The Geography of Coevolution: Comparative Population ...jtaylor/teaching/Fall2011/APM541/papers/... · Evolution, 50(6), 1996, pp. 2264-2275 THE GEOGRAPHY OF COEVOLUTION: COMPARATIVE

The Geography of Coevolution: Comparative Population Structures for a Snail and ItsTrematode ParasiteAuthor(s): Mark F. Dybdahl and Curtis M. LivelySource: Evolution, Vol. 50, No. 6 (Dec., 1996), pp. 2264-2275Published by: Society for the Study of EvolutionStable URL: http://www.jstor.org/stable/2410696 .Accessed: 15/08/2011 22:16

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Evolution, 50(6), 1996, pp. 2264-2275

THE GEOGRAPHY OF COEVOLUTION: COMPARATIVE POPULATION STRUCTURES FOR A SNAIL AND ITS TREMATODE PARASITE

MARK F DYBDAHL1 AND CURTIS M. LIVELY Department of Biology, Indiana University, Bloomington, Indiana 47405

'E-mail: mdybdahl@ ucs. indiana. edu

Abstract.-Gene flow and the genetic structure of host and parasite populations are critical to the coevolutionary process, including the conditions under which antagonistic coevolution favors sexual reproduction. Here we compare the genetic structures of different populations of a freshwater New Zealand snail (Potamopyrgus antipodarum) with its trematode parasite (Microphallus sp.) using allozyme frequency data. Allozyme variation among snail populations was found to be highly structured among lakes; but for the parasite there was little allozyme structure among lake populations, suggesting much higher levels of parasite gene flow. The overall pattern of variation was confirmed with principal component analysis, which also showed that the organization of genetic differentiation for the snail (but not the parasite) was strongly related to the geographic arrangement of lakes. Some snail populations from different sides of the Alps near mountain passes were more similar to each other than to other snail populations on the same side of the Alps. Furthermore, genetic distances among parasite populations were correlated with the genetic distances among host populations, and genetic distances among both host and parasite populations were correlated with "stepping-stone" distances among lakes. Hence, the host snail and its trematode parasite seem to be dispersing to adjacent lakes in a stepping-stone fashion, although parasite dispersal among lakes is clearly greater. High parasite gene flow should help to continuously reintroduce genetic diversity within local populations where strong selection might otherwise isolate "host races." Parasite gene flow can thereby facilitate the coevolutionary (Red Queen) dynamics that confer an advantage to sexual reproduction by restoring lost genetic variation.

Key words.-Coevolution, gene flow, parasites, population structure, Red Queen hypothesis, sexual reproduction.

Received August 23, 1995. Accepted July 3, 1996.

The subdivision of populations, the spatial pattern of selection, and gene flow can all influence the coevolutionary process (Thompson 1994). Consequently, parasite-host coevolution depends on genetic variation and its structure in both interacting species. For example, restricted gene flow among parasite populations should enhance the potential for parasites to track the most common host genotypes in local populations, and may lead to host-race formation (Price 1980). In fact, Price (1980) predicted that parasite populations should become highly structured with little gene flow between populations or host races. High parasite gene flow will tend to counteract local adaptation (Slatkin 1987), and expose parasites to a mosaic of selection (Thompson 1994). Relatively high levels of parasite gene flow, however, could also spread adaptive traits (Thompson 1994), and restore variation that is lost by recurrent extinction of local populations in a metapopulation (Frank 1991, 1993).

The restoration of genetic variation to local populations of parasites may be especially important when selection leads to time-lagged oscillatory or chaotic cycles in allele frequencies (see Jayakar 1970; Clarke 1976; Hutson and Law 1981; Bell 1982; May and Anderson 1983). Parasite alleles engaged in frequency-dependent interactions with host alleles can easily "overshoot" and become fixed in local populations due to the time lags. Such fixation is most likely when selection on the parasite is strong (Seger 1988, Seger and Ham- ilton 1988), and when parasite fitness depends on host density as well as the frequency of host genotypes (May and An- derson 1983). Small amounts of migration have been shown to be very effective in maintaining genetic diversity in local parasite populations (Hamilton 1986, 1993; Frank 1991, 1993), provided the different parasite populations are adapted to different sets of host alleles (i.e., the different populations are oscillating out of phase; Frank 1991).

Frequency-dependent and time-lagged dynamic coevolution is central to recent ideas on the role of parasites in selecting for the production of outcrossed sexual versus par- thenogenetic offspring in their hosts (The "Red Queen hypothesis," Jaenike 1978; Bremermann 1980; Hamilton 1980; Bell 1982). Hence, the genetic structure of parasite-host populations may have important consequences for the evolutionary maintenance of sexual reproduction. New variation in the form of mutation or migration is often included in computer simulations of Red Queen models to "fuel" the coevolutionary process (e.g., Hamilton et al. 1990; Ladle et al. 1993; Howard and Lively 1994; Judson 1995). In addition, the relative migration of hosts and parasites can affect the successful spread of host clones in a metapopulation, and the outcome of competition between sexual and clonal strategies. Ladle et al. (1993) showed that parthenogenesis will replace sexual reproduction if parasite dispersal is low relative to host dispersal, but that sexual reproduction is favored under the reverse situation. They show, for example, that if hosts outdisperse their parasites, then a clonal host genotype can escape infection, and displace sexual populations patch by patch across the metapopulation.

In spite of the importance of comparing the relative structures of host and parasite populations, there have been few studies that attempt to map parasite genetic structure onto host genetic structure (review in Nadler 1995). Mulvey et al. (1991) found significant spatial variation for both deer (hosts) and parasitic flukes. However, the between-population genetic distances for the host and parasite were not concordant with each other or with geographic distances among populations (perhaps due to the wide-ranging movements of the deer). Here we compare the population genetic structures of a freshwater snail (Potamopyrgus antipodarum) and its trem-

2264

(C 1996 The Society for the Study of Evolution. All rights reserved.

HOST-PARASITE POPULATION STRUCTURE 2265

atode parasite (Microphallus sp.) using data from allozyme electrophoresis. This specific host-parasite combination is of particular interest because prevalence of infection is correlated with the frequency of sexual individuals among populations (consistent with the Red Queen hypothesis; Lively 1987, 1992; Jokela and Lively 1995), and because reciprocal cross-infection experiments have shown that the parasite is adapted to its local host populations (Lively 1989). Here we show that this local adaptation is maintained in the face of considerable gene flow by the parasite. We also show that, although parasites migrate more and are less structured than their hosts, the genetic distances in both species are correlated with each other, and with geographic distances among populations.

MATERIALS AND METHODS

Natural History of the Host and Parasite.-The freshwater snail P. antipodarum is a small (< 8 mm) prosobranch gas- tropod, which is common in lakes throughout New Zealand at elevations less than 750 m (Winterbourn 1970). This snail is dioecious. Females may be either sexual and diploid, or apomictic parthenogens (Phillips and Lambert 1987; Dybdahl and Lively 1995a) and triploid (Wallace 1992). Generation time is typically about four months in the lab (unpubl. obs.). This snail is the first intermediate host to at least a dozen species of digenetic trematodes, which castrate both sexes of infected individuals (Winterbourn 1974; MacArthur and Featherston 1976). An undescribed species of the digenetic trematode Microphallus is responsible for most trematode infections in lake populations of Potamopyrgus (Lively 1987). Microphallus sp. has a generation time in the snail of approximately three to four months under laboratory conditions (unpubl. obs.), at which time parasited snails become filled with large numbers of encysted metacercariae. Micro- phallus sp. may then be transmitted when infected snails are ingested by their final hosts, which include a variety of wa- terfowl and wading birds (Lively and McKenzie 1991).

Collection and Electrophoresis.-We collected snails in 1993 from 20 sites spread over eight lakes on the south island of New Zealand (Fig. 1). To examine the differentiation of sites within lakes, we collected from three or four sites from four lakes (Alexandrina, Mapourika, Wahapo, and Paringa). Parasites are known to be adapted to the local host populations in these four lakes (Lively 1989). We also collected from single sites from two lakes (Hawdon and Poerua), and two sites from two other lakes (lanthe and McGregor). Three of these lakes (Alexandrina, McGregor, and Hawdon) are located on the east side of the Southern Alps, and the other five are located on the west side. All lakes contain populations of both sexual and asexual females except McGregor and Poerua, which contain all-female, asexual populations. Col- lections were made from rocks and vegetation along the shoreline.

Live snails were transported to the laboratory, where we obtained two separate samples from each of the 20 sites: a sample of snails and a sample of Microphallus parasite tissue from infected snails. The sample of snails was composed of the first 70 individuals obtained haphazardly from the collections. These snails were placed in groups of 10 in 1.5-mL

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2266 M. F. DYBDAHL AND C. M. LIVELY

(6-phosphogluconate dehydrogenase, 1.1.1.44), Mpi (man- nose-phosphate isomerase, 5.3.1.8), and Aat (aspartate ami- notransferase, 2.6.11).

The parasite samples were ground with 18 FiL of crushing buffer in preparation for electrophoresis. Six presumptive loci were reliably resolved in the parasite and revealed variation within and among localities: Pgm, Idh, Me (malic enzyme, 1.1.1.40), Gpi (glucose-phosphate isomerase, 5.3.1.9), Mdh (malate dehydrogenase, 1.1.1.37), and Ldh (lactate dehydrogenase, 1.1.1.27). Running and soaking buffers were Tris- Maleate (Mdh, Idh), Phosphate (Ldh), and Tris-EDTA-Borate (Gpi, Pgm). For Me, the gels were soaked in a Phosphate buffer supplemented with NAD, and run with a Tris-EDTA- Maleate buffer. Run times varied from 20 to 40 min at 200 V.

Statistical Analysis.-For snail populations containing both sexual and clonal females, allozyme frequencies for each sample were calculated from diploid sexual snails. Conse- quently, sample sizes varied with the proportion of diploid sexuals. For Lakes McGregor and Poerua, both of which contain only triploid asexual females, allozyme frequencies were computed by interpreting the banding pattern as diploid unless there were three distinct allozymes, in which case all three allozymes were scored. In a previous study of allozyme frequencies of snail populations from Lakes Alexandrina, Mapourika, Paringa, and Wahapo, we showed that the frequency of heterozygotes among diploid sexual females met Hardy-Weinberg expectations, and that there was no indication of either inbreeding or further subdivision of populations within sites (Dybdahl and Lively 1995a).

Parasite populations may lack allozyme polymorphism and Hardy-Weinberg conformance either because of repeated bottlenecks caused by dynamic cycles, or because of selfing or mating with close relatives during the sexual portion of their life cycle within their final host. Such inbreeding is possible in Microphallus because of the clonal production of larvae in the snail host; these clonemates are then ingested together by the final host and may be likely to encounter each other during mating. Levels of allozyme polymorphism in the parasite populations were summarized using BIOSYS-1 (Swof- ford and Selander 1989). We compared the observed frequency of heterozygotes with Hardy-Weinberg expectation for each site. The magnitude and direction of departure from expectation was quantified by F1, the fixation index (Wright 1978). High levels of selfing would be reflected in high positive values of Fis, indicating deficiencies of heterozygotes. We combined F1s estimates from different loci assuming that each locus is selectively neutral. We examined the significance of Fis for each site using 1000 bootstrapped samples of the Fis-values for each locus. We corrected the significance values for multiple tests (20 sites) using a sequential Bon- ferroni procedure (Rice 1989).

We determined levels of differentiation among sites within populations for four lakes (Alexandrina, Mapourika, Paringa, and Wahapo) where three or more sites were sampled by two methods: Wright's Fst (Wright 1978) using the FSTAT routine of BIOSYS-1, and Weir and Cockerham's (1984) estimate 0 of Fst using the DIPLOID.FOR program of Weir (1990). Both methods produced similar results, except that the estimate 0 was negative in one instance. The significance of Wright's Fst estimates was assessed using a contingency x2 analysis

of allozyme frequency differences (HETXSQ routine of BIOSYS-1). For the significance of 0, we report the standard deviation of the estimate based on the jackknife procedure across loci, and the 95% confidence limits based on the bootstrap analysis across loci (Weir 1990).

We employed two methods of hierarchical analysis for levels of differentiation among all eight lakes and between the two regions: Wright's Ft (Wright 1978) using the WRIGHT78 routine of BIOSYS-1, and Weir and Cocker- ham's (1984) estimate 0 using a three-level nested analysis (Weir 1990). Again, both methods produced similar results, except that the estimate 0 was negative in one instance. The significance of Wright's Ft estimates was assessed using a contingency x2 analysis of allozyme frequency differences (HETXSQ routine of BIOSYS-1). Standard deviations and 95% confidence limits of 0 were again obtained from the jackknife and bootstrap procedure across loci, respectively.

We calculated the relative gene flow levels among lakes for the host and parasite populations because lake populations of the parasite are locally adapted to their hosts (Lively 1989). Gene flow levels were inferred from Fst estimates using the equation, Nm = {(1IF,t) - 1 }/4, where Nm is the effective number of migrants per generation; this equation provides a relatively robust estimate of gene flow even when the model's assumptions are relaxed (Slatkin and Barton 1989). Nm values were calculated for the 95% confidence limits of 0.

Analysis of F-statistics reveals levels of differentiation, but not the organization of differentiation relative to the spatial arrangement of lakes. To examine the spatial structure of allozyme variation, we depicted the relative differentiation in parasites and hosts using principal component analyses (PCA) (Proc Princomp of SAS, SAS Institute 1982). Data for the PCA were the frequencies of allozymes that exceeded 8% in the total pooled sample for each the parasite and host. The frequencies of 11 and 13 allozymes were used in the parasite and host PCA, respectively.

If parasites and host populations have a spatially correlated structure, we expected that the genetic distance between populations of parasites and hosts would be correlated. We calculated Nei's unbiased genetic distance between all pairwise combinations of the eight different lake populations for both parasites and snails using BIOSYS-1. Matrices were compared using Mantel analysis (Smouse et al. 1986), and the significance of the Mantel statistic z was evaluated using matix randomization. Matrix correlations were considered significant if the probability of obtaining the observed value of z by chance among 1000 reshuffled matrices was small (P < 0.05). We also calculated correlation and partial correlation coefficients using the formulas suggested by Smouse et al. (1986).

To further examine the correlation between genetic distance matrices, we related genetic distances to geographic distances. Geographic distances were calculated two different ways. First, we assumed that dispersal between any pair of lakes depends on straight-line geographic distance between lakes. Second, we assumed that dispersal might be more likely to occur around, rather than over, the highest glaciated portion of the Southern Alps surrounding the region of Mount Cook (Fig. 1). Hence, distances were measured between lakes


TABLE 1. Genetic and genotypic variation of populations of the parasite Microphallus sp. N is the average sample size across loci, n is the average number of alleles per locus, and H is direct count heterozygosity with its standard error (SE). F's is the fixation index averaged across loci, and P is the probability from a bootstrap analysis that the individual Fis differs significantly from zero. Asterisks indicate column-wide significance of Fs at P = 0.05 (sequential Bonferroni adjustment).

Lake Site N n H (SE) FPs P

Alexandrina 1 51 3.7 0.244 (0.08) 0.026 0.54 Alexandrina 3 18 3.2 0.257 (0.07) 0.044 0.73 Alexandrina 4 16 2.8 0.281 (0.09) 0.022 0.64 Hawdon 32 3.0 0.188 (0.06) 0.087 0.06 McGregor N 24 2.8 0.222 (0.09) 0.087 0.12 McGregor S 10 2.0 0.233 (0.08) -0.041 0.22 lanthe S 19 2.5 0.228 (0.09) -0.097 0.44 lanthe N 20 2.7 0.234 (0.10) 0.083 0.52 Mapourika Ottos2 30 3.8 0.303 (0.09) -0.011 0.68 Mapourika Creek 9 2.5 0.250 (0.10) 0.132 0.36 Mapourika Jetty 45 3.8 0.215 (0.09) -0.001 0.82 Mapourika Ottos 37 3.5 0.278 (0.11) -0.010 0.78 Paringa CabinW 30 3.3 0.266 (0.12) 0.021 0.92 Paringa 300S 40 3.8 0.247 (0.08) 0.069 0.03 Paringa BayS 31 3.3 0.289 (0.12) 0.071 0.70 Paringa 300N 36 4.3 0.275 (0.08) 0.008 0.98 Poerua 36 4.2 0.223 (0.06) 0.111 0.01* Wahapo Weir2 24 3.5 0.243 (0.11) -0.077 <0.0005* Wahapo NRA 22 3.3 0.256 (0.10) -0.024 0.56 Wahapo Weir 34 4.0 0.269 (0.11) 0.024 0.70 Mean 3.3 0.250 0.054 0.07

in stepping-stone fashion around the glaciated region. We refer to these as stepping-stone distances.

RESULTS

Allozyme frequencies for host and parasite populations collected from the 20 sites are given in the Appendix. Because parasite populations may exhibit either inbreeding or lack of variation due to bottlenecks, we analyzed the allozyme frequencies of parasite populations for levels of genetic variation, and evidence of inbreeding or further subdivision of populations within sites. (Genetic polymorphisms of snail populations have been analyzed elsewhere; Dybdahl and Lively 1995a).

Parasite Genetic Variation.-Parasites possessed considerable allozyme polymorphism within each population (Table 1; Appendix). The average number of allozymes per locus

for the six loci varied between about two and four, and heterozygosity averaged 0.25. Levels of allozyme polymorphism varied little among collections. There was also no indication of inbreeding in the parasite; heterozygosity of parasite populations did not differ significantly from expectation under Hardy-Weinberg conditions. Of only two values of Fi, that differed significantly from zero, one was positive (Poerua) and one was negative (Wahapo, site Weir2).

Differentiation and Gene Flow among Populations.-Pop- ulations collected from different sites within the same lake are relatively undifferentiated for both hosts and parasites. Although there was significant heterogeneity of allozyme frequencies among sites in most cases (according to x2 tests), levels of differentiation were small for both parasites and hosts according to both Fst and 0 estimates (Table 2). These levels of differentiation correspond to high levels of gene

TABLE 2. Allozyme frequency variation among sites within lakes for both hosts and parasites. P-values are for x2 tests of heterogeneity in allozyme frequencies among sites (asterisks indicate the significance of the test using a sequential Bonferroni adjustment for column- wide probabilities of a Type I error). Both Wright's Fs, and 0 estimates are presented. For estimates based on 0, jackknife standard deviations (SD) and bootstrap 95% confidence limits (CL) are shown.

P Fst 0 (SD) Lower CL Upper CL

Hosts Alexandrina 0.002* 0.033 0.034 (0.018) 0.009 0.062 Mapourika 0.03* 0.018 0.013 (0.003) 0.005 0.017 Paringa 0.012* 0.012 0.004 (0.006) -0.005 0.015 Wahapo 0.0001* 0.020 0.022 (0.004) 0.015 0.029

Parasites Alexandrina 0.400 0.012 -0.006 (0.005) -0.012 0.005 Mapourika 0.001 * 0.026 0.009 (0.002) 0.070 0.013 Paringa 0.080 0.013 0.001 (0.004) -0.003 0.011 Wahapo 0.010* 0.028 0.021 (0.005) 0.012 0.033 * 0.05 > P > 0.001; **0.001 > P > 0.0001.


TABLE 3. Allozyme frequency variation among lakes and between regions for both hosts and parasites. Refer to Table 2 for notes.

Lower Upper P Fst 0 (SD) CL CL

Hosts Lakes 0.0001 0.174 0.128 (0.054) 0.031 0.225 Regions 0.0001 0.010 -0.050 (0.062) -0.149 0.065

Parasites Lakes 0.0001 0.017 0.044 (0.018) 0.009 0.066 Regions 0.0001 0.007 0.013 (0.011) -0.003 0.032

flow among sites within lakes, on the order of lOs of migrants per generation.

Among lake and regional populations of the snail host, allozyme frequencies were significantly heterogeneous (X2 heterogeneity tests in Table 3). However, most of the variation in allozyme frequencies was found among lake populations, and regions add a small component to total variance in the hierarchical nested analysis of differentiation. The variation in allozyme frequencies was much larger among lake populations of the snail (Wright's FSt = 0.174, 0 = 0.128) than between regional populations (Wright's Fst = 0.010, 0 = -0.050) (Table 3). Similar to snail populations, there was more variation in allozyme frequencies for the parasite among lake populations (Wright's Fst = 0.017, 0 = 0.044) than between regional populations (Wright's Fst = 0.007, 0 = 0.013).

We were mainly interested in relative gene flow levels among lake populations of the host and parasite because most of the variation occurs among lake populations (Table 3), and because lake populations of the parasite are locally adapted to their hosts independent of region (Lively 1989). Values of the F-statistics were relatively large for the snail (Wright's F= 0.174, 0 = 0.128) compared to the parasite (Wright's Fst 0.017, 0 = 0.044) (Table 3). Gene flow estimates among lakes based on Wright's Fst were much lower for snails than for parasites (Nm = 1 for snails, Nm = 14 for parasites). The difference in gene flow estimates between hosts and parasites was smaller using 0 (Nm = 2 for snails, Nm = 5 for parasites) and the 95% bootstrapped confidence intervals overlapped (1 < Nm < 8 for snails, 4 < Nm < 28 for parasites). Taken together, these analyses of F-statistics suggest that levels of genetic variation are lower and levels of gene flow are higher among lake populations of the parasite compared to the host.

The Spatial Structure of Genetic Variation.-Principal component analysis (PCA) confirmed that hosts are more strongly structured than parasites, but also revealed the importance of the geographic proximity of lakes. For the snail host, allozyme variation was strongly structured; PCI and PC2 explained 66% of the variation in allozyme frequencies (Fig. 2A). Different sites within lakes were very similar, and clustered together, and different lakes were widely separated. However, some adjacent populations on opposite sides of the Southern Alps near mountain passes are closer to each other in the parameter space defined by PCI and PC2 (e.g., Lakes Poerua and Hawdon, or Lakes Alexandrina and Paringa) than distant populations on the same side of the Alps (e.g., Lakes Poerua and Paringa) (Fig. 1). This similarity between lakes in different regions may help explain the negative value of

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0 among regions for the snail. Negative values of 0 can arise when genes from different populations are more similar than genes from the same population (Weir 1990). Nevertheless, other lakes from the east and west sides of the Alps are quite distinct (e.g., Lakes Alexandrina and lanthe), which suggests that distance, the Alps, or both contribute to the total variance in allozyme frequencies.

For the parasite, the first two principal component axes (PCI and PC2) explained 57% of the variation in allozyme frequencies, but the pattern of differentiation among lakes and regions was less clear (Fig. 2B). Consistent with lower values of F-statistics for parasites, different sites and different lakes within regions were interspersed in the space defined by PCI and PC2. Although the additional contribution of variation among regions is relatively small compared to that among lakes (Table 3), PCA resolved regional populations with two exceptions (Lake Poerua and one Lake Mapourika site). Thus, PCA confirmed that parasite populations were weakly structured across lakes, and that lakes in different regions are slightly more differentiated on average than lakes in the same region, contributing to a small but significant level of among-region allozyme variation.

Although parasite populations are not as highly structured as the host, the spatial pattern of differentiation of parasite populations was similar to that of host populations. The correlation between host and parasite genetic distance matrices


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FIG. 3. The genetic distances (calculated for all pairs of the eight lake populations) between snail host populations plotted with (A) the genetic distances between trematode parasite populations, (B) the genetic distances between host populations plotted with stepping-stone geographic distance between lakes, and (C) the genetic distances between parasite populations plotted with stepping-stone distance.

was positive (Fig. 3A) and the Mantel statistic (z) was significant (Mantel test, z = 0.03, r = 0.40, P < 0.05). The positive correlation coefficient suggests that pairs of lakes with similar host populations also had similar parasite populations.

The correlation of parasite and host genetic distance matrices could arise because the dispersal mechanisms of both species respond similarly to geographic distance, or because one species responds to the other. Straight-line geographic distance did not correlate with the genetic distance of either the host (Mantel test, z = 32.13, r = 0.164, P > 0.10) or the parasite (Mantel test, z = 2.27, r = 0.147, P > 0.10). However, the stepping-stone distance matrix significantly and positively correlated with the host genetic distance matrix (Mantel test, z = 54.44, r = 0.72, P < 0.001) (Fig. 3B). For the parasite, stepping-stone distances were also significantly correlated with genetic distances, although the correlation was not as strong (Mantel test, z = 3.88, r = 0.53, P < 0.001) (Fig. 3C). Considering the parasite genetic distance matrix as the response variable, we found that the partial correlation of parasite genetic distance was much higher with geographic distance (r = 0.37) than with host genetic distance (r = 0.03). This suggests that parasite genetic distance responds more strongly to geographic distance than to host genetic distance.

DISCUSSION

The evolutionary outcome of host-parasite interactions depends on the amount of migration among subpopulations by both host and parasite. Low migration by both participants should lead to high degrees of local adaptation and perhaps host-race formation by the parasite. Local adaptation by parasites is favorable to coevolutionary (Red Queen) models for the maintenance of sex, but some migration seems to be required (1) to prevent the local fixation of alleles (Hamilton 1986, 1993; Frank 1991, 1993); (2) to spread adaptations to host defenses among parasite populations (Thompson 1994); and (3) to prevent a well-dispersed clone from displacing sexual reproduction across a set of populations (Ladle et al. 1993). In the present study, results of allozyme frequency analyses of a freshwater snail and its obligate parasite were concordant. Snail populations were found to be highly structured among lakes, and geographic proximity influenced genetic differentiation. Parasite populations, in contrast, showed little differentiation for allozymes (contra Price 1980; but see review in Nadler 1995), although regional populations were distinguished by PCA. Nevertheless, host and parasite genetic distances were correlated with each other and with the distances between lakes.

Greater levels of genetic differentiation among lake populations of the snail compared to the parasite indicate that gene flow is probably very low among populations of the snail host, but much higher among populations of the trematode parasite. Alternatively, the small degree of allozyme differentiation for the parasite may indicate less genetic drift in parasite populations, or that parasite populations have not yet reached a drift-migration equilibrium. These alternatives seem unlikely, however, because (1) the parasite population size is probably smaller than that of the host snail (only a fraction of the snail population is infected at one time); and (2) recently colonized populations should typically show greater among-population allozyme differentiation rather than less (Whitlock and McCauley 1990). Thus, the observed levels of allozyme differentiation suggest that gene flow is


higher among lake populations of the parasite compared to the host.

We also found that genetic distances between pairs of parasite and host populations were correlated with each other and with stepping-stone distances between populations. This result suggests either that (1) parasite and host are both dispersing to adjacent lakes; or (2) allozymes are linked to loci that are responding to local selection. The strong partial correlation between parasite genetic distance and geographic distance suggests that the correlation between parasite and host genetic distance is due to similar patterns of dispersal, rather than to a response of parasites to their hosts. This result makes sense, in that both parasite and host are likely to be dispersed by water birds moving between adjacent lakes, but parasite dispersal with its final host (birds) should be more frequent than accidental dispersal of the snail over land. Hence, taken together, our results suggest that there is more gene flow among parasite populations than among host populations, but that similar patterns of dispersal apparently pro- duce a correlation such that lakes with genetically similar host populations are likely to have similar parasite populations. In contrast, Mulvey et al. (1991) found little evidence for correlated structure between populations of a trematode fluke parasite and its final host, white-tailed deer.

High levels of gene flow among parasite populations should tend to counteract selection for local adaptation (Slat- kin 1987). However, the results of reciprocal cross-infection experiments showed that parasites are adapted to snail populations at the level of individual lakes, even when these lakes are very close (< 10 km apart) (Lively 1989). This local adaptation in the face of high rates of parasite gene flow suggests that local selection must be strong. Such selection would be expected for any obligate parasite that is dispersing among strongly differentiated host populations. We have recently found that the clonal subpopulations of the snail host are largely endemic to different lakes (Dybdahl and Lively 1995a), and the present results suggest further that the sexual populations of these lakes are also strongly differentiated. As a consequence, interaction alleles of parasite populations that determine the success or failure of infection may be quickly weeded out following migration. On the other hand, neutral alleles unlinked to selected loci are more likely to seep into a parasite population infecting a foreign host population, thereby reducing the observed levels of allozyme differentiation in the parasite. Levels of among- population phenotypic and allozymic differentiation are in- congruent in other studies. In fact, greater phenotypic differentiation compared with allozymic differentiation may indicate that natural selection caused phenotypic divergence (e.g., Spitze 1993 and references therein).

High levels of parasite gene flow could have several consequences for the maintenance of sex under the Red Queen hypothesis. First, coevolutionary cycles must be sustained within populations to provide the advantage to the production of genetically variable outcrossed offspring. One problem for the Red Queen hypothesis is that parasite populations lose polymorphism easily in computer simulations during the overshoot phase of the coevolutionary cycles by fixing for a single host genotype (Seger and Hamilton 1988; review in Lively and Apanius 1995). These models usually require high

rates of acquisition of new variation to sustain the dynamic coevolutionary cycles. If parasite populations are coevolving with highly structured hosts, like populations of Potamopyr- gus, then one source of new variation for the parasite might be gene flow (Frank 1991, 1993; Ladle et al. 1993). If gene flow is removed, parasites may lose variation to infect al- ternate hosts and form a "host race." The relatively high rate of parasite migration by Microphallus sp. could restore genetic polymorphism and prevent dynamic coevolution from being stalled by lack of variation. Along these lines, studies of dynamic coevolution between plants and pathogens suggest that migration by pathogens can maintain variation locally (reviewed in Frank 1992; Thompson and Burdon 1992; for empirical evidence see Burdon and Thompson 1995).

Although parasite migration can help sustain dynamic coevolution, gene flow maintains local parasite variation only if parasites immigrating from different populations are adapted to different host alleles. Models suggest that different populations will likely possess different interaction alleles (i.e., they are oscillating out of phase) even when migration rates are as high as 1% (Frank 1991), which would probably correspond to thousands or millions of immigrants each generation in populations of a parasite like Microphallus. The observed levels of gene flow among Microphallus parasite populations evidently do not present an obstacle to local adaptation. Furthermore, the differential rates of parasitism of host clones endemic to different lake populations suggest that out-of-phase cycles may be occurring (Dybdahl and Lively 1995a,b). At the same time, the high levels of polymorphism and heterozygosity for Microphallus allozymes suggest that gene flow is relatively strong compared to drift and inbreeding, which would otherwise reduce genetic variation locally. Finally, the high rate of gene flow among Microphallus populations may explain why some clones have escaped parasitism. For example, Clone F5 is overwhelmingly the most common clone in Lake McGregor, but we have yet to find a single infected individual from this clone (Dybdahl and Live- ly 1995b; unpubl. obs.). But Lake McGregor is a very small lake (surface area = 0.4 kM2) within a kilometer of Lake Alexandrina (surface area = 5.8 km2); in Alexandrina, clone F5 is rare (Dybdahl and Lively 1995a; Fox et al. 1996). Consequently, the parasite may be responding to the weighted frequency of the clone over both lakes, which is likely to be quite low.

Even when local adaptation and polymorphism are sustained, the relative migration of hosts and parasites have a further consequence for the maintenance of sexual reproduction in a set of populations under the Red Queen hypothesis. Ladle et al. (1993) found that asexuality displaced sexual reproduction when there was a discrepancy in the levels of dispersal between the interacting species. In particular, if parasite dispersal was low compared to host dispersal, a dispersing host clonal genotype could escape the parasites adapted to attack it, and displace sexual populations patch by patch across the set of populations. However, if parasites have higher dispersal rates than their hosts, sexual reproduction is favored under most conditions (see Fig. 1 in Ladle et al. 1993). Our results are consistent with the latter scenario, as the trematode Microphallus shows less population structure and consequently more dispersal than its snail


host. Hence, an important condition seems to be met for the persistence of sexual Potamopyrgus populations under the influences of parasitism and competition from clonal reproduction.

In conclusion, gene flow levels for the trematode parasite Microphallus sp. are higher than for its snail host Potamo- pyrgus, but genetic similarity for both species is correlated with distance between populations. Thus, despite high parasite gene flow, the population structures of parasites and hosts were correlated and related to the spatial arrangement of lakes. Furthermore, selection on parasite migrants imposed by genetically differentiated host populations appears to be sufficiently strong to overcome parasite gene flow, since local parasite populations are apparently adapted to local host populations (Lively 1989). High rates of gene flow among Mi- crophallus sp. populations that are coevolving with highly structured Potamopyrgus populations should continually restore selectable variation in local parasite populations, and enhance the persistence of sexual reproduction in a set of populations.

ACKNOWLEDGMENTS

We thank M. Hellberg, J. Jokela, D. McCauley, M. Ruck- elshaus, J. Thompson, S. Via, and an anonymous reviewer for comments on previous drafts of the manuscript. We also thank B. Weir for assistance with the three-level nested analysis, and J. McKenzie, J. Van Berkle, M. Winterbourn, I. McLean, and the Department of Zoology at the University of Canterbury for logistical support. This study was sup- ported by grants from the U.S. National Science Foundation (BSR-9008848 and DEB-9317924).

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Corresponding Editor: S. Via


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