Hermaphroditic sex allocation evolves with developmental trade-offs between flowers and fruits in Berchemia and Tapiscia: Insights into the evolution of androdioecy

Abstract

Angiosperm sexual systems are complex and diverse. Androdioecy, the co-occurrence of males and hermaphrodites, is rare and considered an intermediate evolutionary state between hermaphrodites and dioecy. However, the evolutionary factors that drive androdioecy remain unclear. Based on studies on Berchemia and Tapiscia life histories, it has been observed that species with long sexual reproductive cycles, in which flowers and fruits develop simultaneously, are typically androdioecious. Conversely, species with short sexual reproductive cycles in which the developmental periods of flowers and fruits do not overlap are typically hermaphroditic. Therefore, we hypothesized that a long reproductive cycle leads to the simultaneous development of flowers and fruits, creating a trade-off in reproductive resources. This trade-off ultimately drives evolution from hermaphroditism to androdioecy. To test this hypothesis, we conducted artificial experiments to remove fruits and defoliate representative species of Berchemia and Tapiscia to simulate resource release and shortage scenarios, respectively. Differences in the size and biomass of the flower parts between the treatment and control groups were compared. Our findings indicate that the simultaneous development of flowers and fruits leads to a tradeoff in reproductive resources, resulting in reduced investment in flowers. Additionally, limited resources are reallocated between female and male functions in bisexual flowers. Interestingly, when reproductive resources fluctuate, female functions are affected to a greater extent, whereas male functions are more resilient to resource changes. These results indicate that when reproductive resources are traded off, it leads to a bias toward male functions in hermaphrodites, promoting the emergence of male individuals and thus forming an androdioecious sexual system.

Keywords

androdioecy / hermaphrodite / plant life history / reproductive cycle / reproductive resource trade-off / sex allocation / sexual systems evolution

RIGHTS & PERMISSIONS

2025 Institute of Botany, Chinese Academy of Sciences.