Carlos Roberto Fonseca, Universidade Federal do Rio Grande do Norte (UFRN) in Brazil, discusses his article: The Red Queen unveils the sexual and mating strategies of flowers
In 1876, Charles Darwin wrote the book “The effects of cross and self-fertilization in the vegetable kingdom” to answer a simple, but important question: if self-fertilisation is the easier way to produce seeds, why have so many species developed numerous mechanisms to allow or enforce cross-fertilisation? After showing data from 13 years of breeding experiments performed in his gardens, he concluded that “cross-fertilisation is generally beneficial and self-fertilisation injurious”. Although Darwin clearly demonstrated the phenomenon of inbreeding depression caused by self-fertilisation, the mechanisms behind the benefits of cross-fertilisation remained to be uncovered. In a comparative study performed across 1884 European plants, we found evidence that herbivory pressure, caused by insects feeding on leaves, stems, roots, and other plant parts, caused the evolution of many key sexual and mating traits determining outcrossing levels.
The theory
We did not find that by chance. Instead, this was a direct prediction of the Red Queen Hypothesis, proposed by the evolutionists D. A. Levin and W. D. Hamilton, which states that sex is an adaptation of hosts against their parasites (defined as short-lived natural enemies).
The reasoning behind such theory is that, due to their shorter life-cycles, the evolutionary rates of attack genes of parasites are much higher than the evolutionary rates of the hosts’ defence genes. If hosts reproduce asexually, producing copies of themselves generation after generation, their defence genes tend to quickly become obsolete. In contrast, sexual hosts, in each reproductive event, mix half of their defence genes with half of their partners to produce offspring with unique or rare combinations of defences. So, sex makes the parasite’s life much more difficult.
The predictions
In plants, there are many floral traits that determine whether a plant performs auto-fertilisation, producing offspring that mix the defences already present in the genome of the parent plant, or cross-fertilisation, producing offspring that are a mixture of the defence genes of the parent plant with the defence genes of neighbour plants. In our study, we tested the interspecific prediction that plant species associated with a higher richness of insect herbivores (used as a proxy for a higher, more diverse, and consistent herbivory pressure over geographic space and evolutionary time) should have sexual and mating traits leading to outcrossing.
Our findings
The results were striking. Nine out of the ten selected sexual and mating traits which modulate outcrossing levels responded as expected to the insect richness gradient (from one to 501 herbivore species per plant species).
For instance, the probability to be self-incompatible, a fundamental reproductive trait controlled by a few genes, went from 20% to 70% across the insect richness gradient. Also, hermaphrodite plants associated with more insect herbivores had a higher probability for their male and female organs to mature asynchronously, therefore inhibiting selfing.
The probability of hermaphroditism dropped from 46% to 3% along the insect richness gradient, while the probability of exhibiting flowers and plants with different sexual strategies increased, promoting outcrossing.
Furthermore, plants used by a higher richness of insect herbivores had a higher probability to cross-fertilise and exhibited a higher pollen to ovule ratio, a metric traditionally seen as a quantitative proxy of breeding system. This corroborates a recent study in which we demonstrated that hermaphroditic plants used by more insects allocate relatively more biomass to the male organs rather than to the female organs, thus displaying higher flower maleness.
Finally, we demonstrated that plants used by a lower richness of insect herbivores had a higher tendency to also use non-sexual means of reproduction (e.g., stolons), while plants under stronger herbivory pressure were more prone to reproduce exclusively by sex-generated seeds.
Further implications for pollination biology
Our results also help to explain the question “Why do plants hire costly pollinators to perform cross-fertilisation?” Indeed, we found out that insect-pollinated plants used by a higher richness of insect herbivores have a higher dependence on their mutualistic pollinators to perform cross-fertilisation, relying less on self-fertilisation. This suggests that when plants are under relatively weaker herbivory pressure, they can rely on self-fertilisation or low cost, small-bodied pollinators, while plants under higher pressure are obliged to hire high-cost, large-bodied pollinators which can perform long-distance pollen exchange, insuring unique and well defended offspring.
Additionally, our results also demonstrated that wind-pollinated plants under higher herbivory pressure, instead of relying on self-fertilisation, have higher dependence on wind to perform cross-fertilisation.
Conclusion
Although it is widely recognised that flower evolution is closely linked to their associated mutualistic pollinators, here we showed that antagonistic insect herbivores play an important role in the evolution of many key sexual and mating traits of plants. So, 150 years after Darwin formulated a very important question concerning the reproductive strategy of plants, we provide multiple pieces of evidence that Red Queen dynamics modulate the evolution of the inbreeding-outcrossing gradient across the angiosperms.
