A not so modest proposal for pathogens: evolutionary diversification

Due to a ground swell of interest, we recently read Robert Ricklefs inaugural article (Ricklefs 2010) in to the National Academy of Sciences (of the United States of America) in which he proposes a new mechanistic role for parasites and pathogens to generate diversity within the tree of life. In this paper, Ricklefs (2010) distinguishes between two compartments of the ecological niche of a species: 1) the individual niche space and 2) the population niche space. He contrasts these two concepts of niche space by indicating which processes are most involved in defining the boundaries: 1) evolution and adaptation of an individual versus 2) demographic properties of a population in a point in space. Being a fan of processes not patterns, I thought that these definitions were particularly helpful when reading the rest of the article and understanding his proposed novel mechanism of diversification at the end.

Ricklefs asks how different clades occupy population niche space: do more taxon rich clades occupy larger niche space or simply pack the available space more tightly with narrower species niches or larger overlap between species? Among several lines of evidence, the most crucial to his proposal is that there is independence of the diversity of a clade and the total population niche space occupied. That is, larger clades must pack niche space more tightly. But apparently they are doing it not by lowering the species densities because species abundance does not decrease with increasing local diversity. What Ricklefs suggests is it that the tighter packing is achieved via uneven filling of particular population niche space. This uneven filling is due to interactions with pathogens and parasites. The outcome of these interactions being determined by spatially and temporally varying antagonistic interactions that may also vary not just in the composition of those interactions but the diversity of the players involved (conjuring the idea of geographic mosaic of coevolution [Thompson 2005]).

How is this proposal different from adaptive radiations or escape and radiate coevolution? The paper makes the first contrast from adaptive radiations by presenting his mechanism in context of seemingly saturated niches rather than a having diversification happen in a wide open landscape. What about escape and radiate coevolution (Ehrlich and Raven 1964) which also has a role for interacting species in diversification? Again, this is a case were new adaptive zones (Simpson 1953) are opened up and allow species to occupy these new empty niches. Ricklefs' idea is fundamentally different in that pathogen interactions are seen as a mechanism that reduces efficient packing and saturation of population niches. This is achieved by affecting the population demographics which can result in a feedback to evolutionary dynamics at the individual niche level. This last part highlights the importance of linking demographic and evolutionary factors into models of coevolutionary interactions when concerned with patterns of diversification. Others have already pointed out this need in models exploring other evolutionary important traits (Mideo et al 2008)

While I was expecting something different at the conclusion of this article, what Ricklefs does do is lay out a program of study and call for data to defend his proposal. This request does not only extend to the field parasitologist but also to theoreticians as well.

References

Ehrlich, P. R., and P. H. Raven. 1964. Butterflies and plants: a study in coevolution. Evolution 18:586-608.

Mideo, N., S. Alizon, and T. Day. 2008. Linking within- and between-host dynamics in the evolutionary epidemiology of infectious diseases. Trends in Ecology & Evolution 23:511-517.

Ricklefs, R. E. 2010. Evolutionary diversification, coevolution between populations and their antagonists, and the filling of niche space. Proceedings of the National Academy of Sciences of the United States of America 107:1265-1272.

Simpson, G. G. 1953. The major features of evolution. Columbia University Press, New York.

Thompson, J. N. 2005. The Geographic Mosaic of Coevolution. University of Chicago Press, Chicago.

Paper Read

Ricklefs, R. (2010). Inaugural Article: Evolutionary diversification, coevolution between populations and their antagonists, and the filling of niche space Proceedings of the National Academy of Sciences, 107 (4), 1265-1272 DOI: 10.1073/pnas.0913626107

Selection Mosaics or environmental interactions

Vale and Little (2009) published recent work on parasite infection variation across a temperature gradient. Specific parasite infections are often the result of genetic interactions of both the host and parasite, sometimes referred to as genotype by genotype interactions (GxG). The authors of this paper used an ideal interaction between Daphnia magna and a bacterial parasite, Pasteuria ramose. The experiment was such that they could test multiple levels on interactions. They isolated multiple host clonal lines (n = 4) as well as parasite lines (n = 4) and compared infection rates as well as parasite growth rates across three different temperatures. The paper details the experiment very well, so I'll spare details here, but a good model for future studies.

The authors found significant GxG interactions for most of the traits measured in the infection process, including both early (probability of infection) and later (parasite growth rate). However differences in genotype by environment (GxE) interactions showed up for different places in the infection timeline. The probability of infection showed a host genotype by temperature interaction, but this was a weak affect and the authors make the important point that the relative rank order wasn't changed. The reason this is key is that it is often emphasized that GxE interactions are a mechanism of the maintenance of different genotypes. If each genotype has high fitness in only some environments, and the environment varies, then there can be some period of time where polymorphism is maintained. In terms of interactions of the parasite genotype and the environment, there were initially some interactions with transmission potential and growth rate, however rank differences were again absent. The paper makes one further step and examines the combined transmission potential (spore production and infectivity). This isn't quite a measure of R₀ because of complications with the effect of dose on infection rate and the interaction between parasite genotype and temperature disappears.

The study failed to find evidence of a GxGxE interaction, but the authors were correct to point out, that this is only the case for the environmental variable measured (temperature). Given that temperature is an important component of the environment for this interaction, I was surprised by this result. Perhaps, it would have been different if the difference were not just in constant temperature, but in some sort of variable environment. In the very last paragraph, Vale and Little (2009) emphasize that the lack of GxGxE interactions mean that the specificity of the interactions are robust to environmental noise. However, it is just such noise that others have proposed as important in maintaining variation. These interactions are the selection mosaics in the Geographic Mosaic Theory of Coevolution (Thompson 1999, 2005).

References

Thompson, J. N. 1999. Specific hypotheses on the geographic mosaic of coevolution. American Naturalist 153:S1-S14.

Thompson, J. N. 2005.
The Geographic Mosaic of Coevolution. University of Chicago Press, Chicago.

Vale, P. F., and T. J. Little. 2009. Measuring parasite fitness under genetic and thermal variation. Heredity online early.

Paper read

Vale, P., & Little, T. (2009). Measuring parasite fitness under genetic and thermal variation Heredity DOI: 10.1038/hdy.2009.54

Selection mosaics and the GMTC

This past week in Coevolvers, we dropped back into the empirical world and ready a paper from Piculell et al (2008) on evidence of selection mosaics. Selection mosaics describe a case where the fitness function of the interacting players varies across space (Gomulkiewicz et al 2007; Thompson 1999, 2005), sometimes described as GxGxE interactions (G: genetic; E: environment). What does this mean more generally? Simply put, the fitness of a plant may change from one population to the next because the nature of the interaction with a mutualist is affected by the environment. This can occur even if the genotypes that make up those populations are exactly the same.

The experimental design was certainly setting up the case for a maximum chance of detection of interaction effects. With only levels of each factor, (e.g. two genotypes of the host) the authors had less power to detect any main effects, but that clearly wasn't the objective. They wanted to find evidence of significant GxGxE. Essentially this experiment had 4 environmental treatments, so they maximized the chance of an interaction. The authors of this paper were very upfront that they were not intending to measure a selection mosaic in the natural setting. Their objective was to demonstrate the possibility and they certainly obtained that goal. With that limitation in mind, how general are these results? Measuring the potential for a selection mosaic is one thing, but for this to really have an impact in generating or maintaining diversity as imagined in the Geographic Mosaic Theory of Coevolution (Thompson 1999, 2005) then it must hold for a broad sample of the populations under investigation. The authors are on a good track though to discovering more about this system. Perhaps they plan on taking the methodology outlined in Nuismer and Gandon (2008) on reciprocal-transplant designs. Picking a larger sample of the genetic variation found in nature for at least one of the players would extend their results from the possible into the probable.

References

Gomulkiewicz, R., D. M. Drown, M. F. Dybdahl, W. Godsoe, S. L. Nuismer, K. M. Pepin, B. J. Ridenhour, C. I. Smith, and J. B. Yoder. 2007. Dos and don'ts of testing the geographic mosaic theory of coevolution. Heredity 98:249-258.

Nuismer, S. L., and S. Gandon. 2008. Moving beyond Common-Garden and Transplant Designs: Insight into the Causes of Local Adaptation in Species Interactions. American Naturalist 171:658-668.

Piculell, B., J. Hoeksema, and J. Thompson. 2008. Interactions of biotic and abiotic environmental factors in an ectomycorrhizal symbiosis, and the potential for selection mosaics. Bmc Biol 6:23.

Thompson, J. N. 1999. Specific hypotheses on the geographic mosaic of coevolution. American Naturalist 153:S1-S14.

Thompson, J. N. 2005.
The Geographic Mosaic of Coevolution. University of Chicago Press, Chicago.

Paper Read

Piculell, B., Hoeksema, J., & Thompson, J. (2008). Interactions of biotic and abiotic environmental factors on an ectomycorrhizal symbiosis, and the potential for selection mosaics BMC Biology, 6 (1) DOI: 10.1186/1741-7007-6-23