The Geography of Coevolution: Comparative Population Structures for a Snail and Its
Trematode Parasite
Author(s): Mark F. Dybdahl and Curtis M. Lively
Source: Evolution, Vol. 50, No. 6 (Dec., 1996), pp. 2264-2275
Published by: Society for the Study of Evolution
Stable URL: http://www.jstor.org/stable/2410696 .
Accessed: 15/08/2011 22:16
Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .
http://www.jstor.org/page/info/about/policies/terms.jsp
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of
content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms
of scholarship. For more information about JSTOR, please contact [email protected].
Society for the Study of Evolution is collaborating with JSTOR to digitize, preserve and extend access to
Evolution.
http://www.jstor.org
Evolution, 50(6), 1996, pp. 2264-2275
THE GEOGRAPHY OF COEVOLUTION: COMPARATIVE POPULATION
STRUCTURES FOR A SNAIL AND ITS TREMATODE PARASITE
MARK
F
AND CURTIS
DYBDAHL1
M.
LIVELY
Bloomington,Indiana 47405
Departmentof Biology,Indiana University,
'E-mail: [email protected]
of host and parasitepopulationsare criticalto the coevolutionary
Abstract.-Geneflowand the geneticstructure
Here we compare
coevolutionfavorssexualreproduction.
process,includingtheconditionsunderwhichantagonistic
with
antipodarum)
New Zealand snail (Potamopyrgus
of different
populationsof a freshwater
the geneticstructures
data.Allozymevariationamongsnailpopulations
its trematode
parasite(Microphallussp.) usingallozymefrequency
amonglake
amonglakes; but fortheparasitetherewas littleallozymestructure
was foundto be highlystructured
with
populations,suggestingmuchhigherlevels of parasitegene flow.The overallpatternof variationwas confirmed
forthesnail(butnot
of geneticdifferentiation
principalcomponentanalysis,whichalso showedthattheorganization
sides
of lakes. Some snailpopulationsfromdifferent
theparasite)was strongly
relatedto thegeographicarrangement
of theAlps nearmountainpasses weremoresimilarto each otherthanto othersnail populationson thesame side
of the Alps. Furthermore,
geneticdistancesamongparasitepopulationswere correlatedwiththe geneticdistances
amonghostpopulations,and geneticdistancesamongbothhostand parasitepopulationswerecorrelatedwith"stepparasiteseemto be dispersingto adjacent
ping-stone"distancesamonglakes. Hence,thehostsnail and its trematode
fashion,althoughparasitedispersalamonglakes is clearlygreater.High parasitegene flow
lakes in a stepping-stone
reintroduce
geneticdiversitywithinlocal populationswherestrongselectionmightothshouldhelp to continuously
(Red Queen) dynamicsthat
erwiseisolate "host races." Parasitegene flowcan therebyfacilitatethecoevolutionary
lost geneticvariation.
by restoring
conferan advantageto sexual reproduction
sexual reproduction.
Red Queen hypothesis,
Key words.-Coevolution,gene flow,parasites,populationstructure,
ReceivedAugust23, 1995. AcceptedJuly3, 1996.
The subdivision of populations, the spatial patternof selection, and gene flow can all influence the coevolutionary
process (Thompson 1994). Consequently, parasite-host coevolution depends on genetic variation and its structurein
both interactingspecies. For example, restrictedgene 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 structuredwith little gene flow
between populations or host races. High parasite gene flow
will tend to counteractlocal 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 restorevariation that is lost by recurrentextinctionof local populations
in a metapopulation (Frank 1991, 1993).
The restorationof genetic variationto local populations of
parasites may be especially importantwhen 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
interactionswithhostalleles
engaged in frequency-dependent
can easily "overshoot" and become fixedin local populations
due to the time lags. Such fixationis most likely when selection on the parasite is strong(Seger 1988, Seger and Hamilton 1988), and when parasite fitnessdepends on host density
as well as the frequency of host genotypes (May and Anderson 1983). Small amounts of migrationhave been shown
to be very effectivein maintaininggenetic diversityin local
parasite populations (Hamilton 1986, 1993; Frank 1991,
parasite populations are adapted
1993), provided the different
to differentsets of host alleles (i.e., the differentpopulations
are oscillating out of phase; Frank 1991).
Frequency-dependentand time-lagged dynamic coevolution is central to recent ideas on the role of parasites in
selecting forthe productionof outcrossed sexual versus parthenogeneticoffspringin their hosts (The "Red Queen hypothesis," Jaenike 1978; Bremermann1980; Hamilton 1980;
Bell 1982). Hence, the genetic structureof parasite-hostpopulations may have importantconsequences 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; Judson1995). In addition,
the relative migrationof hosts and parasites can affectthe
successful spread of host clones in a metapopulation,and the
outcome of competitionbetween sexual and clonal strategies.
Ladle et al. (1993) showed thatparthenogenesiswill replace
sexual reproductionif parasite dispersal is low relative to
host dispersal, but that sexual reproductionis 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 importanceof comparing the relative structures of host and parasite populations, there have been few
studies that attemptto map parasite genetic structureonto
host genetic structure(review in Nadler 1995). Mulvey et al.
(1991) foundsignificantspatial variationforboth deer (hosts)
and parasitic flukes. However, the between-population genetic distances forthe host and parasite were not concordant
with each other or with geographic distances among populations (perhaps due to the wide-rangingmovements of the
deer). Here we compare the population genetic structuresof
a freshwatersnail (Potamopyrgusantipodarum)and its trem-
2264
(C 1996 The Society forthe Study of Evolution. All rightsreserved.
2265
HOST-PARASITE POPULATION STRUCTURE
atode parasite(Microphallussp.) usingdata fromallozyme
This specifichost-parasite
combination
is of
electrophoresis.
particularinterestbecause prevalenceof infectionis correlated withthe frequencyof sexual individualsamongpopulations(consistentwiththeRed Queen hypothesis;Lively
1987, 1992; Jokelaand Lively 1995), and becausereciprocal
have shownthattheparasiteis
cross-infection
experiments
adaptedto its local hostpopulations(Lively 1989). Herewe
show thatthislocal adaptationis maintainedin theface of
considerablegene flowby the parasite.We also show that,
than
althoughparasitesmigratemoreand are less structured
theirhosts,thegeneticdistancesinbothspeciesarecorrelated
witheach other,and withgeographicdistancesamongpopulations.
MATERIALS
Poerua
,IHawdon
IF~~~~~~~
..
|
~~~I
AND METHODS
Natural Historyof the Host and Parasite.-The
freshwater region(dar shading in the South
is a small (< 8 mm)prosobranch
gas- 1!|11 _ _ ! I i 1E
snailP. antipodarum
z ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~~~~__
New Zealand
tropod,whichis commonin lakes throughout
1970). This snail
at elevationsless than750 m (Winterbourn
is dioecious. Females may be eithersexual and diploid,or
40
~ ~ ~ ~ ~~0k
(PhillipsandLambert1987;Dybdahl
apomicticparthenogens
and Lively 1995a) and triploid(Wallace 1992). Generation
timeis typicallyaboutfourmonthsin thelab (unpubl.obs.).
host to at least a dozen
This snail is the firstintermediate
whichcastratebothsexes of
speciesof digenetictrematodes,
infectedindividuals(Winterbourn1974; MacArthurand
Featherston
1976). An undescribedspecies of thedigenetic
micocntrfue
ube adsapfrzenbAimexaindrinalqi
trematodeMicrophallusis responsiblefor most trematode
infectionsin lake populationsof Potamopyrgus(Lively
timein thesnailof
1987). Microphallussp. has a generation
threeto fourmonthsunderlaboratoryconapproximately
ditions(unpubl.obs.), at whichtimeparasitedsnailsbecome
Microfilledwithlargenumbersof encystedmetacercariae.
wheninfectedsnailsare
phallussp. maythenbe transmitted
ingestedby theirfinalhosts,whichincludea varietyof waterfowland wadingbirds(Lively and McKenzie 1991).
by immersio inrliq
sp-frze
microcentrifuge tubes.a
ofr
laaksiontheSouthcIslanda
Collection and Electrophoresis.-We collected snails in FIag. 1.nTertiveb licohatiolofth
the
glaciate
whic
Zaland
from
snailstiwerecollected,rand
Newse
1993 from20 sitesspreadovereightlakeson thesouthisland
of parasite ames. Thecpasiesamples
of New Zealand (Fig. 1). To examinethedifferentiation
cerforme infete
siteswithinlakes,we collectedfromthreeor foursitesfrom
fourlakes (Alexandrina,Mapourika,Wahapo,and Paringa). nitrogn.rigemann
Th
s
snailwerelhousdtemporarly
drvdfoasingl
Parasitesare knownto be adaptedto thelocal hostpopulaonfaquaria
1-all
teowobai
beeroprocites(sed
uniltheypecould
tions in these fourlakes (Lively 1989). We also collected
r
fromsinglesitesfromtwo lakes (Hawdonand Poerua),and
twositesfromtwootherlakes (lantheand McGregor).Three
of these lakes (Alexandrina,McGregor,and Hawdon) are
locatedon theeast side of theSouthernAlps, and theother
fivearelocatedon thewestside.All lakescontainpopulations
of both sexual and asexual femalesexcept McGregorand
Poerua,whichcontainall-female,asexual populations.Collections were made fromrocks and vegetationalong the
shoreline.
wherewe
Live snails were transported
to the laboratory,
obtainedtwo separatesamplesfromeach of the 20 sites: a
sampleof snailsand a sampleofMicrophallusparasitetissue
frominfectedsnails.The sampleof snailswas composedof
the first70 individualsobtainedhaphazardlyfromthe collections.These snailswereplaced in groupsof 10 in 1.5-mL
tesnails
tatdwere ullsied,
fromg theoletaionsSnailsfwerrecdipsse Rctrdusinge
almicroscope,
andlassesed frcetaerclarisa-d
byrMupicropyHallus.
Parasit metacercariaweres.
saequipmnfetio
Frteaehpr rmte
anedsnap-frozenting1u.5-m
snailtetrphreissues
foasingleb
asexal
withoind
singlessnail
e desrived
shoulypodbe
pattrnonzthegrels
was9confirmedbthebadetring
eg,ahihladLvy
bot
Cuellulose aetaen
pesuectrvophreiswase perfolyrmedsonve
the snails:an theppartiasiesusing
thestanoan buffer
rec
Ipes
adah andhLivel
1995a)s and tsodetermineallydozyenfre-
mutase, 2.5.7.3), 6pgd
1.1.1.42), Pgm (phosphoglycerate
2266
M. F. DYBDAHL AND C. M. LIVELY
(6-phosphogluconate
dehydrogenase,
1.1.1.44), Mpi (man- of allozyme frequencydifferences(HETXSQ routineof
nose-phosphate
isomerase,5.3.1.8), and Aat (aspartateami- BIOSYS-1). Forthesignificance
of 0, we reportthestandard
notransferase,
2.6.11).
deviationof the estimatebased on thejackknifeprocedure
The parasitesamplesweregroundwith18 FiLof crushing acrossloci, andthe95% confidence
limitsbased on thebootinpreparation
buffer
forelectrophoresis.
Six presumptive
loci strapanalysisacrossloci (Weir1990).
werereliablyresolvedin theparasiteand revealedvariation We employedtwomethodsofhierarchical
analysisforlevwithinand amonglocalities:Pgm,Idh, Me (malic enzyme, els of differentiation
amongall eightlakes and betweenthe
1.1.1.40), Gpi (glucose-phosphate
isomerase,5.3.1.9), Mdh two regions: Wright's Ft (Wright 1978) using the
(malatedehydrogenase,
1.1.1.37),and Ldh (lactatedehydro- WRIGHT78 routineof BIOSYS-1, and Weir and Cockergenase, 1.1.1.27). Runningand soakingbufferswere Tris- ham's (1984) estimate0 usinga three-levelnestedanalysis
Maleate(Mdh,Idh),Phosphate(Ldh),andTris-EDTA-Borate (Weir 1990). Again,bothmethodsproducedsimilarresults,
(Gpi, Pgm). For Me, the gels were soaked in a Phosphate exceptthattheestimate0 was negativein one instance.The
buffersupplemented
withNAD, and runwitha Tris-EDTA- significance
of Wright'sFt estimateswas assessed usinga
Maleatebuffer.
Runtimesvariedfrom20 to 40 minat 200 V. contingency
x2 analysisof allozymefrequencydifferences
StatisticalAnalysis.-For snail populations containingboth (HETXSQ routineof BIOSYS-1). Standarddeviationsand
sexual and clonal females,allozymefrequenciesfor each 95% confidencelimitsof 0 were again obtainedfromthe
sample were calculatedfromdiploid sexual snails. Conse- jackknifeand bootstrapprocedureacrossloci, respectively.
of diploid
quently,sample sizes variedwiththeproportion
We calculatedthe relativegene flowlevels amonglakes
sexuals. For Lakes McGregorand Poerua, both of which forthehostandparasitepopulations
becauselakepopulations
containonlytriploidasexual females,allozymefrequencies oftheparasitearelocallyadaptedtotheirhosts(Lively1989).
werecomputedby interpreting
thebandingpattern
as diploid Gene flowlevels wereinferred
fromFstestimatesusingthe
unlesstherewerethreedistinctallozymes,in whichcase all equation, Nm =
1
where Nm is the effective
}/4,
{(1IF,t)
threeallozymeswerescored.In a previousstudyofallozyme numberof migrants
thisequationprovidesa
pergeneration;
frequenciesof snail populationsfromLakes Alexandrina, relatively
robustestimateofgeneflowevenwhenthemodel's
Mapourika,Paringa,and Wahapo,we showedthatthe fre- assumptionsare relaxed(Slatkinand Barton1989). Nmvalquencyof heterozygotes
amongdiploidsexual femalesmet ues werecalculatedforthe95% confidencelimitsof 0.
Hardy-Weinberg
expectations,and thattherewas no indiAnalysisof F-statisticsreveals levels of differentiation,
cationof eitherinbreedingor further
subdivisionof popu- butnotthe
of differentiation
relativeto thespaorganization
lationswithinsites(Dybdahland Lively 1995a).
tial arrangement
of lakes.To examinethespatialstructure
of
Parasitepopulationsmaylackallozymepolymorphism
and
allozymevariation,we depictedthe relativedifferentiation
Hardy-Weinberg
eitherbecauseofrepeatedbotconformance
in parasitesand hosts using principalcomponentanalyses
tleneckscaused by dynamiccycles,or because of selfingor
(PCA) (Proc Princompof SAS, SAS Institute1982). Data
matingwithclose relativesduringthesexualportionoftheir
for
thePCA werethefrequencies
ofallozymesthatexceeded
lifecyclewithintheirfinalhost.Such inbreeding
is possible
8%
in
the
total
for
each theparasiteandhost.
pooled
sample
in Microphallusbecause of the clonal productionof larvae
11
The
13
frequencies
of
and
allozymes
were used in the
in thesnailhost;theseclonematesaretheningestedtogether
host
and
parasite
PCA,
respectively.
by thefinalhostand maybe likelyto encountereach other
Ifparasitesandhostpopulationshavea spatiallycorrelated
in theparduringmating.Levels of allozymepolymorphism
we expectedthatthegeneticdistancebetweenpopstructure,
asitepopulationsweresummarized
usingBIOSYS-1 (Swofulations
of
parasitesand hostswouldbe correlated.We calfordand Selander 1989). We comparedthe observedfreculated
Nei's
unbiasedgeneticdistancebetweenall pairwise
withHardy-Weinberg
quencyof heterozygotes
expectation
of theeightdifferent
lake populationsforboth
foreach site.The magnitude
and directionof departure
from combinations
snails
and
BIOSYS-1.
Matriceswere comparasites
using
expectationwas quantified
by F1, thefixationindex(Wright
Mantel
et
pared
using
al. 1986), and the
analysis
(Smouse
in highpos1978). Highlevels of selfingwouldbe reflected
of
the
Mantel
statistic
was
evaluatedusing
significance
z
itivevalues of Fis, indicatingdeficienciesof heterozygotes.
Matrixcorrelationswere considered
We combinedF1sestimatesfromdifferent
loci assumingthat matixrandomization.
iftheprobability
of obtainingtheobservedvalue
each locus is selectivelyneutral.We examinedthe signifi- significant
z
of
chance
1000
reshuffled
by
matriceswas small(P
among
cance of Fis foreach site using 1000 bootstrapped
samples
<
correlation
0.05).
We
also
calculated
andpartialcorrelation
oftheFis-valuesforeach locus.Wecorrected
thesignificance
usingthe formulassuggestedby Smouse et al.
values formultipletests(20 sites) using a sequentialBon- coefficients
(1986).
ferroni
procedure(Rice 1989).
examinethe correlationbetweengeneticdisWe determined
levelsofdifferentiation
amongsiteswithin To further
tance
we relatedgeneticdistancesto geographic
matrices,
for
four
lakes
populations
(Alexandrina,
Mapourika,Paringa,
andWahapo)wherethreeor moresitesweresampledbytwo distances.Geographicdistanceswerecalculatedtwodifferent
methods:Wright's
Fst(Wright1978) usingtheFSTAT routine ways. First,we assumedthatdispersalbetweenanypair of
geographicdistancebetween
of BIOSYS-1, and Weirand Cockerham's(1984) estimate0 lakes dependson straight-line
ofFstusingtheDIPLOID.FOR program
ofWeir(1990). Both lakes.Second,we assumedthatdispersalmightbe morelikemethodsproducedsimilarresults,exceptthattheestimate0 ly to occur around,ratherthanover,the highestglaciated
was negativein one instance.The significanceof Wright's portionoftheSouthern
theregionofMount
Alps surrounding
x2 analysis Cook (Fig. 1). Hence,distancesweremeasuredbetweenlakes
Fstestimateswas assessed usinga contingency
2267
HOST-PARASITEPOPULATIONSTRUCTURE
TABLE 1. Geneticand genotypicvariationof populationsof theparasiteMicrophallussp. N is theaveragesamplesize across loci, n
is the averagenumberof alleles per locus, and H is directcountheterozygosity
withits standarderror(SE). F's is the fixationindex
froma bootstrapanalysisthattheindividualFis differssignificantly
fromzero. Asterisks
averagedacross loci, and P is theprobability
indicatecolumn-widesignificance
of Fs at P = 0.05 (sequentialBonferroni
adjustment).
Site
N
n
H (SE)
FPs
N
S
S
N
Ottos2
Creek
Jetty
Ottos
CabinW
300S
BayS
300N
51
18
16
32
24
10
19
20
30
9
45
37
30
40
31
36
36
24
22
34
3.7
3.2
2.8
3.0
2.8
2.0
2.5
2.7
3.8
2.5
3.8
3.5
3.3
3.8
3.3
4.3
4.2
3.5
3.3
4.0
3.3
0.244 (0.08)
0.257 (0.07)
0.281 (0.09)
0.188 (0.06)
0.222 (0.09)
0.233 (0.08)
0.228 (0.09)
0.234 (0.10)
0.303 (0.09)
0.250 (0.10)
0.215 (0.09)
0.278 (0.11)
0.266 (0.12)
0.247 (0.08)
0.289 (0.12)
0.275 (0.08)
0.223 (0.06)
0.243 (0.11)
0.256 (0.10)
0.269 (0.11)
0.250
0.026
0.044
0.022
0.087
0.087
-0.041
-0.097
0.083
-0.011
0.132
-0.001
-0.010
0.021
0.069
0.071
0.008
0.111
-0.077
-0.024
0.024
0.054
Lake
Alexandrina
Alexandrina
Alexandrina
Hawdon
McGregor
McGregor
lanthe
lanthe
Mapourika
Mapourika
Mapourika
Mapourika
Paringa
Paringa
Paringa
Paringa
Poerua
Wahapo
Wahapo
Wahapo
Mean
1
3
4
Weir2
NRA
Weir
P
0.54
0.73
0.64
0.06
0.12
0.22
0.44
0.52
0.68
0.36
0.82
0.78
0.92
0.03
0.70
0.98
0.01*
<0.0005*
0.56
0.70
0.07
in stepping-stone
fashionaroundthe glaciatedregion.We forthesix loci variedbetweenabouttwo and four,and hetreferto theseas stepping-stone
distances.
erozygosity
averaged0.25. Levels ofallozymepolymorphism
variedlittleamongcollections.Therewas also no indication
RESULTS
in theparasite;heterozygosity
of inbreeding
ofparasitepopulations
did
not
differ
significantly
from
expectation
under
Allozymefrequenciesfor host and parasitepopulations
Hardy-Weinberg
conditions.
Of
only
two
values
of
Fi, that
collectedfromthe20 sitesaregivenintheAppendix.Because
differed
from
one
was
significantly
zero,
positive
(Poerua)
or lack of
parasitepopulationsmayexhibiteitherinbreeding
variationdue to bottlenecks,
we analyzedtheallozymefre- and one was negative(Wahapo,siteWeir2).
Differentiationand Gene Flow among Populations.-Popquenciesof parasitepopulationsforlevels of geneticvariasiteswithinthe same lake
subdivisionof ulationscollectedfromdifferent
tion,and evidenceof inbreedingor further
are
undifferentiated
for
bothhostsand parasites.
relatively
of snail
populationswithinsites. (Geneticpolymorphisms
Although
there
was
significant
heterogeneity
ofallozymefrepopulationshave been analyzed elsewhere;Dybdahl and
quenciesamongsites in mostcases (accordingto x2 tests),
Lively 1995a).
were small forbothparasitesand
Parasite Genetic Variation.-Parasites possessed consid- levels of differentiation
erableallozymepolymorphism
withineachpopulation(Table hostsaccordingto bothFst and 0 estimates(Table 2). These
correspondto high levels of gene
1; Appendix).The averagenumberof allozymesper locus levels of differentiation
2. Allozymefrequency
variationamongsiteswithinlakes forbothhostsand parasites.P-valuesare forx2 testsof heterogeneity
in allozymefrequenciesamongsites(asterisksindicatethesignificance
of thetestusinga sequentialBonferroni
forcolumnadjustment
wide probabilitiesof a Type I error).Both Wright'sFs, and 0 estimatesare presented.For estimatesbased on 0, jackknifestandard
deviations(SD) and bootstrap95% confidencelimits(CL) are shown.
TABLE
P
Fst
0
(SD)
Lower CL
Upper CL
Hosts
Alexandrina
Mapourika
0.002*
0.03*
0.033
0.018
0.034
0.013
(0.018)
(0.003)
Wahapo
0.0001*
0.020
0.022
(0.004)
Paringa
Parasites
Alexandrina
Mapourika
Paringa
Wahapo
0.012*
0.400
0.001 *
0.080
0.010*
* 0.05 > P > 0.001; **0.001 > P > 0.0001.
0.012
0.004
0.009
0.005
0.062
0.017
0.015
0.029
(0.006)
-0.005
0.012
-0.006
(0.005)
-0.012
0.028
0.021
(0.005)
0.012
0.026
0.013
0.009
0.001
(0.002)
(0.004)
0.070
-0.003
0.015
0.005
0.013
0.011
0.033
2268
M. F. DYBDAHL AND C. M. LIVELY
3. Allozymefrequency
variationamonglakesandbetween
regionsforbothhostsand parasites.Referto Table 2 fornotes.
TABLE
P
Fst
Hosts
Lakes
0.0001 0.174
Regions 0.0001 0.010
Parasites
Lakes
0.0001 0.017
Regions 0.0001 0.007
0
(SD)
Lower
CL
A. HOST
A
Upper
CL
**AA
2
0
0.128 (0.054)
-0.050 (0.062)
0.031 0.225
-0.149 0.065
0.044 (0.018)
0.013 (0.011)
0.009 0.066
-0.003 0.032
.0
cm
oO
w
*0+
East
- -22
-
0
0
A
0
flowamong sites withinlakes, on the orderof lOs of migrants
per generation.
Among lake and regional populations of the snail host,
allozyme frequencies were significantlyheterogeneous (X2
heterogeneitytestsin Table 3). However, mostof thevariation
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 variationin allozyme frequenciesfortheparasite among
lake populations (Wright'sFst = 0.017, 0 = 0.044) than between regional populations (Wright'sFst = 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 variationoccurs among lake populations (Table 3), and
because lake populations of the parasite are locally adapted
to theirhosts independentof 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 flowestimatesamong
lakes based on Wright'sFst were much lower for snails than
forparasites (Nm = 1 forsnails, Nm = 14 forparasites). The
differencein gene flowestimatesbetween hosts and parasites
was smaller using 0 (Nm = 2 forsnails, Nm = 5 forparasites)
and the 95% bootstrappedconfidenceintervalsoverlapped (1
< Nm < 8 for snails, 4 < Nm < 28 for parasites). Taken
together,these analyses of F-statistics suggest thatlevels of
genetic variationare lower and levels of gene floware higher
among lake populations of the parasite compared to the host.
The Spatial Structure of Genetic Variation.-Principal
component analysis (PCA) confirmedthat hosts are more
stronglystructuredthan parasites, but also revealed the importance of the geographic proximityof lakes. For the snail
host, allozyme variation was stronglystructured;PCI and
PC2 explained 66% of the variation in allozyme frequencies
(Fig. 2A). Differentsites withinlakes were very similar,and
clusteredtogether,and differentlakes were widely separated.
However, some adjacent populations on opposite sides of the
SouthernAlps near mountainpasses are closer to each other
in the parameterspace definedby PCI and PC2 (e.g., Lakes
Poerua and Hawdon, or Lakes Alexandrina and Paringa) than
distantpopulations on the same side of the Alps (e.g., Lakes
Poerua and Paringa) (Fig. 1). This similaritybetween lakes
in differentregions may help explain the negative value of
A4-4
0
-2
4
0
Q
2
+
*
Paringa
Poerua
Wahapo
a
3
4
A~~~~~~
AN
a
Hawdon
McGregor
West
*
lanthe
* Mapourika
A
PARASITE
2cm
N ?-
4
(36%)
PC1
B.
l
a0
Alexandrina
. 0v
A*
-2
4
2
0
PC1 (33%)
-2
-4
scoresbased on allozymefrequencies
FIG.2. Principalcomponent
of20 collectionsforthe(A) snailhostand(B) itstrematode
parasite.
0 among regions forthe snail. Negative values of 0 can arise
when genes fromdifferentpopulations are more similar than
genes fromthe same population (Weir 1990). Nevertheless,
otherlakes fromthe east and west sides of the Alps are quite
distinct(e.g., Lakes Alexandrina and lanthe), which suggests
thatdistance,the Alps, or both contributeto the totalvariance
in allozyme frequencies.
For the parasite, the firsttwo principal component axes
(PCI and PC2) explained 57% of the variation in allozyme
frequencies, but the patternof differentiationamong lakes
and regions was less clear (Fig. 2B). Consistent with lower
values of F-statisticsforparasites,differentsites and different
lakes within regions were interspersedin the space defined
by PCI and PC2. Although the additional contributionof
variation among regions is relativelysmall compared to that
among lakes (Table 3), PCA resolved regional populations
with two exceptions (Lake Poerua and one Lake Mapourika
site). Thus, PCA confirmedthat parasite populations were
weakly structuredacross lakes, and that lakes in different
on average thanlakes
regions are slightlymore differentiated
in the same region, contributingto a small but significant
level of among-regionallozyme variation.
Although parasite populations are not as highlystructured
as the host, the spatial patternof differentiationof parasite
populations was similar to thatof host populations. The correlation between host and parasite genetic distance matrices
2269
HOST-PARASITE POPULATION STRUCTURE
0
0.25-
The correlation
of parasiteand hostgeneticdistancematricescould arisebecause thedispersalmechanismsof both
speciesrespondsimilarlyto geographicdistance,or because
one species respondsto the other.Straight-line
geographic
distancedid notcorrelatewiththegeneticdistanceof either
the host (Manteltest,z = 32.13, r = 0.164, P > 0.10) or
A.
uW 0.2
0
0.15 -
03
the parasite (Mantel test, z = 2.27, r = 0.147, P > 0.10).
~~ ~~~
I
0
0
0
0.0
0.1
0.2 - LI
C
However,thestepping-stone
distancematrixsignificantly
and
positivelycorrelatedwiththe host geneticdistancematrix
0
I3
015
.2
3
005
0
0.25 -
& 0.2
0-a
H O
B
so
u
a
(Mantel test,z = 54.44, r = 0.72, P < 0.001) (Fig. 3B). For
theparasite,stepping-stone
distanceswerealso significantly
correlatedwithgeneticdistances,althoughthe correlation
was notas strong(Manteltest,z = 3.88, r = 0.53,P < 0.001)
(Fig. 3C). Consideringthe parasitegeneticdistancematrix
as theresponsevariable,we foundthatthepartialcorrelation
ofparasitegeneticdistancewas muchhigherwithgeographic
distance(r = 0.37) thanwithhostgeneticdistance(r = 0.03).
This suggeststhatparasitegeneticdistancerespondsmore
strongly
to geographicdistancethanto hostgeneticdistance.
DISCUSSION
The evolutionary
outcomeofhost-parasite
interactions
dependson theamountof migration
amongsubpopulations
by
bothhost and parasite.Low migration
by bothparticipants
100
oD
00
10003030 20
shouldlead to highdegreesof local adaptationand perhaps
host-raceformation
by theparasite.Local adaptationbyparasitesis favorableto coevolutionary
(Red Queen) modelsfor
the maintenanceof sex, but some migrationseems to be
required(1) to preventthelocal fixation
of alleles (Hamilton
Geographic distance (kin)
1986, 1993; Frank1991, 1993); (2) to spreadadaptationsto
hostdefensesamongparasitepopulations(Thompson1994);
0 .02 0~0C.
PARASITE
and (3) to preventa well-dispersedclone fromdisplacing
sexual reproduction
acrossa set of populations(Ladle et al.
1993). In the presentstudy,resultsof allozymefrequency
0
0.01510
snail and its obligateparasitewere
analysesof a freshwater
concordant.
Snail
werefoundto be highlystrucpopulations
0.01
a
turedamonglakes,and geographicproximity
influenced
ge0.0
netic differentiation.
Parasite populations, in contrast,
showedlittledifferentiation
forallozymes(contraPrice1980;
0
._~~
in
but
see
review
Nadler
1995),
although
regionalpopulations
0.05
0
0
0~~~~~~
weredistinguished
by PCA. Nevertheless,
hostand parasite
geneticdistanceswere correlatedwitheach otherand with
thedistancesbetweenlakes.
0
100
200
300
400
Greaterlevels of geneticdifferentiation
amonglake populationsof the snail comparedto the parasiteindicatethat
Geographic distance (km)
flowis probablyverylow amongpopulationsof the
FIG. 3. The geneticdistances(calculatedforall pairsof theeight gene
snail
butmuchhigheramongpopulationsof thetremhost,
lake populations)betweensnail hostpopulationsplottedwith(A)
the small degreeof allozyme
thegeneticdistancesbetweentrematode
parasitepopulations,(B) atode parasite.Alternatively,
the geneticdistancesbetweenhostpopulationsplottedwithstep- differentiation
fortheparasitemayindicateless geneticdrift
ping-stonegeographicdistancebetweenlakes,and (C) thegenetic in parasitepopulations,
or thatparasitepopulationshave not
distancesbetweenparasitepopulationsplottedwithstepping-stone
yetreacheda drift-migration
These alternatives
equilibrium.
distance.
seem unlikely,however,because (1) theparasitepopulation
size is probablysmallerthanthatof the host snail (only a
of thesnailpopulationis infectedat one time);and
was positive (Fig. 3A) and the Mantel statistic(z) was sig- fraction
nificant(Mantel test, z = 0.03, r = 0.40, P < 0.05). The (2) recentlycolonized populationsshould typicallyshow
positive correlation coefficientsuggests that pairs of lakes greateramong-population
rather
allozyme differentiation
with similar host populations also had similar parasite pop- thanless (WhitlockandMcCauley1990). Thus,theobserved
ulations.
levels of allozymedifferentiation
suggestthatgene flowis
OU
colo
00
0
2270
M. F. DYBDAHL AND C. M. LIVELY
higheramonglake populationsof theparasitecomparedto ratesof acquisitionof new variationto sustainthedynamic
cycles.If parasitepopulationsarecoevolving
coevolutionary
thehost.
hosts,like populationsof PotamopyrWe also foundthatgeneticdistancesbetweenpairsofpar- withhighlystructured
asite and host populationswere correlatedwitheach other gus,thenone sourceof new variationfortheparasitemight
distancesbetweenpopulations.This be gene flow(Frank1991, 1993; Ladle et al. 1993). If gene
and withstepping-stone
resultsuggestseitherthat(1) parasiteand hostare bothdis- flowis removed,parasitesmay lose variationto infectalhighrate
persingto adjacentlakes; or (2) allozymesare linkedto loci ternatehostsandforma "hostrace." The relatively
by Microphallussp. could restoregeto local selection.The strongpartialcor- of parasitemigration
thatare responding
and preventdynamiccoevolutionfrom
relationbetweenparasitegeneticdistanceand geographic neticpolymorphism
betweenparasiteand beingstalledby lack of variation.Alongtheselines,studies
distancesuggeststhatthe correlation
hostgeneticdistanceis due to similarpatternsof dispersal, of dynamiccoevolutionbetweenplantsand pathogenssugby pathogenscan maintainvariationlorather
thanto a responseofparasitestotheirhosts.Thisresult gestthatmigration
makessense,in thatbothparasiteand hostare likelyto be cally(reviewedin Frank1992; Thompsonand Burdon1992;
dispersedby waterbirdsmovingbetweenadjacentlakes,but forempiricalevidencesee Burdonand Thompson1995).
can help sustaindynamiccoAlthoughparasitemigration
parasitedispersalwithits finalhost(birds)shouldbe more
frequentthan accidentaldispersalof the snail over land. evolution,gene flowmaintainslocal parasitevariationonly
populationsareadaptfromdifferent
ourresultssuggestthatthereis more ifparasitesimmigrating
Hence,takentogether,
host alleles. Models suggestthatdifferent
gene flowamongparasitepopulationsthanamonghostpop- ed to different
alleles
interaction
ofdispersalapparently
pro- populationswill likelypossess different
ulations,butthatsimilarpatterns
duce a correlationsuch thatlakes withgeneticallysimilar (i.e., theyare oscillatingout of phase) even whenmigration
hostpopulationsare likelyto have similarparasitepopula- ratesare as highas 1% (Frank1991),whichwouldprobably
each gento thousandsor millionsof immigrants
Mulveyet al. (1991) foundlittleevidence correspond
tions.In contrast,
betweenpopulationsof a trematode erationin populationsof a parasitelike Microphallus.The
forcorrelatedstructure
observedlevels of gene flowamongMicrophallusparasite
deer.
flukeparasiteand its finalhost,white-tailed
High levels of gene flow among parasitepopulations populationsevidentlydo notpresentan obstacleto local adratesof parasitismof
thedifferential
selectionforlocal adaptation(Slat- aptation.Furthermore,
shouldtendto counteract
lakepopulationssuggestthat
kin 1987). However,theresultsof reciprocalcross-infectionhostclonesendemicto different
cycles maybe occurring(Dybdahland Lively
showedthatparasitesare adaptedto snail pop- out-of-phase
experiments
ulationsat the level of individuallakes, even when these 1995a,b).At thesametime,thehighlevelsofpolymorphism
forMicrophallusallozymessuggestthat
lakes are veryclose (< 10 km apart)(Lively 1989). This and heterozygosity
local adaptationin the face of highratesof parasitegene gene flowis relativelystrongcomparedto driftand inbreedflowsuggeststhatlocal selectionmustbe strong.Such se- ing,whichwouldotherwisereducegeneticvariationlocally.
lectionwould be expectedforany obligateparasitethatis Finally,thehighrateof gene flowamongMicrophalluspophost populations. ulationsmay explainwhysome clones have escaped paradispersingamong stronglydifferentiated
themost
ofthe sitism.For example,Clone F5 is overwhelmingly
We haverecentlyfoundthattheclonalsubpopulations
lakes (Dybdahl commonclone in Lake McGregor,butwe have yetto finda
snail host are largelyendemicto different
individualfromthisclone(DybdahlandLiveand Lively 1995a), and the presentresultssuggestfurther singleinfected
thatthe sexual populationsof theselakes are also strongly ly 1995b; unpubl.obs.). But Lake McGregoris a verysmall
alleles of par- lake (surfacearea = 0.4 kM2) withina kilometerof Lake
As a consequence,interaction
differentiated.
clone
thesuccessor failureof in- Alexandrina(surfacearea = 5.8 km2); in Alexandrina,
asite populationsthatdetermine
On F5 is rare (Dybdahl and Lively 1995a; Fox et al. 1996).
fectionmaybe quicklyweededout followingmigration.
totheweighted
theparasitemaybe responding
the otherhand,neutralalleles unlinkedto selectedloci are Consequently,
of theclone overbothlakes,whichis likelyto be
more likelyto seep into a parasitepopulationinfectinga frequency
reducingtheobservedlevels quitelow.
thereby
foreignhostpopulation,
are susEven when local adaptationand polymorphism
in theparasite.Levels of amongof allozymedifferentiation
are in- tained,the relativemigrationof hostsand parasiteshave a
populationphenotypicand allozymicdifferentiation
consequencefor the maintenanceof sexual reprocongruentin otherstudies.In fact,greaterphenotypicdif- further
mayin- ductionin a set of populationsunderthe Red Queen hyferentiation
comparedwithallozymicdifferentiation
dicate thatnaturalselectioncaused phenotypicdivergence pothesis.Ladle et al. (1993) foundthatasexualitydisplaced
sexual reproduction
when therewas a discrepancyin the
therein).
(e.g., Spitze 1993 and references
species. In parHigh levels of parasitegene flowcould have severalcon- levels of dispersalbetweenthe interacting
of sex undertheRed Queen ticular,if parasitedispersalwas low comparedto hostdissequencesforthemaintenance
cycles mustbe sustained persal,a dispersinghost clonal genotypecould escape the
hypothesis.First,coevolutionary
withinpopulationstoprovidetheadvantagetotheproduction parasitesadaptedto attackit,anddisplacesexualpopulations
One problemfor patchby patch across the set of populations.However,if
ofgenetically
variableoutcrossedoffspring.
the Red Queen hypothesisis thatparasitepopulationslose parasiteshave higherdispersalratesthantheirhosts,sexual
is favoredundermostconditions(see Fig. 1 in
easily in computersimulationsduringthe reproduction
polymorphism
overshootphase of thecoevolutionary
cyclesby fixingfora Ladle et al. 1993). Our resultsare consistentwiththelatter
Microphallusshowsless populasinglehost genotype(Seger and Hamilton1988; reviewin scenario,as thetrematode
moredispersalthanits snail
and consequently
LivelyandApanius1995). Thesemodelsusuallyrequirehigh tionstructure
HOST-PARASITE POPULATION STRUCTURE
2271
in a host with
. 1993. Haploid dynamicalpolymorphism
conditionseemsto be metforthe
host.Hence,an important
linkageand
matching
parasites,effectsof mutation/subdivision,
populationsunderthe
persistenceof sexual Potamopyrgus
patternsof selection.J. Hered.84:328-338.
fromclonal repro- HAMILTON,W. D., R. AXELROD, AND R. TANESE. 1990. Sexual
influencesof parasitismand competition
duction.
as an adaptationto resistparasites:A review.Proc.
reproduction
Nat. Acad. Sci. USA 87:3566-3573.
parasite
In conclusion,gene flowlevels forthetrematode
Microphallussp. are higherthanforits snail hostPotamo- HOWARD,R. S., AND C. M. LIVELY. 1994. Parasitism,mutation
of sex. Nature367:554-557
accumulationand themaintenance
forbothspecies is correlated
pyrgus,but geneticsimilarity
in vol. 368, p. 358)
(figuresreprinted
withdistancebetweenpopulations.Thus, despitehighpar- HUTSON,V., AND R. LAW. 1981. Evolutionof recombination
in
selectionwith
populationsexperiencingfrequency-dependent
of parasitesand
asite gene flow,the populationstructures
hostswerecorrelatedand relatedto thespatialarrangement timedelay.Proc. R. Soc. Lond. B Biol. Sci. 213:345-359.
J. 1978. An hypothesisto accountforthe maintenance
imposed JAENIKE,
selectionon parasitemigrants
oflakes.Furthermore,
of sex withinpopulations.Evol. Theory3:191-194.
hostpopulationsappearsto be JAYAKAR, S. 1970. A mathematical
by geneticallydifferentiated
modelforgenefrequenciesin
strongto overcomeparasitegeneflow,sincelocal
sufficiently
parasitesand theirhosts.Theor.Popul. Biol. 1:140-164.
adaptedto local hostpop- JOKELA, J., AND C. M. LIVELY. 1995. Parasites,sex and earlyreparasitepopulationsareapparently
snails.Evolution
in a mixedpopulationoffreshwater
production
ulations(Lively 1989). High ratesof gene flowamongMi49:1268-1271
crophallussp. populationsthatare coevolvingwithhighly JUDSON,0. P. 1995. Preservinggenes:A modelofthemaintenance
restructured
Potamopyrgus
populationsshouldcontinually
underfrequency-deof geneticvariationin a metapopulation
pendentselection.Genet.Res. Camb. 65:175-191.
storeselectablevariationin local parasitepopulations,and
in a set of LADLE, R. J.,R. A. JOHNSTONE,AND 0. P JUDSON. 1993. Coevoenhancethe persistenceof sexual reproduction
Escaping the
lutionarydynamicsof sex in a metapopulation:
populations.
Red Queen. Proc. R. Soc. Lond. B Biol. Sci. 253:155-160.
ACKNOWLEDGMENTS
LIVELY, C. M. 1987. Evidencefroma New Zealand snail forthe
of sex by parasitism.Nature328:519-521.
maintenance
. 1989. Adaptationby a parasitictrematodeto local pop-
We thankM. Hellberg,J.Jokela,D. McCauley,M. Ruckulationsof its snail host.Evolution43:1663-1671
elshaus,J. Thompson,S. Via, and an anonymousreviewer
in a freshwater
snail:Reproductive
. 1992. Parthenogenesis
assurance versus parasitic release. Evolution 46:907-913
We also
forcommentson previousdraftsof themanuscript.
nestedanal- LIVELY, C. M., AND V. APANIUS. 1995. Geneticdiversityin hostthankB. Weirforassistancewiththethree-level
parasite interactions.Pp. 421-449 in A. Dobson and B. Grenfell,
I.
ysis, and J. McKenzie, J. Van Berkle,M. Winterbourn,
eds. Ecology of infectiousdiseases in naturalpopulations. Camof Zoology at the University bridge Univ. Press. Cambridge.
McLean, and the Department
for logisticalsupport.This studywas sup- LIVELY, C. M., ANDJ. McKENZIE. 1991. Experimental infectionof
of Canterbury
a freshwatersnail, Potamopyrgusantipodarum,with a digenetic
portedby grantsfromtheU.S. NationalScienceFoundation
trematode,
Microphallussp. NZ Nat. Sci. 18:59-62.
(BSR-9008848 and DEB-9317924).
C.
AND D. W. FEATHERSTON.1976.
Suppression
MAcARTHUR, P.,
of egg production in Potamopyrgus antipodarum (Gastropoda:
LITERATURE
CITED
NZ J. Zool. 3:35-38.
Hydrobiidae)by larvaltrematodes.
G. 1982. The masterpieceof nature:The evolutionand ge- MAY, R. M., AND R. M ANDERSON. 1983. Epidemiology and genetics in the coevolution of parasites and hosts. Proc. R. Soc.
neticsof sexuality.Univ.of CaliforniaPress,Berkeley.
Lond. B Biol. Sci. 219:281-313.
as strategiesin
BREMERMANN, H. J. 1980. Sex and polymorphism
MULVEY, M., J. M. AHO, C. LYDEARD, P. L. LEBERG, AND M. H.
interactions.
J.Theor.Biol. 87:671-702.
host-pathogen
SMITH. 1991. Comparative population genetic structureof a
of
BURDON, J. J., AND J. N. THOMPSON. 1995. Changedpatterns
parasite (Fascioloides magna) and its definitivehost. Evolution
resistancein a populationof Linummarginaleattackedby the
45:1628-1640.
rustpathogenMelampsoralini.J.Ecol. 93:199-206
of
and thegeneticstructure
rela- NADLER, S. A. 1995. Microevolution
CLARKE, B. 1976. The ecological geneticsof host-parasite
parasite populations. J. Parasitol. 81:395-403.
tionships.Pp. 87-103 in A. E. R. Taylorand R. Muller,eds.
Blackwell,Ox- PHILLIPS, N. R., AND D. M. LAMBERT. 1987. Geneticsof Potarelationships.
Geneticaspects of host-parasite
(Gastropoda:Prosobranchia):Evidence
antipodarum
mopyrgus
ford.
forreproductive
modes.NZ J.Zool. 16:435-445.
DYBDAHL, M. F, AND C. M. LIVELY. 1995a. Diverse,endemicand
snail PRICE, P. W. 1980. Evolutionary biology of parasites. Princeton
clones in mixedpopulationsof a freshwater
polyphyletic
BELL,
(Potamopyrgus antipodarum). J. Evol. Biol. 8:385-398.
Univ. Press. Princeton,NJ.
Infectionof common RICE, W. R. 1989. Analyzing tables of statistical tests. Evolution
. 1995b. Host-parasiteinteractions:
43:223-225
snail (Potamopyrclones in naturalpopulationsof a freshwater
Proc.R. Soc. Lond. B Biol. Sci. 260:99-103. RICHARDSON, B. J.,P. R. BAVERSTOCK, AND M. ADAMS. 1986. Allogus antipodarum).
and
A handbookforanimalsystematics
zymeelectrophoresis:
Fox, J. A., M. F DYBDAHL, J. JOKELA, AND C. M. LIVELY. 1996.
populationalstudies.AcademicPress,San Diego, CA.
ofcoexistingsexualandclonalsubpopulations
Geneticstructure
SAS INSTITUTE. 1982. SAS user'sguide: Statistics.SAS Institute,
in a freshwatersnail (Potamopyrgusantipodarum). Evolution 50:
Cary,NC.
1541-1548.
models
FRANK, S. A. 1991. Ecologicalandgeneticmodelsofhost-pathogen SEGER, J. 1988. Dynamicsof some simple host-parasite
with more than two genotypes in each species. Philos. Trans. R.
coevolution.Heredity67:73-83.
Soc. Lond. B 319:541-555.
coevolution.TrendsGe. 1992. Models of plant-pathogen
SEGER J., AND W. D. HAMILTON.
1988. Parasites and sex. Pp. 176net.8:213-219.
193 in R. E. Michod and B. R. Levin, eds. The evolution of sex.
. 1993. Coevolutionarygeneticsof plantsand pathogens.
Sinauer, Sunderland MA.
Evol. Ecol. 7:45-75.
HAMILTON, W. D. 1980. Sex versusnon-sexversusparasite.Oikos SLATKIN, M. 1987. Gene flow and the geographic structureof naturalpopulations.Science 236:787-792
35:282-290.
and cyclingof twocompetinghostswith SLATKIN, M., AND N. H. BARTON. 1989. A comparisonof three
. 1986. Instability
indirect methods for estimating average levels of gene flow.
twoparasites.Pp. 645-668 in S. Karlinand E. Nevo, eds. EvoEvolution 43:1349-1368.
lutionaryprocessesand theory.AcademicPress,New York.
2272
M. F. DYBDAHL AND C. M. LIVELY
P. B., J. C. LONG, AND R. R. SOKAL. 1986. Multiple regression and correlation extensions of the Mantel test of matrix
correspondence. Syst. Zool. 35:627-632.
SPITZE, K. 1993. Population structurein Daphnia obtuse: Quantitativegenetic and allozymic variation. Genetics 135:367-374.
SWOFFORD,
D. L., AND R. B. SELANDER.
1989. BIOSYS-1: A computer program for the analysis of allelic variation in population
genetics and biochemical systematics. Release 1.7. Univ. of Illinois, Urbana.
THOMPSON,
J. N. 1994. The coevolutionary process. Univ. of Chicago Press, Chicago.
THOMPSON,
J. N., AND J. J. BURDON. 1992. Gene-for-genecoevolution between plants and parasites. Nature 360:121-125.
WALLACE,
C. 1992. Parthenogenesis, sex and chromosomes in Potamopyrgus.J. Moll. Stud. 58:93-107.
WEIR, B. S. 1990. Genetic data analysis. Sinauer, Sunderland, MA.
SMOUSE,
B. S., AND C. C. COCKERHAM.
1984. Estimating F-statistics
for the analysis of population structure. Evolution 38:13581370.
WHITLOCK,
M. C., AND D. E. MCCAULEY.
1990. Some population
genetic consequences of colony formationand extinction: Genetic correlations within founding groups. Evolution 44:17171724.
WINTERBOURN,
M. J. 1970. The New Zealand species of Potamopyrgus(Gastropoda: Hydrobiidae). Malacologia 10:283-321.
. 1974. Larval Trematoda parasitizing the New Zealand species of Potamopyrgus(Gastropoda: Hydrobiidae). Mauri Ora 2:
17-30.
WRIGHT, S. 1978. Evolution and Genetics of Populations. Vol. 4.
Variability within and among populations. Univ. of Chicago
Press, Chicago.
WEIR,
Editor:S. Via
Corresponding
2273
HOST-PARASITE POPULATION STRUCTURE
ON
>c
t.
<
0
ON--0
Z
Cl
00sN
o
0000N
tO??.
-e~
CMO
>1
C
oooo0
00
r-
03
-
C)
~-~Clt---
CC~~~~~~~~C
/)CN
Z
<11 X[
o
{
ce tX tI
o
03
O
01)
CO
Y
Z
l
Cm m kD
9z $
t00000
9l
CC
.>
CO
c
c
o
ooo
O 0
~
_$ooN~
:
C/NC
mO
-ON
0 0 0 0
0 0 0 0 0
Cl
0
0
rONo
0
0
ooo
O
0
00000
-0000
_000
0
_OINON_
0 0 0
-
0
IC)
00000
?
N
-00
0
-00000
COC0
VN
'trON
rN
O
0
O
lV)
CCC
C)
v
Q
|
C)S{c
ozl
>
00NO
m00000
CO
I-
0
CO
00
o
. 0
m0000
>
? [-mt
00C'1 b
000
000
C
t000
r?> m1
t
0
m000
-
t000
m000
>xn
? t00Cl
00
-000
-0000
t00000
<
m
OC
? cun
'rt\0
O
000000
0
T)
C=>
[-
x
0
m00000
)
5
?o>C
-000
C
m00000
)C
?Oct
m0000
mO
O?
>
mC
0
c
cIc
H~~~~~~
-
66o
00
t0000 \o6oo
[?rCu N?Vft)
)C
? {B ttC)
P
N
000
0000
?tvC/NON\.O
Cl~~~~~~~~~~~~~~cCC
c/l
>
000NCl
~00
00000oo
C)~~~~~~~~~~~~~~~~~~~~I
tS
66ooo0
t
C/
uN
?mk
c)
E~~~~~~~~~~~~~~~~~~~~~~~~~~
0~~~~~~~~~~~~~~~~~0m
O
>oO
>m
>
00
; 0O
O
OC
ot N
o
ONCl~~~~~~~~~~~~~~~~~~-
) 0 0 0
0
-0000
OCw)
0 \IC
0 0
rN
ooooo
Nm
S
E=
0
0
r-
-o0~
'C/NOO
fW N
O
'uOCl
m
~t
0
0
000
oOCl
V')
OCO
00
00m
-ON
Or-
]~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~cnm
t000
6o0
t00000
OC)-
r-
0
t0000
cq > tr
C
000M
oOmo
000
CN
O N-
'to6o6
V)
ooo
Ch
0
n N
Cm
4:
tA
Ct)
c
t> N00
C
NfN)
OO
z
x
-O
,XO
ruC--
0
SC
C
_
-~C--Cl
I
ru?
0
ON-
000
~
c) c
l0
o
0000
0c
C)
z
CC
I
CCtCC/N
I1)N
0
~00c0
00 -
00 cq,tm,a
N~~~~~~~~~~~~~~~~~~~~~~~~~~~~0
I
0 I
OOC
000
00
0000
0
ooooo
C/ooo
oo
?
ON~Cfm
OCr)o
r-
r--m
0
C/N
0
oo
o
00
O?oN
oo
??N00
emof0C/o
tC/
0
oO-.-
o
CN
-N
0C OfC C/ N
mOCm0
0 ooN0
ooo
ooo
00N0
o
?O
st/N
Cl
tNtN
u r
0r-ri
N
00C
~~~0000
oooo
00000
~ooo
0
tOm
N
"P
t
r--.
cu
0~-CNo0c
Crg
rN
~
" V/ "I'
t
"t
N?f
r--.
cum
o~"~-
(4
CuN
C)
C)
uN
CN
O
t
V O
.
NC
It
truN
I
V)N
N
u
C
2274
M. F. DYBDAHL
M
00
-
tn 00 C,\ M
,c
,c
cq
M
x r- V) x V) M M
-
03
=
cf
03
r- "t ,c "t N N
M C,\M r- 't
'It
M It
M
u
03
M
M
M
00 V) 00 V)
cf cf
C,\
M
M0
cq ',C - 00
C'\'It 00 "C
M
03
00
00
OC)
C) C)
r-
00
00
N tn 00
CN CN ,c
M
M
',C
ct
00
M
00
N
C)
r- cq
C) C)
rN
V')
cq
M "t
00
cq
"C cq
cq It
M
00 00
OC)
C)
C)
C
C
C
M M
CIN C
C
OC)
M
M
00 M M
M r- C
M
41)
M
C
C)
C)
M
C)
MO
M
<=)
C)
C 00-
N
M M
00
cc
VI)
M
N
M
N N
C)
C
C
V)
C
M
C
M
r-
00
-
N 00
C
CIN
C
00
00
-
00
M
C
C
-
V) 00 "C
M
M tn
0
00
M
,C
V)
oc c) c)
M
00 r- M
M 00
00
M
00
M
C)
00 M tn
cq OIN
03
C C)
"C
cq cq
C,\ M M
00 00 00 M
M
M
M - rOC)
M
,cM
O
03
03
-
M
CN
V')
cq cq
0
It
N
C,\
mm
OC)
00 M
"Coo C)
M V)
AND C. M. LIVELY
C
C)
00
V)
N
C
00
C
r N C)
C
0
N 00
M
00
00
V)
00
M
C
clq 00
00 C
V)
C
M
C
M
clq CIN M
00 r-
C
"C
C
M
00 00 r-
M
C
M
C
HOST-PARASITE POPULATION STRUCTURE
B
ooooooo
oooooooo
oooooo
~~~~ON 000o
ooo6oo
U
-0000000
X
U
cm
oooooooo
ooo6oo
000000
U
ooooooo
?~~~~
o
1rO
oooooo
00000000oo
O0
CNooo0o
oooo6o
O
00000000
- 0000000
X
ooo
oooooo
Z
z
oooooo
00000
00000o
o00000000
-00000
00000000
0~00000
2275