Variation in fitness is an underlying tenet of adaptive evolution, and as such it is an essential goal of evolutionary biology to understand the mechanisms and forces that generate it. We explored two mechanisms that could potentially generate variation in fitness in the invasive fire ant, Solenopsis invicta: within-individual genetic diversity and viral infection. In order to explore the former, we conducted a heterozygosity-fitness association (HFA) study across twelve fitness-related traits in S. invicta queens and incipient colonies. Analyses revealed that HFAs are uncommon in our study population, with queen multilocus heterozygosity a significant predictor of just a small subset of the fitness traits that we measured. The same analyses also highlighted the influence exerted by stress, life-history tradeoffs, and variation in life-cycle stages assayed on HFAs in our system. An analytical pipeline, HeFPipe, was constructed to facilitate and streamline future HFA studies.In order to explore the effects of viral infection on fitness of S. invicta queens and incipient colonies, we looked for differences across the same fitness-related traits leveraged in the HFA study between queens infected by various permutations of three positive, single-stranded RNA viruses, SINV-1, -2, and -3, and uninfected queens. We demonstrated that at least one virus infecting fire ants, SINV-2, has significant, negative effects on several traits associated with early queen and colony growth and survival. Our evidence for clear fitness costs of SINV-2 on S. invicta queens and colonies runs contrary to previous studies suggesting this virus is largely asymptomatic. Our study highlights how rigorous, quantitative measurements of fitness-related traits may reveal significant host effects of viruses that otherwise would go undetected. Such quantitative studies will become important from medical, agricultural, economic, and conservation perspectives as globalization continues to bring viruses into contact with an increasing diversity of hosts.
