The pleiotropic cost of host specialization in Tobacco etch potyvirus

Infection, Genetics, and Evolution 8 (2008) 806-814
Patricia Agudelo-Romero, Francisca de la Iglesia, Santiago F. Elena

I've been getting interested in the way host specialization shapes the evolution of pathogens, so I picked up this fairly recent article that discusses the pleiotropic costs of host specialization in the plant virus, Tobacco etch potyvirus (TEV). Specifically I want to gain better insight into the way virulence factor gene family expansions/contractions have contributed to host range expansion/contraction, and what the factors are that influence these dynamics.

For parasites, host organisms are the environment and supply most of the selection pressure for parasite evolution. When the number of possible host species becomes reduced (i.e. when specialization occurs), parasites are put at a selective disadvantage to generalist parasites that have access to wider access to resources. Host heterogeneity has been shown to drive parasite diversity, while host homogeneity usually results in specialization and enhancing local adaptation. This all makes sense, however generalist parasites are the exception, not the rule, implying there are unseen advantages to host specialization. One common theory is that the genetic load of generalist lifestyles is too costly to compete with specialists, citing the well-known aphorism that "a jack-of-all-trades is a master of none." One mechanism driving this trend toward specialism could be rooted in antagonistic pleiotropy, which is essentially when one gene that is involved in two traits is selected for in opposite directions. For a more visual example, this might occur when one gene is selected for enhanced eyesight but at the cost of coat camouflage. This type of antagonistic pleiotropy could limit range expansion and lead to specialization. Here this investigators looked for evidence of this by experimentally evolving a virus on a non-optimal host (pepper - Caspicum annuum), and then looking for virulence depression when the new virus strain was returned to its original host (tobacco - Nicotiana tabacum var Xanthi).

TEV causes stunting, mottling, necrotic etching and malformations in leaves. It has a fairly wide host range (149 species, 19 families), although it occurs most often in the family Solanaceae. The study compared markers of infection (height & weight, as seen above) between the two Solanaceae species post TEV infection, and were able to show a significant increase in virulence as TEV evolved on the new host (pepper), while evolution on the ancestral host did not show much of a virulence increase in the tobacco or the pepper. Furthermore, they also showed that there exists a significant negative correlation between virulence in evolution on the evolution host and the alternative one. In other words, as the TEV lineages evolved to become more pathogenic to the pepper, they also became less pathogenic to tobacco, indicating a trade-off. They were also able to show that changes in the NIa and NIb genes in the parasite genome were likely associated with this trade-off. Furthermore, three of the four replicate lines of pepper-evolved TEV had the same mutation, indicating evolutionary convergence.

This study is particular interest to my thesis because it address some of the genetic factors that drive host range expansion and specialization. Since many of the fungal species I am interested in are opportunistic pathogens, they would use the same suites of enzymes for decomposition as they would for pathogenicity. Antagonistic pleiotropy could be playing a large role in the evolution of the regulatory genes that I realized.