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