Does protection against natural enemies help in the spread of symbionts in insect populations?

Author(s)

Cássia de Souza Siqueira Cesar

• Document type: Doctoral Thesis
• Press: São Paulo.
• Institution: Universidade de São Paulo (USP). Instituto de Biociências (IBIOC/SB)
• Defense date: 2024-09-13

Examining board members

Rodrigo Cogni; Brandon Cooper; Julien Martinez

• Advisor: Rodrigo Cogni; André Coppe Pimentel

Abstract

Symbiosis is extremely common in nature and comprises interactions that vary from harmful (i.e., parasitism) to advantageous (i.e., mutualism). Symbionts are widely spread among terrestrial arthropods, especially insects, and many abiotic and biotic factors can influence the abundance and distribution of symbionts. For example, there are facultative bacterial symbionts (symbionts hereafter) that can manipulate the reproduction of their hosts (i.e., reproductive parasitism), enhancing the proportion of infected individuals across generations. However, not all symbionts found infecting insects are reproductive parasites. Taking Wolbachia as an example, until recently it was believed that reproductive parasitism was the main reason for its successful spread in nature. However, there are Wolbachia strains found infecting natural insect populations that are not reproductive parasites. Other symbionts such as Hamiltonella are also frequently found infecting aphid populations but are not reproductive parasites. Many studies in the last two decades showed that there are several defensive symbionts (i.e., symbionts that protect hosts against natural enemies) infecting insects, such as Wolbachia, Hamiltonella, Spiroplasma, among others. These symbionts can protect their hosts against a great variety of natural enemies such as viruses, bacteria, fungi, and parasitoids. Thus, the successful spread of symbionts among insects may be in part attributed to the mutualistic benefit provided by symbionts in protecting their hosts against natural enemies. Here, we tested the hypothesis that symbionts can spread within insect populations by increasing the fitness of their hosts when they are in the presence of natural enemies. To test this hypothesis, we adopted three distinct approaches. In the first chapter we conducted a meta-analysis to assess the costs and benefits of hosting defensive symbionts, showing that in the presence of natural enemies, symbionts provide protection by enhancing the fitness of their hosts, and that in the absence of natural enemies, symbionts cause little reduction in the fitness of their hosts. This shows that the interaction with symbionts can be highly advantageous for hosts and facilitate the spread of symbionts. In the second chapter we focused on the insect-virus association and conducted a meta-analysis to assess the level of harm that viruses can cause on their hosts. It is known that Wolbachia confers antiviral protection, however the association with Wolbachia can be advantageous to insect hosts only if the viruses that infect these insects cause a significant reduction in their fitness. We found that most host-virus interactions evolved to become parasitic, with viruses exerting a significant decrease on the fitness of hosts. Hence, harboring Wolbachia can benefit the hosts. Meanwhile, Wolbachia can benefit from the presence of viruses in the environment to facilitate their spread. In the third chapter we conducted an experiment to investigate how virus selective pressure and fly genotype (i.e., if the fly is resistant or susceptible to 10 virus infection) influence the increase of Wolbachia frequency in Drosophila melanogaster populations over time and whether the change in Wolbachia frequency increases the fitness of flies infected with virus. After ten generations, the frequency of Wolbachia in populations that were under virus selective pressure increased drastically, while in control populations - not infected with virus - there was almost no change in Wolbachia frequency. Moreover, we showed that after selection, the presence of Wolbachia in D. melanogaster populations increased their resistance to viral infection, improving their survival rates, whereas control populations showed no change in fitness. Together, our results combine multiple approaches that show evidence that protection against natural enemies can be a powerful factor responsible for the widespread success of symbionts in insects. (AU)

• FAPESP's process: 19/03997-2 - On the host-symbiont-natural enemy interaction: from parasitism to mutualism
• Grantee: Cássia de Souza Siqueira Cesar
• Support Opportunities: Scholarships in Brazil - Doctorate