UC Berkeley

Nestmate recognition is an essential component of fitness for all eusocial insects yet is vulnerable to disruption by common processes such as population bottlenecks associated with introductions. Disrupted nestmate recognition systems, such as those resulting from species introductions, can permit the growth of vast networks of genetically similar yet spatially disconnected nests called supercolonies. Though supercoloniality is a common feature of many widespread and destructive invasive ant species, its stability and evolutionary consequences are still poorly understood. In this dissertation, I integrate behavioral, chemical, and genomic data across spatiotemporal scales to characterize the genomic consequences of supercoloniality in one of the most abundant and widespread invasive ants in California, Linepithema humile. As supercoloniality is often cited as a major contributing factor in shaping the scale and impact of eusocial insect invasions, understanding its ecological and evolutionary consequences can directly inform management strategies and provide insights into the evolution of social behavior.In the first chapter of this dissertation, I present the results of a statewide resurvey of twenty L. humile populations, using behavioral assays to assess the stability of the globally widespread Large Supercolony over a multi-decadal timescale. By sequencing ultra-conserved elements from ants collected between 1964 and 2024, I show that the Large Supercolony has been present in California for at least 60 years but has undergone extensive turnover in the last 25-27 years. Analysis of behavioral, chemical, and genomic data from twenty different sites indicates that all instances of turnover represent the expansion of a single, genetically diverse supercolony first identified near Lake Hodges in Escondido, California.In the second chapter, I examine how direct behavioral interactions between supercolonies shape selection at genes associated with nestmate recognition. By mapping colony boundaries and sequencing a panel of candidate colony recognition genes from workers collected at different distances from the boundary, I test whether the presence of a competing supercolony is associated with relaxed selection at colony recognition genes. While there were no significant differences in the strength of selection relative to the colony boundary, there were genetic differences between workers collected close to and far from the boundary, suggesting fine-scale population structure associated with the social environment. Most distance-associated differences were found in a population where the boundary between supercolonies has been present for over twenty years, which may indicate that genetic differentiation between nests in different social environments accumulates over time, despite the potential for connectivity between nests adjacent to boundaries and several hundred meters away. Furthermore, distance-associated genetic variants in the Large Supercolony were primarily located within candidate colony recognition genes, while in the Lake Hodges supercolony variants were identified across most of the different gene families tested in the study.In the third and final chapter, I use whole-genome sequencing to characterize how population structure has changed in the Large Supercolony and Lake Hodges supercolony over a 23–25-year period. By identifying regions consistently differentiated between the two supercolonies over time, I compile a list of candidate genes that may contribute to the distinct chemical, behavioral, and morphological phenotypes of each supercolony. I also identified regions showing differential signatures of selection between supercolonies, which may reflect different evolutionary processes acting in the high-diversity Lake Hodges and low-diversity Large Supercolony. The temporal genomic results provide insights into potential mechanisms underlying the recent spread of the Lake Hodges supercolony, including the presence of mutations in genes associated with pesticide resistance and exploratory behavior.Together, these results highlight a previously undescribed process of large-scale turnover in invasive ant supercolonies and explore the social, environmental, and evolutionary factors that contribute to the maintenance and erosion of supercolony boundaries. They represent a fundamental step towards understanding how social structure shapes invasiveness and provide a foundation for future studies exploring the functional implications of genetic differences between supercolonies.