Saturday, 17 November 2012

On testing the Red Queen hypothesis

[See also Part 2: On testing the Red Queen hypothesis]

Two versions of the Red Queen hypothesis
The Red Queen hypothesis comes in a general and a specific form. Van Valen (1973) found that the probability of extinction of a taxon is independent of its age. He proposed that an adaptation of one species means a loss of fitness to interacting species, no matter whether these were hosts, parasites, preators, or competitors. This is the general Red Queen hypothesis making no assumption about the mode of reproduction of the extinct taxa nor about the life-form of the taxa that drove them to extinction.

Hamilton specified pathogens and parasites with shorter variation-selection cycles than their hosts as particularly likely to exterminate the hosts. If pathogens or parasites go through the variation-selection cycle a multiple of the times that their hosts do, they should adapt more quickly to the hosts than the hosts could escape.
Here are two of Hamilton's introductions of the idea:
“A puzzle likely to occur to anyone hearing about evolution for the first time, and later very often forgotten, is that the rate of the whole process by natural selection must depend on the generation time. How, the listener then wonders, does anything manage to be as large and slow-breeding as an elephant? On the elephant’s timescale of change, why do not bacteria of skin or gut, turning over generation a hundred thousand times faster, evolve almost instantly an ability to eat the vast body up? Worse still, among plants there are the aspen clones and redwood trees ...” Hamilton (1982/2001, p. 179)
“Parasites are ubiquitous. There are almost no organisms too small to have parasites. They are usually short-lived compared with their hosts, and this gives them a great advantage in rate of evolution.” Hamilton et al. (1990/2001, p. 648)
Hamliton further differentiated between asexual and sexual hosts, that is, asexual hosts should be particularly vulnerable to such pathogens and parasites, because their offspring is genetically identical to them. He therefore thought that pathogens and parasites with short variation-selection cycles could keep sexual reproduction advantageous in the face of asexual competitors. This is the specific or parasite Red Queen hypothesis for the maintenance of sexual reproduction.

What is a Hamiltonian parasite?
By Hamiltonian I mean that the variation-selection cycle of the parasite is shorter than that of the host, because Hamilton took that as his point of departure. Previously I wondered about the problem of over-specialisation of Hamiltonian parasites (see here). But now I wonder about something else. Some research articles try to test the parasite Red Queen with host-parasitoid systems that do not qualify as Hamiltonian.

For a Hamiltonian example, trematodes have up to three hosts with snails often being the first host. Nevertheless, they go through cycles of asexual reproduction within the snails. Variation and selection among parasites can occur within the first host. Therefore a trematode and its first host is a Hamiltonian systems, even though it invlovels only part of the parasite's life-cycle.

Parasitoids, however, are small wasps that lay their eggs into the larvae of insects. The parasitoid larvae develop inside the host and kill it. Parasitoids do not go through a phase of multiplication within the host. Their variation-selection cycle is therefore as long as that of their host. The system will not be Hamiltonian in this respect.

The empirical evidence
Tobler and Schlupp (2008) reviewed the empirical evidence for and against the parasite Red Queen hypothesis, but did not ask whether the variation-selection cycle of the parasite was shorter than that of the host (Hamiltonian). I added some more recent sources to their table 2 (Tobler and Schlupp 2008, p. 768) and tried to estimate whether or not the study systems were Hamiltonian. If the situation was not clear, I simply put a questionmark in the column for the Hamiltonian status of the study system. 

The status (Hamiltonian vs. not Hamiltonian) does not map on the evidence in favour of or against the parasite Red Queen. Reference 4 in the above table, however, seems to be a correction of reference 12. That is, non-Hamiltonian systems would consitently yield negative evidence. Nevertheless, only half of the Hamiltonian systems yield evidence in favour of the Red Queen hypothesis. 

Hamiltonian and host specific parasites
Tobler and Schlupp (2008) reviewed some peculiarities of the hosts that could prevent parasites from exterminating asexual strains (e.g., hybridization, polyploidization, general immune responses). They did not look at the parasite's side of the interaction however.

The parasite might simply not be host specific. It could infests several host species -- not in different stages of a complex life-cycle but as alternative hosts in one stage. Such a parasite will be selected to be a generalist over all its alternative host species and not to specialise on genotypes within one of its host species. Dawkins's (1982, p. 65) rare-enemy effect and life/dinner principle should apply.

Depending on the availability of data on host specificity, this might be easy to test. Maybe I'll look into it, when I can spare some time (or maybe someone already did and I'm not aware).   

References (text)
References (table)
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  2. Brown SG, Kwan S, Shero S (1995) The parasite theory of sexual reproduction: parasitism in unisexual and bisexual geckos. Proc. R. Soc. Lond. B 260: 317-320.
  3. Dybdahl MF, Lively CM (1998) Host-parasite co-evolution: evidence for rare advantage and time-lagged selection in a natural population. Evolution 52: 1057-1066.
  4. Elzinga J., Chevasco V, Mappes J, Grapputo A (in press) Low parasitism rate in parthenogenetic bagworm moths do not support the parasitoid hypothesis for sex. J. Evol. Biol.
  5. Hakoyama H, Nishimura T, Matsubara N, Iguchi K (2001) Difference in parasite load and non specific immune reaction between sexual and gynogenetic forms of Crassius auratus. Biol. J. Linn. Soc. 72: 401-407.
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  12. Kumpulainen T, Grapputo A, Mappes J (2004) Parasites and sexual reproduction in psychid moths. Evolution 58: 1511-1520.
  13. Lively CM (1987) Evidence from a New Zealand snail for the maintenance of sex by parasitism. Nature 328: 519-521.
  14. Lively CM (1989) Adaptation by a parasitic trematode to local populations of its snail host. Evolution 43: 1663-1671.
  15. Lively CM, Dybdahl MF (2000) Parasite adaptation to locally common host genotypes. Nature 405: 679-681. 
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  17. Mee JA, Rowe L (2006) A comparison of parasite loads on asexual and sexual Phoxinus (Pisces: Cyprinidae). Can. J. Zool. 84: 808-816.
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