Multidimensional coevolution, no oscillation overthruster required

Conventional wisdom suggests that pathogens and parasites are more rapidly evolving because of various reasons such as short generation time or stronger selection. Yet somehow, they have not completely won the battle against the host. Recently, a theoretical paper on coevolution in Nature caught my eye (Gilman et al., 2012). Here the authors address this paradox: “How do victim species survive and even thrive in the face of a continuous onslaught of more rapidly evolving enemies?”

Instead of treating a coevolutionary interaction between two species as the interaction of only two traits, the authors investigate the nature of an interaction among a suite of traits in each species. It’s not hard to think of a host having a fortress of defenses against attack from a parasite with an arsenal loaded with many weapons.

Bacterial Thunderdome: Decoding virulence, spiteful interactions, and diversity

What happens when two parasites infect the same host individual? Is the outcome similar to the Thunderdome: two parasites enter, one parasite leaves? Host-parasite interactions are rarely so simple. While a reductionist approach to understanding the interaction of a parasite or pathogen with its host may decompose the system to a single infection, nature is full of much more complex puzzles. Within the host, the battle itself raging between parasites (within-host competition) may have cascading effects on the host.

A recent paper on virulence caught my eye (Bashey et al., 2012) which provides an update to a very interesting result from the group a few years ago. The system includes bacterial parasites, along with parasitic nematodes, that infect insect larvae and eat/digest them from the inside out. Vigneux et al. (2008) found that when multiple parasite isolates are mixed in a host, the host mortality decreased. However, this only occurred when the isolates were not related. In the experiment, the researchers created low relatedness by mixing populations with migration. I reviewed the 2008 paper previously. The hypothesis was that chemical warfare among the parasites decreased the parasite load and reduced the negative effects on the host, virulence.

The bacteria produce chemical weapons, bateriocins, which can broadly harm other isolates, but relatives are left unharmed. These chemical weapons can be classified as spiteful: in the process of harming others they also harm the focal individual. This self-harm comes from the cost of making the chemical weapon. Others have labeled this antagonistic trait a greenbeard gene.

Greenbeards are genes that can identify the presence of copies of themselves in other individuals, and cause their bearer to behave nepotistically toward those individuals (Gardner and West, 2010).

Gardner and West explain that the origin of this term comes from Richard Dawkins illustrative example where individuals bearing this trait had green beards.

Experimental results: Recently, natural system specific isolates of the parasite have been cultured in the lab allowing more specific tests of the within-host competition (Hawlena et al., 2010a; Hawlena et al., 2010b). In the most recent paper, Bashey et al. (2012) found that the bacterial isolates that produce the toxin have a higher growth rate in coinfections (where within-host competition might be important). However, in the absence of coninfections, there was no relative growth rate advantage of the toxin producing, inhibitory, isolates. In coninfections, even though the toxin producing isolate was winning the internal host battle, lower host mortality rate emerged as an outcome.

A beautiful world: As an evolutionary biologist, I’m interested not only in the diversity of the natural world, but also the mechanisms that keep that diversity around. We often think of natural selection as favoring the fittest. If a single type is better than the rest, then over time, diversity will decrease. Often the analogy of hill climbing is used. On the other hand, if the fittest depends on the context of the other players involved, than diversity might be maintained. That is, what if the shape of the mountain range is constantly changing. In relation to this research,

bacteriocins might promote local diversity when producer, sensitive, and resistant strains are engaged in a version of the rock‐paper‐scissors game (i.e., the producer can kill the sensitive strain, the resistant strain outcompetes the producer, and the sensitive strain outcompetes the resistant strain) in a spatially structured environment (Hawlena et al., 2010b).

If bacteriocins are costly to produce, than they must provide some benefit in some contexts. Bashey et al (2012) suggest that this mechanism, where the fitness of a particular parasite isolate is context dependent, may explain the high frequency of bacteriocin production found in the natural populations surveyed in their earlier work (Hawlena et al., 2010a).

Stay tuned for future research by Dr. Farrar Bashey as she assures me more pieces to this puzzle will be revealed.

References

• Bashey F, Young SK, Hawlena H, Lively CM (2012) Spiteful Interactions between Sympatric Natural Isolates of Xenorhabdus Bovienii Benefit Kin and Reduce Virulence. Journal of Evolutionary Biology 25: 431-437. DOI: 10.1111/j.1420-9101.2011.02441.x
• Gardner A, West SA (2010) Greenbeards. Evolution 64: 25-38. DOI: 10.1111/j.1558-5646.2009.00842.x
• Hawlena H, Bashey F, Lively CM (2010a) The Evolution of Spite: Population Structure and Bacteriocin-Mediate Antagonism in Two Natural Populations of Xenorhabdus Bacteria. Evolution 64: 3198-3204. DOI: 10.1111/j.1558-5646.2010.01070.x
• Hawlena H, Bashey F, Mendes Soares H, Lively CM (2010b) Spiteful Interactions in a Natural Population of the Bacterium Xenorhabdus Bovienii. The American Naturalist 175: 374-381. DOI: 10.1086/650375
• Vigneux F, Bashey F, Sicard M, Lively CM (2008) Low Migration Decreases Interference Competition among Parasites and Increases Virulence. Journal of Evolutionary Biology 21: 1245-1251. DOI: 10.1111/j.1420-9101.2008.01576.x

Main Paper
BASHEY, F., YOUNG, S., HAWLENA, H., & LIVELY, C. (2012). Spiteful interactions between sympatric natural isolates of Xenorhabdus bovienii benefit kin and reduce virulence Journal of Evolutionary Biology, 25 (3), 431-437 DOI: 10.1111/j.1420-9101.2011.02441.x

Double, double toil and trouble: a tale of two infections

What are the evolutionary consequences of parasite superinfection (i.e. simultaneous infection by multiple parasites)? When parasites are genetically distinct, coexistence within a host generates conflict because of limited resources. How this conflict is resolved is the source of evolutionary research on the evolution of parasite life history traits such as virulence, the negative effects on the host caused by infection, and transmission mode, how parasites infect a new host. The transmission mode of a parasite is often characterized as occurring in one of two different modes: vertical or horizontal. With vertical transmission, an offspring obtains its parasites directly from its parents. In contrast, with horizontal transmission, infections occur either directly from the environment or contagiously by infection from other individuals.

My interest in the evolution of transmission mode in parasites and symbionts led me to a recent paper (Ben-Ami et al. 2011), which addresses the consequences of superinfection by two different parasites with different transmission modes of the waterflea, Daphnia magna, on virulence and parasite fecundity. Pasteuria ramosa is a castrating, horizontally transmitted, blood-infecting bacterium where spores are produced from the cadaver of the host Daphnia. Octosporea bayeri, a microsporidium, utilizes both vertical transmission to eggs and horizontal transmission via waterborne spores.

Photo by Paul Herbert in Gewin (2005)

Conflict resolution: The difference in the transmission strategies among the parasites generates an extreme conflict. O. bayeri needs the host to produce offspring for vertical transmission, that is the host and parasite have an aligned interest in producing offspring. On the other hand, P. ramosa is using host resources, including the reproductive tissues, to produce spores for infecting other hosts. Because of the alignment of interests between host and the vertically transmitting parasite, the question becomes: does infection by O. bayeri provide host protection from future infection by P. ramosa? In contrast, virulent parasites are expected to be more competitive by exploiting host resources more quickly than less virulent parasites. Here, P. ramosa may reduce infection by O. bayeri by competitive exclusion but at the cost of additionally reducing host survival.

To test these hypotheses, Ben-Ami et al. (2011) used two different infection experiments. The first tested the impact of horizontally occurring superinfection on host and parasite life history. These infections occurred simultaneously or sequentially (separated by 7 days). The second experiment used vertically infected hosts with O. bayeri parasites which were then exposed to P. ramosa for secondary infection. P. ramosa competitively excluded O. bayeri in double infections. Additionally, host fecundity was lower with super infections than with P. ramosa infection alone indicating an increase in virulence due to the interaction. The authors also found that vertical infection by O. bayeri provided no significant protection from future horizontal infection by P. ramosa. In fact, they found that P. ramosa was able to clear O. bayeri vertical infections and was clearly the superior competitor.

The part of the paper that I found most interesting was how the authors related their results to previous theoretical predictions. Many authors have addressed the interaction of parasites with different transmission modes (Altizer and Augustine 1997; Faeth et al. 2007; Haine et al. 2005; Jones et al. 2007, 2010; Lipsitch et al. 1996; Lively et al. 2005). Most of these previous models make assumptions about the lack of superinfection, suggesting one infection protects against a second. The authors of this paper point out that no one has specifically modeled the combination of a vertically transmitted parasite with one that can use both strategies and allows for superinfection.

In summary, I found that this paper and the results contained are clearly presented. While the authors did not find the support for the protective hypothesis, they did find evidence of increased virulence with coinfections as predicted. The authors do point out that these two parasites have a very narrow range of coexistence, in southwestern Finland, and suggest that coexistence may be a difficult or transient dynamic for this system. I would agree.

Interested in more? In addition to this interesting paper, Dieter Ebert’s group has recently published exciting research on the specificity and mechanism of infection by one of the parasites discussed the above paper, P. ramosa.: (Luickx et al. 2011; Duneau et al. 2011).

References

• Altizer SM, Augustine DJ (1997) Interactions between frequency-dependent and vertical transmission in host-parasite systems. Proceedings of the Royal Society of London Series B-Biological Sciences 264: 807-814. http://dx.doi.org/10.1098/rspb.1997.0113
• Ben-Ami F, Rigaud T, Ebert D (2011) The expression of virulence during double infections by different parasites with conflicting host exploitation and transmission strategies. Journal of Evolutionary Biology 24: 1307-1316. http://dx.doi.org/10.1111/j.1420-9101.2011.02264.x
• Duneau, D, Luijckx P, Ben-Ami F, Laforsch C, Ebert D (2011) Resolving the infection process reveals striking differences in the contribution of environment, genetics and phylogeny to host-parasite interactions. BMC Biology, 9:11. http://dx.doi.org/10.1186/1741-7007-9-11
• Faeth SH, Hadeler KP, Thieme HR (2007) An apparent paradox of horizontal and vertical disease transmission. Journal of Biological Dynamics 1: 45-62. http://dx.doi.org/10.1080/17513750601040367
• Haine ER, Boucansaud K, Rigaud T (2005) Conflict between parasites with different transmission strategies infecting an amphipod host. Proceedings of the Royal Society B-Biological Sciences 272: 2505-2510. http://dx.doi.org/10.1098/rspb.2005.3244
• Jones EO, White A, Boots M (2007) Interference and the persistence of vertically transmitted parasites. Journal of Theoretical Biology 246: 10-17. http://dx.doi.org/10.1016/j.jtbi.2006.12.007
• Jones EO, White A, Boots M (2010) The evolutionary implications of conflict between parasites with different transmission modes. Evolution 64: 2408-2416. http://dx.doi.org/10.1111/j.1558-5646.2010.00992.x
• Lipsitch M, Siller S, Nowak MA (1996) The evolution of virulence in pathogens with vertical and horizontal transmission. Evolution 50: 1729-1741. http://dx.doi.org/10.2307/2410731
• Lively CM, Clay K, Wade MJ, Fuqua C (2005) Competitive co-existence of vertically and horizontally transmitted parasites. Evolutionary Ecology Research 7: 1183-1190. http://www.evolutionary-ecology.com/issues/v07n08/iiar1894.pdf
• Luijckx P, Ben-Ami F, Mouton L, Pasquier L, Ebert D (2011) Cloning of the unculturable parasite Pasteuria ramosa and its Daphnia host reveals extreme genotype-genotype interactions. Ecology Letters 14:125-131. http://dx.doi.org/10.1111/j.1461-0248.2010.01561.x

Paper read

BEN-AMI, F., RIGAUD, T., & EBERT, D. (2011). The expression of virulence during double infections by different parasites with conflicting host exploitation and transmission strategies Journal of Evolutionary Biology, 24 (6), 1307-1316 DOI: 10.1111/j.1420-9101.2011.02264.x

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