The genomes of two key bumblebee species with primitive eusocial organization

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Genomic signatures of evolutionary transitions from solitary to group living

The evolution of eusociality is one of the major transitions in evolution, but the underlying genomic changes are unknown. We compared the genomes of 10 bee species that vary in social complexity, representing multiple independent transitions in social evolution, and report three major findings. First, many important genes show evidence of neutral evolution as a consequence of relaxed selection with increasing social complexity. Second, there is no single road map to eusociality; independent evolutionary transitions in sociality have independent genetic underpinnings. Third, though clearly independent in detail, these transitions do have similar general features, including an increase in constrained protein evolution accompanied by increases in the potential for gene regulation and decreases in diversity and abundance of transposable elements. Eusociality may arise through different mechanisms each time, but would likely always involve an increase in the complexity of gene networks.

Multifemale nests and social behavior in Euglossa melanotricha (Hymenoptera,Apidae, Euglossini)

The nesting biology and social behavior of the euglossine bee species Euglossa melanotricha was analyzed based on the monitoring of eight nests found in man-made cavities and transferred to observation boxes. Euglossa melanotricha females usually construct their nests in cavities in the ground, in buildings, or in mounds. In this study, we present new data on the nesting biology of E. melanotricha. The process of reactivation of nests was commonly observed with one to three females participating in the reactivation. The duration of the process of reactivation ranged from 10 to 78 days (n = 31) and were longer during the rainy season. Time spent (in days) for provisioning, oviposition and closing a single cell was higher in reactivations that occurred during the dry period. 151 emergences were observed (39 males and 112 females). 90 (80.3%) of the emerged females returned to the natal nest, but only 35(38.9%) remained and actively participated in the construction and provisioning of cells. The other 55 abandoned the nests after several days without performing any work in the nest. Matrifilial nest structure was regulated by dominance-subordinate aggressive behavior among females, where the dominant female laid almost all eggs. Task allocation was recognized by behavioral characteristics, namely, agonism and oophagy in cells oviposited by other females. Euglossa melanotricha is multivoltine and its nesting is asynchronous with respect to season. Our observations suggest a primitively eusocial organization. These observations of E. melanotricha provide valuable information for comparison with other species of Euglossa in an evolutionary context.

Demography in eusocial Hymenoptera

In my doctoral thesis I investigated the evolution of demographic traits within eusocial Hymenoptera. In the social bees, wasps and ants, eusociality has a unique effect on life span evolution as female larvae with the same genetic background can develop through phenotypic plasticity to a queen or a worker with vastly diverging life-history traits. Ant queens belong to the longest-lived insect species, while workers in most species live only a fraction of the queen’s life span. The average colony size of a species is positively correlated with social complexity, division of labor and diverging morphological female phenotypes all of which also affect life span. Therefore the demographic traits of interest in this thesis were life span and colony size. To understand the evolution of worker life span I applied a trade-off model that includes both hierarchical levels important in eusocial systems, namely the colony- and the individual-level. I showed that the evolution of worker life span may be an adaptive trait on the colony level to optimize resource allocation and therefore fitness in response to different levels of extrinsic mortality. A shorter worker life span as a result of reduced resource investments under high levels of extrinsic mortality increases colony fitness. In a further study I showed that Lasius niger colonies produce different aging phenotypes throughout colony development. Smaller colonies which apply a different foraging strategy than larger colonies produced smaller workers, which in turn have a longer life span as compared to larger workers produced in larger colonies. With the switch to cooperative foraging in growing colonies individual workers become less important for the colony caused by their increasing redundancy. Alternatively a trade of between growth and life span may lead to the results found in this study. A further comparative analysis to study the effect of colony size on life span showed a correlation between queen and worker life span when colony size is taken into account. While neither worker nor queen life span was associated with colony size, the differences between queen and worker life span increase with larger average colony sizes across all eusocial Hymenoptera. As colony size affects both queen and worker life span, I aimed to understand which factors lead to the small colony sizes displayed by some ant species. I therefore analyzed per-capita productivity at different colony sizes of eight cavity dwelling ant species. Most colonies of the study species grew larger than optimal productivity predicted. Larger colony size was shown to increase colony homeostasis, the predictability of future productivity and in turn the survival probability of the colony. I also showed that species that deploy an individual foraging mode may circumvent the density dependent decline in foraging success by splitting the colony to several nest sites.

Monophyly and extensive extinction of advanced eusocial bees: Insights from an unexpected Eocene diversity

Advanced eusociality sometimes is given credit for the ecological success of termites, ants, some wasps, and some bees. Comprehensive study of bees fossilized in Baltic amber has revealed an unsuspected middle Eocene (ca. 45 million years ago) diversity of eusocial bee lineages. Advanced eusociality arose once in the bees with significant post-Eocene losses in diversity, leaving today only two advanced eusocial tribes comprising less than 2% of the total bee diversity, a trend analogous to that of hominid evolution. This pattern of changing diversity contradicts notions concerning the role of eusociality for evolutionary success in insects.