disease in domestic animals, such as vesicular stomatitis virus in cattle and avian influenza in chickens, result in significant economic and personal losses. Rabies in wild animal populations in the eastern United States has spread continually during the past half‐century. The presence of this disease poses real threats to domestic animals and, through them occasionally, to humans. An example of an agricultural infection leading to severe economic disruption is the growing spread of the cadang‐cadang viroid in coconut palms of the Philippine Islands and elsewhere in Oceania. The loss of coconut palms has led to serious financial hardship in local populations.
Examples of the evolutionary impact of the virus–host interaction
There is ample genetic evidence that the interaction between viruses and their hosts has a measurable impact on evolution of the host. Viruses provide environmental stresses to which organisms evolve responses. Also, it is possible that the ability of viruses to acquire and move genes between organisms provides a mechanism of gene transfer between lineages.
Development of the immune system, the cellular‐based antiviral interferon (IFN) response, and many of the inflammatory and other responses that multicellular organisms can mount to ward off infection is the result of successful genetic adaptation to infection. In addition, virus infection may provide an important (and as yet underappreciated) basic mechanism to affect the evolutionary process in a direct way.
There is good circumstantial evidence that the specific origin of placental mammals is the result of an ancestral species being infected with an immunosuppressive proto‐retrovirus. It is suggested that this immunosuppression permitted an immunological accommodation in the mother to the development of a genetically distinct individual in the placenta during a prolonged period of gestation!
Two current examples provide very strong evidence for the continued role of viruses in the evolution of animals and plants. Certain parasitic wasps lay their eggs in the caterpillars of other insects. As the wasp larvae develop, they devour the host, leaving the vital parts for last to ensure that the food supply stays fresh! Naturally, the host does not appreciate this attack and mounts an immune defense against the invader – especially at the earliest stages of the wasp's embryonic development. The wasps uninfected with a polydnavirus do not have a high success rate for their parasitism, and their larvae are often destroyed. The case is different when the same species of wasp is infected with a polydnavirus that is then maintained as a persistent genetic passenger in the ovaries and egg cells of the wasps. The polydnavirus inserted into the caterpillar along with the wasp egg induces a systemic, immunosuppressive infection so that the caterpillar cannot eliminate the embryonic tissue at an early stage of development! The virus maintains itself by persisting in the ovaries of the developing female wasps.
A further example of a virus's role in development of a symbiotic relationship between its host and another organism can be seen in replication of the Chlorella viruses. These viruses are found at concentrations as high as 4 × 104 infectious units/ml in freshwater throughout the United States, China, and probably elsewhere in the world. Such levels demonstrate that the virus is a very successful pathogen. Despite this success, the viruses can only infect free algae; they cannot infect the same algae when the algae exist semi‐symbiotically with a species of paramecium. Thus, the algae cells that remain within their symbiotes are protected from infection, and it is a good guess that existence of the virus is a strong selective pressure toward establishing or stabilizing the symbiotic relationship.
The origin of viruses
In the last decade or so, molecular biologists have developed a number of powerful techniques to amplify and sequence the genome of any organism or virus of interest. The correlation between sequence data; classical physiological, biochemical, and morphological analyses; and the geological record has provided one of the triumphs of modern biology. We now know that the biosphere is made up of three domains, the eubacteria (bacteria), the eukaryotes (nucleated cells), and the archaebacteria – the latter only discovered through the ribosomal RNA(rRNA) sequence studies of Woese and his colleagues in the past 30 years or so. Further, analysis of genetic changes in conserved sequences of critical proteins as well as rRNA confirms that eukaryotes are more closely related to (and thus derived from) the ancestors of archaea than they are to eubacteria.
Carefully controlled statistical analysis of the frequency and numbers of base changes in genes encoding conserved enzymes and proteins mediating essential metabolic and other cellular processes can be used to both measure the degree of relatedness between greatly divergent organisms, and provide a sense of when in the evolutionary time scale they diverged from a common ancestor. This information can be used to generate a phylogenetic tree, which graphically displays such relationships. An example of such a tree showing the degree of divergence of some index species in the three domains is shown in Figure 1.1.
Although there is no geological record of viruses (they do not form fossils in any currently useful sense), analyses of the relationship between the amino acid sequences of viral and cellular proteins and of the nucleotide sequences of the genes encoding them provide ample genetic evidence that the association between viruses and their hosts is as ancient as the origin of the hosts themselves. Some viruses (e.g., retroviruses) integrate their genetic material into the cell they infect, and if this cell happens to be germ line, the viral genome (or its relict) can be maintained essentially forever. Analysis of the sequence relationship between various retroviruses found in mammalian genomes demonstrates integration of some types before major groups of mammals diverged.
While the geological record cannot provide evidence of when or how viruses originated, genetics offers some important clues. First, the vast majority of viruses do not encode genes for ribosomal proteins or genetic evidence of relicts of such genes. Second, this same vast majority of viruses do not contain genetic evidence of ever having encoded enzymes involved in energy metabolism. This is convincing evidence that the viruses currently investigated did not evolve from free‐living organisms. This finding distinctly contrasts with two eukaryotic organelles, the mitochondrion and the chloroplast, which are known to be derived from free‐living organisms.
Figure 1.1 A phylogenetic tree of selected species from the three domains of life: Eukaryota (or Eukarya), Eubacteria, and Archaea. The tree is based upon statistical analysis of sequence variation in seven universally conserved protein sequences: arginyl‐t‐RNA synthetase, methionyl‐t‐RNA synthetase, tyrosyl‐t‐RNA synthetase, RNA pol II largest subunit, RNA pol II second largest subunit, PCNA, and 5′‐3′ exonuclease.
Source: Based upon Raoult, D., Audic, S., Robert, C., et al. (2004). The 1.2‐megabase genome sequence of mimivirus. Science306: 1344–1350.
Genetics also demonstrates that a large number of virus‐encoded enzymes and proteins have a common origin with cellular ones of similar or related function. For example, many viruses containing DNA as their genetic material have viral‐encoded DNA polymerases that are related to all other DNA polymerase isolated from plants, animals, and archaea.
Statistical analysis of the divergence in three highly conserved regions of eukaryotic DNA polymerases suggests that the viral enzymes, including those from herpesviruses and from poxviruses and relatives (including mimiviruses), have existed as long as the three domains themselves. Indeed, convincing arguments exist that the viral enzymes are more similar to the ancestral form. This, in turn, implies that viruses or virus‐like self‐replicating entities (replicons) had a major role, if not the major role, in the origin of
