Date Published: March 16, 2004
Publisher: Public Library of Science
Author(s): Jennifer J Wernegreen
Abstract: Endosymbiotic bacteria live within a host species. There are many and diverse examples of such relationships, the study of which provides important lessons for ecology and evolution.
Partial Text: Symbiosis, an interdependent relationship between two species, is an important driver of evolutionary novelty and ecological diversity. Microbial symbionts in particular have been major evolutionary catalysts throughout the 4 billion years of life on earth and have largely shaped the evolution of complex organisms. Endosymbiosis is a specific type of symbiosis in which one—typically microbial—partner lives within its host and represents the most intimate contact between interacting organisms. Mitochondria and chloroplasts, for example, result from endosymbiotic events of lasting significance that extended the range of acceptable habitats for life. The wide distribution of intracellular bacteria across diverse hosts and marine and terrestrial habitats testifies to the continued importance of endosymbiosis in evolution.
At one end of the spectrum, beneficial endosymbionts provide essential nutrients to about 10%–15% of insects and provide models for highly specialized, long-term mutualistic associations (Figure 1). These ‘primary’ endosymbionts are required for the survival and reproduction of the host, most of which feed on unbalanced diets such as plant sap, blood, or grain, and occur within specialized host cells called bacteriocytes (or mycetocytes) (Baumann et al. 2000; Moran and Baumann 2000). Molecular phylogenetic analyses demonstrate stability of these obligate mutualists over long evolutionary periods, ranging from tens to hundreds of millions of years. By allowing their hosts to exploit otherwise inadequate food sources and habitats, the acquisition of these mutualists can be viewed as a key innovation in the evolution of the host (Moran and Telang 1998). Owing to their long-term, stable transmission from generation to generation (vertical transmission), these cytoplasmic genomes have been viewed as analogs to organelles.
The distinct lifestyle of endosymbionts has clear effects on rates and patterns of molecular evolution. Compared to free-living relatives, endosymbionts are thought to have reduced effective population sizes due to population bottlenecks upon transmission to host offspring and, in the case of obligate mutualists that coevolve with their hosts, limited opportunities for gene exchange. The nearly neutral theory of evolution (Ohta 1973) predicts accelerated fixation of deleterious mutations through random genetic drift in small populations, a phenomenon that has been observed in endosymbionts (Moran 1996; Lambert and Moran 1998). Over time, this lifestyle-associated accumulation of deleterious mutations may negatively affect the fitness of both the host and symbiont.
Given their diverse evolutionary strategies, insect endosymbionts also provide a rich playing field to explore genetic conflicts (Frank 1996a, 1996b), which might involve the mode of symbiont transmission, the number of symbionts transmitted, and the sex of host offspring. Genetic conflicts described between organelle and nuclear genomes of the same organism (Hurst 1995) can provide a context to understand the evolutionary dynamics of insect–bacterial associations and the diverse outcomes of these relationships. For example, the uniparental (maternal) mode of inheritance of both mitochondria and insect endosymbionts may reflect host defense against invasion by foreign microbes with strong deleterious effects, which spread more easily under biparental inheritance (Law and Hutson 1992).
In sum, the past few years have witnessed a surge of new empirical and theoretical approaches to understand the dynamics of bacterial–insect relationships. These tools have shed light on the roles of recombination, selection, and mutation on endosymbiont genome evolution and have highlighted parameters that shape the outcome of genetic conflicts between hosts and symbionts. These data provide a foundation for studying the evolution of mutualism and parasitism and modes of transitions between them. In the near future, we can look forward to full genome sequences that span a broader ecological and phylogenetic diversity of endosymbionts and provide a richer comparative framework to test existing models and develop new ones.