Disentangling the influence of environmental conditions on sex determination in haplodiploid organisms

Abstract Sex determination is essential for the life history of sexually reproducing organisms. Understanding the mechanism behind sex determination decisions, however, is not trivial, as processes such as random meiosis can shape the sex of the offspring besides environmental conditions. Haplodiploid organisms are relatively unconstrained from these internal influences: Males develop from unfertilized and females from fertilized eggs. Females can thus base sex allocation on their individual parental expenditure and account for the prevalent environmental conditions they live in. We aim to disentangle the influence of environmental conditions on sex determination and resource allocation decisions of haplodiploid organisms (population sex ratio, individual sex allocation probability, individual resource allocation and foraging efficiency). For this, we studied the European orchard bee ( Osmia cornuta ) at a high spatial and temporal resolution in a quantitative field study. We applied a recently developed camera system and deep‐learning‐based evaluation toolset that allowed us to analyse over 1000 pollen collection flights (food provisioning for offspring) and over 800 clay collection flights (nest‐building material) to test whether sex determination and resource allocation in haplodiploid organisms depend on environmental conditions. Contrary to expectations based on established sex determination theories, the overall population sex ratio and individual offspring resource allocation were independent of environmental conditions. Individual sex allocation probability, however, shifted with flower cover, connectivity of seminatural habitat, temperature and progressing season. Pollen and clay collection durations, proxies for foraging efficiency, were not influenced by available resources in the landscape. Instead, pollen collection efficiency decreased with higher temperatures and clay collection efficiency decreased with lower temperatures and progressing season (both represented by increasing flight durations). A short‐term insurance strategy may explain the diverse influences of environmental conditions on individual sex allocation probability, whereas long‐term bet‐hedging might result in consistent offspring resource allocation and population sex ratio within a year, with potential carry‐over effects into the next generation. We therefore conclude that sex determination is not monocausal and that nest‐provisioning females might pursue multiple aims at the same time. We emphasize the importance of long‐term data to further unravel the sex determination mechanisms of sexually reproducing organisms.

The authors unravel how environmental conditions influence sex determination and resource allocation in a haplodiploid bee species. Using high‐resolution field data, they show that individual sex allocation shifts with environmental conditions, while population sex ratio and individual resource allocation remain stable, highlighting the complexity of maternal decision‐making in solitary bees. image