Coevolution of parasites and their hosts

It may seem straightforward that parasites in a population select for the evolution of more resistant hosts, which in turn select for more infective parasites: a classic coevolutionary arms race. In fact, the process is not necessarily so straightforward, although there are certainly examples where the host and parasite drive one another's evolution. A most dramatic example involves the rabbit and the myxoma virus, which causes myxomatosis. The virus originated in the South American jungle rabbit Sylvilagus brasiliensis, where it causes a mild disease that only rarely kills the host. The South American virus, however, is usually fatal when it infects the European rabbit Oryctolagus cuniculus. In one of the greatest examples of the biological control of a pest, the myxoma virus was introduced into Australia in the 1950s to control the European rabbit, which had become a pest of grazing lands. The disease spread rapidly in 1950-51, and rabbit populations were greatly reduced - by more than 90% in some places. At the same time, the virus was introduced to England and France, and there too it resulted in huge reductions in the rabbit populations. The evolutionary changes that then occurred in Australia were followed in detail by Fenner and his associates (Fenner & Ratcliffe, 1965; Fenner, 1983) who had the brilliant research foresight to establish baseline genetic strains of both the rabbits and the virus. They used these to measure subsequent changes in the virulence of the virus and the resistance of the host as they evolved in the field.

When the disease was first introduced to Australia it killed more than 99% of infected rabbits. This 'case mortality' fell to 90% within 1 year and then declined further (Fenner & Ratcliffe, 1965). The virulence of isolates of the virus sampled from the field was graded according to the survival time and the case mortality of control rabbits. The original, highly virulent virus (1950-51) was grade I, which killed 99% of infected laboratory rabbits. Already by 1952 most of the virus isolates from the field were the less virulent grades III and IV. At the same time, the rabbit population in the field was increasing in resistance. When injected with a standard grade III strain of the virus, field samples of rabbits in 1950-51 had a case mortality of nearly 90%, which had declined to less than 30% only 8 years later (Marshall & Douglas, 1961) (Figure 12.28).

This evolution of resistance in the European rabbit is easy to understand: resistant rabbits are obviously favored by natural selection in the presence of the myxoma virus. The case of the virus, however, is subtler. The contrast between the virulence of the myxoma virus in the European rabbit and its lack of virulence in the American host with which it had coevolved, combined with the attenuation of its virulence in Australia and Europe after its introduction, fit a commonly held view that parasites evolve toward becoming benign to their hosts in order to prevent the parasite eliminating its host and thus eliminating its habitat. This view, however, is quite wrong. The parasites favored by natural selection are those with the greatest fitness (broadly, the greatest

(a) Australia

1950-51

1952-55

1955-58

1959-63

1964-66

1967-69

1970-74

1975-81

II III IV V

(b) Britain

100 0

1953

1962

1975

1976-80

II III IV V

Virulence grade

myxomatosis

Figure 12.28 (a) The percentages in which various grades of myxoma virus have been found in wild populations of rabbits in Australia at different times from 1951 to 1981. Grade I is the most virulent. (After Fenner, 1983.) (b) Similar data for wild populations of rabbits in Great Britain from 1953 to 1980. (After May & Anderson, 1983; from Fenner, 1983.)

reproductive rate). Sometimes this is achieved through a decline in virulence, but sometimes it is not. In the myxoma virus, an initial decline in virulence was indeed favored - but further declines were not.

The myxoma virus is blood-borne and is transmitted from host to host by blood-feeding insect vectors. In Australia in the first 20 years after its introduction, the main vectors were mosquitoes (especially Anopheles annulipes), which feed only on live hosts. The problem for grade I and II viruses is that they kill the host so quickly that there is only a very short time in which the mosquito can transmit them. Effective transmission may be possible at very high host densities, but as soon as densities decline, it is not. Hence, there was selection against grades I and II and in favor of less virulent grades, giving rise to longer periods of host infectiousness. At the other end of the virulence scale, however, the mosquitoes are unlikely to transmit grade V of the virus because it produces very few infective particles in the host skin that could contaminate the vectors' mouthparts. The situation was complicated in the late 1960s when an alternative vector of the disease, the rabbit flea Spilopsyllus cuniculi (the main vector in England), was introduced to Australia. There is some evidence that more virulent strains of the virus may be favored when the flea is the main vector (see discussion in Dwyer et al., 1990).

Overall, then, there has been selection in the rabbit-myxomatosis system not for decreased virulence as such, but for increased transmissibility (and hence increased fitness) -which happens in this system to be maximized at intermediate grades of virulence. Many parasites of insects rely on killing their host for effective transmission. In these, very high virulence is favored. In yet other cases, natural selection acting on parasites has clearly favored very low virulence: for example, the human herpes simplex virus may do very little tangible harm to its host but effectively gives it lifelong infectiousness. These differences reflect differences in the underlying host-parasite ecologies, but what the examples have in common is that there has been evolution toward increased parasite fitness.

In other cases, coevolution is more definitely antagonistic: increased resistance in the host and increased infectivity in the parasite. A classic example is the interaction between agricultural plants and their pathogens (Burdon, 1987), although in this case the resistant hosts are often introduced by human intervention. There may even be gene-for-gene matching, with a particular virulence allele in the pathogen selecting for a resistant allele in the host, which in turn selects for alleles other than the original allele in the pathogen, and so on. This, moreover, may give rise to polymorphism in the parasite and host, either as a result of different alleles being favored in different subpopulations, or because several alleles are simultaneously in a state of flux within their population, each being favored when they (and their matching allele in the other partner) is rare. In fact, such detailed processes have proved difficult to observe, but this has

bacteria and bacteriophages

10 20 30 40 50

10 20 30 40 50

20 30

Transfer number

Figure 12.29 (a) Over evolutionary time (1 'transfer' « 8 bacterial generations) bacterial resistance to phage increased in each of 12 bacterial replicates. 'Mean' resistance was the mean calculated over the 12 phage isolates from the respective time points. (b) Similarly, phage infectivity increased, where 'mean' infectivity was calculated over the 12 bacterial replicates. (After Buckling & Rainey, 2002.)

20 30

Transfer number

Figure 12.29 (a) Over evolutionary time (1 'transfer' « 8 bacterial generations) bacterial resistance to phage increased in each of 12 bacterial replicates. 'Mean' resistance was the mean calculated over the 12 phage isolates from the respective time points. (b) Similarly, phage infectivity increased, where 'mean' infectivity was calculated over the 12 bacterial replicates. (After Buckling & Rainey, 2002.)

been done with a system comprising the bacterium Pseudomonas fluorescens and its viral parasite, the bacteriophage (or phage) SBW25^2 (Buckling & Rainey, 2002).

Changes in both the host and parasite were monitored over evolutionary time, as 12 replicate coexisting populations of bacterium and phage were transferred from culture bottle to culture bottle. It is apparent that the bacteria became generally more resistant to the phage at the same time as the phage became generally more infective to the bacteria (Figure 12.29): each was being driven by the directional selection of an arms race. But this was only apparent because any given bacterial strain (from one of the 12 replicates) was tested against all 12 phage strains, and the phage strains were tested similarly. When, at the end of the experiment (Table 12.4), the resistance of each bacterial strain was tested against each phage strain in turn, it was clear that the bacteria were almost always most resistant (and often wholly resistant) to the phage strain with which they coevolved. There was therefore extensive evolutionary divergence amongst the strains - or subpopulations - and extensive polymorphism within the metapopulation as a whole.

Thus we close this chapter, appropriately, with another reminder that despite being relatively neglected by ecologists in the past, parasites are increasingly being recognized as major players in both the ecological and the evolutionary dynamics of their hosts.

Table 12.4 For each of 12 bacterial replicates (B1-B12) and their 12 respective phage replicates (^1-^12), entries in the table are the proportion of bacteria resistant to the phage at the end of a period of coevolution (50 transfers « 400 bacterial generations). Coevolving pairs are shown along the diagonal in bold. Note that bacterial strains are usually most resistant to the phage strain with which they coevolved. (After Buckling & Rainey, 2002.)

Bacterial replicates

Table 12.4 For each of 12 bacterial replicates (B1-B12) and their 12 respective phage replicates (^1-^12), entries in the table are the proportion of bacteria resistant to the phage at the end of a period of coevolution (50 transfers « 400 bacterial generations). Coevolving pairs are shown along the diagonal in bold. Note that bacterial strains are usually most resistant to the phage strain with which they coevolved. (After Buckling & Rainey, 2002.)

Bacterial replicates

Phage replicates

B1

B2

B3

B4

B5

B6

B7

B8

B9

B10

B11

B12

f1

0.8

0.9

1

1

1

1

1

1

0.85

0.85

0.75

0.65

f 2

0.1

1

0.3

1

0.85

0.25

1

1

0.85

0.9

0.8

0.65

f 3

0.75

0.75

1

1

1

0.9

1

1

0.85

0.9

0.9

0.65

f4

0.15

0.9

0.8

1

0.85

0.6

0.6

1

0.85

1

0.85

0.35

f 5

0.25

0.9

1

1

1

0.9

1

0.8

0.85

1

0.8

0.65

f 6

0.2

1

0.85

0.8

0.75

0.8

0.85

0.9

0.85

0.75

0.45

0.25

f7

0.2

0.75

0.6

1

0.4

0.45

1

0.9

0.85

1

0.75

0.35

f 8

0

0.95

0.55

0.95

0.35

0.25

0.8

1

0.85

1

0.7

0.25

f9

0

0.7

0.55

0.45

0.7

0.35

1

1

0.85

1

0.5

0.1

f10

0

0.7

0.9

0.7

0.55

0.9

1

1

0.7

1

0.5

0.4

f11

0

0.5

0.9

0.75

0.7

1

1

0.95

0.75

1

1

0.35

f 12

0

0.15

0

0.1

0.65

0.35

1

1

0.7

0.8

0.85

0.4

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