The persistence of sexual reproduction in natural populations remains as one of the major unsolved problems for evolutionary biology. The problem stems from the fact that male-producing, sexual populations are subject to invasion and rapid replacement by clonal females. In fact, a population of one million sexual individuals would be replaced in less than 50 generations by a clone beginning with a single asexual female (explanation). Why, then, is there sex? A similar paradox exists for recombination. The effect of recombination is to break up the non-random associations between alleles at different loci. Why would this be favored by selection, especially if these non-random associations (linkage disequilibria) were generated by selection in the previous generations? Why break up a good thing? Over 20 hypotheses have been suggested to explain the evolutionary stability of sexual reproduction, most of which focus on the possible advantages gained by the production of variable offspring. Many of these ideas also apply to recombination. The solution seems far from certain, but most of the effort at present is focused on two general areas: the advantages of sex in clearing deleterious mutations, and the advantages of sex in variable environments. We have been engaged in both empirical and theoretical studies of these hypotheses (link to theoretical studies). Empirical studies. We work on a New Zealand snail in order to contrast the predictions of the leading theories. The snail is useful for this purpose because sexual and asexual females exist, and often coexist in the same (mixed) population (more about the snail). We have taken a strong-inference approach of forcing the different theories to make different falsifiable predictions, which can be evaluated using biogeographic and/or experimental evidence. Our work to date has been inconsistent with many of the leading hypotheses, but we have been unable to falsify the idea that coevolution with parasites provides an advantage to cross-fertilization in hosts, and vice versa (the Red Queen hypothesis). The basic idea behind the Red Queen hypothesis is that parasites will be under strong selection to infect the most common host genotypes. This kind of frequency-dependent selection will favor rare host genotypes, which should increase in frequency over time, eventually becoming common. The parasite is then under selection to infect these previously rare, but now common host genotypes. This sort of coevolutionary interaction easily leads to oscillations in genotypic frequencies in both the host and the parasite. Under the Red Queen hypothesis, sexual reproduction is selected over asexual reproduction as a mechanism to produce variable progeny, some of which may have relatively rare genotypes, which escape infection. The gist of the idea can be seen, perhaps, by asking this question: if I have a garden, and my family depends solely on the production of this garden for its survival, should I plant a monoculture of the highest yielding wheat, or should I plant a mixture of genotypes? There are clear advantages of planting the high-yield monoculture, but there is also one huge disadvantage: any disease or herbivore that can successfully infect (or attack) this genotype might potentially wipe it out. Your family suffers catastrophic consequences as a result. There is also one obvious disadvantages of the mixture; lower yield. But low sustained yield may be better in the long run. This is classic bet-hedging. Sex may be a bet-hedging strategy, if the Red Queen is correct: a lower arithmetic mean, but a higher geometric mean over time. In other words, for the family, it may be better to have consistent, but low resources, rather than extremes in boom and bust. The cost of a bust year is too high. Similarly, the cost of a clonal genotype may become too high (extinction) once the clone becomes common. The Red Queen hypothesis makes several straightforward predictions. 1. Sexual individuals should be favored where the risk of infection is high. We have found support for this expectation both within and between lakes. In general, we find more sexual females in areas where the frequency of infection by trematode worms is high (Lively 1987, 1992; Jokela & Lively 1995a,b; King & Lively 2009) [more about the parasite]. This result suggests that asexual females have displaced sexuals where the risk of infection is low. Recently we have also found that infection levels and male frequency are highly correlated over a 10-15 year period, suggesting that selection pressures exerted by parasites and levels of sexual reproduction in the hosts are stable over time (Lively & Jokela, 2002; King & Lively 2009). [more on Jokela] 2. Host genotypes should oscillate over time. Mark Dybdahl and I followed the dynamics of an all clonal population in L. Poerua, New Zealand over a six-year period. We found that changes in the frequencies of clones were correlated with later changes in the prevalence of infection in the clones, exactly as expected under the Red Queen hypothesis (Dybdahl & Lively 1998). Specifically, clones oscillated over time. When they first became common they were under-infected, but the prevalence of infection increased over time (years), until the clones were over-infected. The clones then decreased in frequency. There are, of course, alternative ways to explain these coupled changes over time, but they require odd assumptions. (Link to Mark Dybdahl's home page.) 3. There should be selection against genotypes that were common in the recent past. We conducted laboratory infection experiments to test the idea that clonal genotypes that were common in the recent past were also more susceptible to infection by local populations of parasites. In our first experiment, we found striking support for the idea: all four of the recently common clones from L. Poerua were more infected than the aggregate of rare clonal genotypes (Dybdahl & Lively 1998). We then repeated
the experiment, with a twist. We wondered if the
common clonal genotypes were more infected because
they were being tracked by the local parasites (the
Red Queen hypothesis), or whether there were more
infected because they trade-off parasite resistance
with rapid growth and reproduction (the trade-off
hypothesis). To contrast the Red Queen with the
trade-off hypothesis, we exposed snails from L. Poerua
to two sources of parasites: one from L. Poerua (the
local source), and one from another lake (L. Ianthe)
70 km to the South (the remote source). Under the Red
Queen hypothesis, the common clones should only be
more susceptible to the local source of parasites. In
contrast, under the trade-off hypothesis, the common
clones should be more susceptible to both sources of
parasites. The results were consistent with the Red
Queen, and inconsistent with the trade-off hypothesis
(Lively & Dybdahl 2000). Specifically, the four
common clones were all more susceptible than rare
clones to the local source of parasites, but no such
pattern was observed for the remote source of
parasites. The trade-off hypothesis is thus rejected
by the data. They results are, however,
consistent with expectation under the Red Queen.
More recently,
we have found direct support for the idea that
parasites help to prevent the fixation of common
clones in populations that contain mixtures of sexual
and asexual snails (Jokela et al 2009).
Specifically, we found that clones that were common in
the 1990s had become more susceptible and decreased in
frequency in 7-10 years. In other words, there
seems to be strong natural selection against common
clones in nature, which could contribute to the
persistence of sexual reproduction in mixed
populations. These basic results were backed up
by controlled laboratory experiments (Koskella &
Lively 2007, 2009) 4. Parasites should become adapted to infecting local populations of their hosts. If parasites are tracking locally common host genotypes, they should also become better (at least periodically) at infecting hosts from their local population than hosts from remote populations. We have found strong support for this idea in three different experiments, involving seven different populations (Lively 1989; Lively & Dybdahl 2000) (show me the data). Recent theoretical work has suggested that this kind of local adaptation does not require that parasites have faster generation times than their hosts (as commonly asserted), and that it can persist in the face of substantial gene flow between parasite populations (Lively 1999). In addition, we
have found (in two separate experiments) a cline in
susceptibility of snails along a depth gradient.
Specifically, snails from shallow water are more
susceptible to infection than snails from deep water
(Lively & Jokela 1995; Krist et al. 2000).
There are two possible explanations for this striking
pattern. One is that shallow-water snails are
physiologically compromised for some unknown reason,
which renders them more susceptible to infection (the
inherent susceptibility hypotheses). Another
possibility is that coevolutionary interactions are
restricted to shallow water, which makes the
shallow-water snails more tractable by the parasites
(the coevolution hypothesis). This later idea might
work as follows. The final host for these parasites
are ducks, which tend to forage along the
shallow-water margins of the lake. Thus they are more
likely to pick up infections from snails living in
shallow water than deep water; and, hence, coevolution
might be a stronger force in shallow water (see diagram).
Coevolution is required for tracking of common
genotypes. Interestingly, we find more sexual females
and higher infection levels in shallow water than deep
water (Jokela & Lively 1995a), which is consistent
with the Red Queen hypothesis for sex. We recently
found a way to directly contrast the predictions of
the "coevolution hypothesis" and the "inherent
susceptibility hypothesis". We exposed snails
collected from both shallow and deep from each of two
lakes (L. Alexandrina and L. Kanieri) to parasites
collected from both lakes. Here the parasites
were obtained by collecting the feces of the final
hosts (ducks) from around the lake. The idea
here was that the feces would contain eggs produced by
the worms from the parasites in that lake, and that
these parasites would be naturally sampled by the
final host. We reasoned that, if shallow water
snails were inherently more susceptible, then the
would be more infected by parasites, independent of
the source of the parasites. We were able to
reject this idea. In contrast, if the parasites
are coevolving with the shallow-water snails in their
local populations, they should be more infective to
the shallow-water snail, but only those collected from
the same lake. This is exactly what we found
(King et al. 2009). In fact, the parasites where
vastly more infective to sympatric (same location)
snails from the shallow water, but they were no more
infective to sympatric snails from the deep water than
they were to snails from the other (allopatric)
lake. Thus, sex and coevolution seem to be
restricted to the shallow-water margins of the lake,
where the final hosts are feeding, which is striking
evidence in favor of the Red Queen (King et al. 2009,
2011). It is also striking evidence in favor of
the geographic mosaic theory of coevolution. In summary, much of our work points to coevolutionary interactions with parasites as a mechanism selecting for sexual reproduction over parthenogenesis. There, nonetheless, remain important theoretical (link to theory) and empirical difficulties. For example, critical details regarding the genetic basis of infection have yet to be worked out. It remains to be seen whether the Red Queen will survive future attacks by the data in this and other systems. But, even if she does not survive, the knowledge of host-parasite interactions gained in the attempt will more than repay the effort.
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*This work
has been supported by grants from the US National
Science Foundation. |
C. M. Lively, Dept. of Biology,
Indiana University
Go back to Lively's homepage.
