • Bateman Gradients: Analyzed the relationship between mating success and reproductive success to quantify the strength of sexual selection.
  • Controls: Models accounted for inbreeding (internal relatedness) and spatial genetic structure.

3. Key Results

A. Habitat and Pollinator Dynamics

• Visitation Rates: Flowers in anthropogenic habitats received 1.4 times fewer visits per flower than those in forests. However, the total number of visits per hour did not differ significantly.
• Cause: The lower visitation rate in anthropogenic sites was driven by larger floral displays (more flowers per plant) in those habitats, not a lack of pollinators.
• Pollination Service: Hand-pollination experiments revealed no pollen limitation in either habitat. Fruit set and seed set were comparable between open and hand-pollinated plants, indicating that natural pollination was sufficient to fertilize available ovules in both environments.

B. Selection on Floral Traits

• Females: Selection acted primarily on fertility-related traits (number of ovules and number of open flowers).
  • Selection on flower number was significantly stronger in anthropogenic habitats, but this was attributed to higher trait variance in those populations rather than reduced pollinator quality.
  • Crucially, mating success (number of partners) did not predict female reproductive success.
• Males: Selection patterns were more complex.
  • Selection on calyx height (a trait influencing pollen removal efficiency) was significantly stronger in anthropogenic habitats.
  • Unlike females, male reproductive success showed a strong, positive dependence on mating success across all populations.

C. Sexual Selection and Bateman Gradients

• Male Bias: A significant positive Bateman gradient (relationship between mating success and reproductive success) was found in males in 5 out of 6 populations. This confirms that male fitness increases with the number of mates.
• Female Neutrality: No positive relationship was found between mating success and reproductive success in females; in some cases, the relationship was negative.
• Habitat Effect: The strength of the male Bateman gradient did not differ between forest and anthropogenic habitats. Male-biased sexual selection persisted despite the altered landscape.

4. Key Contributions

1. Sex-Specific Perspective: The study demonstrates that focusing solely on female reproductive success provides an incomplete picture of floral evolution. It highlights that male and female selection pressures respond differently to environmental change.
2. Persistence of Male Bias: Contrary to the hypothesis that pollen limitation would equalize selection pressures, the study shows that male-biased sexual selection persists even in anthropogenic habitats where pollinator visitation rates are lower.
3. Mechanism of Selection: The findings suggest that in S. dioica, male reproductive success is driven more by post-pollination processes (e.g., pollen competition, efficient pollen transfer via calyx height) than by simple pollinator attraction (corolla width).
4. Trait Variance vs. Selection Strength: The study clarifies that differences in selection strength between habitats can sometimes be statistical artifacts of trait variance rather than changes in the underlying fitness function.

5. Significance and Implications

• Evolutionary Resilience: The results suggest that common, generalist-pollinated dioecious plants may be more resilient to land-use changes than previously thought, as their reproductive success is not immediately limited by pollinator decline in these specific contexts.
• Conservation Biology: Conservation strategies should consider sex-specific selection pressures. While female fitness may be resource-limited, male fitness remains tightly coupled to mate acquisition, meaning that traits facilitating efficient pollen transfer (even if not "attractive" in the traditional sense) are critical for male fitness in degraded habitats.
• Theoretical Refinement: The study supports the anisogamy hypothesis (males compete for mates, females compete for resources) even under sub-optimal pollination conditions, challenging the notion that environmental stress automatically shifts selection to favor female mate-acquisition traits.

In summary, the paper provides robust evidence that male-biased sexual selection is a persistent force in Silene dioica, operating independently of habitat type, and that the primary driver of male fitness is the efficiency of pollen transfer and the number of mates, rather than the sheer quantity of pollinator visits.