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Animal Conservation (2001) 4, 103–109 © 2001 The Zoological Society of London Printed in the United Kingdom
Parasite resistance and genetic variation in the endangered
Gila topminnow
Philip W. Hedrick, Timothy J. Kim and Karen M. Parker1
Department of Biology, Arizona State University, Tempe, AZ 85287, USA
1
Present address: Inst. de Zoologie et d’Ecologie Anim., Université de Lausanne, Bâtiment de Biologie, Lausanne 1015, Switzerland
(Received 22 May 2000; accepted 8 November 2000)
Abstract
In recent years, it has become apparent that introduced or novel pathogens or parasites may have a sig-
nificant negative impact on endangered species. Here we examine experimentally the effect of an exotic
fluke from guppies on the endangered Gila topminnow. Populations from different sources showed vari-
able responses (although statistically non-significant) to the fluke and, in particular, the most homozy-
gous population had high fluke infections and high subsequent mortality. Homozygotes for a MHC
(major histocompatibility complex) gene had lower (although statistically non-significant) survival when
infected with flukes than did heterozygotes. An inbred line from one of the populations had statistically
significant lower survival and higher fluke infection than did a simultaneous outbred control. Overall,
Gila topminnows appear quite susceptible to infection by the non-native fluke compared to other related
species. In addition, it was shown that Gila topminnows can be infected by casual contact with infected
guppies. This is another example of the potential detrimental effects of a parasite on an endangered
species, a threat that may constitute a particular problem for species with low genetic variation, either
in general, for important MHC genes, or for populations with a past history of inbreeding.
INTRODUCTION Resistance to HIV and hepatitis in humans appears to
be higher for MHC heterozygotes than for homozygotes
Threats to endangered species include human mediated
(Thurz et al., 1997; Carrington et al., 1999). However,
effects of habitat alteration and destruction, hunting and
the level of genetic variation in the MHC, and other
pollution, and the biotic effects of introduced competi-
genes that influence host resistance, may be lower in
tors and predators. In recent years, it has become widely
endangered species because of past or present small pop-
recognized that endangered species may be also threat-
ulation size. This may make endangered species even
ened by exposure to parasites (O’Brien & Evermann,
more susceptible to the effects of parasites than com-
1988; Lyles & Dobson, 1993), many of them exotic and
mon species that have large population sizes and con-
novel to the endangered species. Here we will define
sequently higher levels of genetic variation. In addition,
parasites broadly to include viruses, bacteria, protozoa,
inbred animals within a population (inbreeding may be
helminths and arthropods, which can cause a reduction
of higher frequency in the small populations of endan-
in fitness to the host (Anderson & May, 1979). Often
gered species) may have higher susceptibility than out-
parasites may not be able to maintain themselves in an
bred individuals (Coltman et al., 1999).
endangered species because of low host density.
The Gila topminnow (Poeciliopsis o. occidentalis)
However, if the parasites can infect multiple hosts, they
was once the most common fish species in the Gila River
may have a reservoir in more common related taxa, such
watershed, which drains much of southeastern and east
as introduced or domesticated species, including live-
central Arizona, United States, but now it is present in
stock or pets (Woodroffe, 1999).
only a few isolated headwaters and springs (Minckley,
Resistance of a host to parasites often has an impor-
1999). The major reasons for this decline are thought to
tant genetic component. In particular, genes in the MHC
be loss of habitat and the introduction of the non-native
(major histocompatibility complex) (Edwards &
western mosquito fish (Gambusia affinis). The Gila
Hedrick, 1998) play an important role in disease resis-
topminnow was listed in the United States as endangered
tance to parasites in vertebrates (Hedrick & Kim, 2000).
in 1967 and has since been the subject of extensive
For example, the MHC in humans has been shown to be
translocation and research efforts to promote recovery.
important in resistance to HIV, hepatitis and malaria.
Research includes genetic studies to determine the
All correspondence to: Philip W. Hedrick. Tel: (480) 965-0799; amount and pattern of molecular genetic variation and
Fax: (480) 965-2519; E-mail: philip.hedrick@asu.edu. fitness differences over the extant populations
104 P. W. HEDRICK ET AL.
(Vrijenhoek, Douglas & Meffe, 1985; Quattro & heavily infected guppy was anaesthetized with MS 222
Vrijenhoek, 1989; Sheffer, 1997; Parker, Sheffer & (23 mg/l). Flukes from this guppy were used to infect
Hedrick, 1999; Sheffer, Hedrick & Velasco, 1999). In topminnows with two flukes each, an average standard
addition, Hedrick & Parker (1998) investigated variation used in other investigations (Scott, 1982; Leberg &
for a class II MHC gene in Gila topminnow populations Vrijenhoek, 1994) (a pilot study on Gila topminnow
from the four watersheds in which they remain. Relevant indicated inoculation with five flukes quickly over-
to our study here, they found no variation at this MHC whelmed the fish). The topminnow to receive flukes was
gene in the Bylas Spring population while they found also anaesthetized with MS 222 and, using two fine for-
MHC variation in samples from Cienega Creek, Monkey ceps, an infected guppy fin was placed on the caudal fin
Spring and Sharp Spring. of the topminnow under a dissecting microscope
We investigated resistance of the Gila topminnow to (25–30×). After two flukes were transferred, the top-
the exotic fluke, Gyrodactylus turnbulli, a short-lived, minnow was placed in a plastic container with 500 ml
native parasite on wild guppies, Poecilia reticulata, in of water. Each was fed Tetramin daily and was on a
Trinidad (Harris, 1986). This fluke has been a subject of 10/14 dark/light cycle. Topminnows were sedated at
study both in guppies (Scott, 1982; Lyles, 1990) and in 5-day intervals and the fluke numbers assayed until day
Mexican Poeciliopsis species (Leberg & Vrijenhoek, 25. By this time, virtually all of the fish either had elim-
1994) closely related to P. o. occidentalis. It is a mono- inated the flukes or had died from heavy fluke infesta-
genean helminth living on body surfaces, mainly gills, tion. During experiments, a topminnow from each test
and multiplying viviparously and generally asexually. category, such as different populations, received flukes
Guppies are native to northern South America and from the same guppy to reduce any differences that may
nearby Caribbean islands, but have been spread world- occur by using flukes from different source guppies.
wide in suitable habitat and persist in warm springs in Generation length of the fluke is short, on average 4.2
several western states of the United States, including days on guppies (Scott, 1982) and Leberg & Vrijenhoek
Arizona. As a result, guppy parasites, such as G. turn- (1994) stated that generation length at 25°C was 2.4
bulli, have increased in geographic distribution and may days. Although we did not specifically measure genera-
potentially become an exotic parasite on populations of tion length with life-history information, under our hus-
Gila topminnows. A related fluke, G. salaris, has bandry and temperature (average 25°C) conditions, we
become a major source of mortality in Atlantic salmon estimated that it was about 3 to 4 days.
in Norway (Johnsen & Jensen, 1986).
Our specific goals were to determine if resistance in
RESULTS
Gila topminnows to the exotic fluke (1) varies among
individuals from the four remaining watersheds, (2) dif- During the infection of the first 20 fish, five from each
fers between heterozygotes and homozygotes at the of the four populations, five control fish from each pop-
MHC gene, and (3) differs between inbred and outbred ulation were also handled in the same manner except for
topminnows. infection with flukes. All but one control fish survived.
In other words, there appeared to be no effect of han-
dling and anesthesia and it seemed unnecessary to con-
MATERIALS AND METHODS
tinue controls with uninfected fish for other parts of the
Gila topminnows were sampled from stocks originally study. However, in all cases there were simultaneous
collected from four Arizona sites with natural popula- infections of fish from different populations or groups
tions, Bylas Spring, Cienega Creek, Monkey Spring and so that effects were measured relative to those in other
Sharp Spring, under US Fish and Wildlife Services per- individuals. For different MHC genotypes, individual
mit. These stocks are now maintained at Arizona State fish that were heterozygous or homozygous were not
University (ASU) in large raceways at adult population known at the time of infection. Therefore, although
numbers averaging around 1000. We also used an inbred infection for all groups by flukes from the same guppy
line derived from our Cienega Creek stock and main- was not controlled, infection was unrelated (at random)
tained by brother–sister mating for seven generations. to MHC genotype.
The fluke stock was originally acquired from a feral We observed three general patterns of infection by
population of guppies in a water treatment pond at Davis, flukes (Table 1) and Madhavi & Anderson (1985) have
California. To reduce genetic variation in the flukes and given host susceptibility designations for these three cat-
thereby standardize virulence of the parasite over the dif- egories. First, resistant hosts are those ‘on which the par-
ferent hosts, flukes were passed through ten bottleneck asite either fails to establish or fails to reproduce after
generations. Specifically, to initiate the stock, two flukes temporary establishment’ (see Bylas 13 in Table 1). For
were used to manually infect a guppy. Once this guppy Bylas 13, because flukes were checked after experi-
was heavily infected, two flukes from it were used to mental transfer for attachment, it is assumed that flukes
infect another. This was done serially for ten guppy died over the first 5 days without reproducing. In addi-
infections and the resulting flukes were used in the tion, if there were one or two flukes on day 5 and no
experiments. flukes on day 10, then the host is also categorized as
In the challenge protocol, as approved by the ASU resistant. Second, moderately susceptible hosts (see
Institutional Animal Care and Use Committee, first a Cienega 5 in Table 1) are ones ‘on which the parasite
Parasite resistance in topminnows 105
Table 1. Description of different typical courses of infection of the
fluke on topminnows observed at 5-day intervals and the categoriza-
tion of the host susceptibility type where – indicates no fish
Number of flukes on day
Individual 0 5 10 15 20 25 Host susceptibility
Bylas 13 2 0 0 > 0 0 0 Resistant
Cienega 5 2 13 6 > 0 0 0 Moderately susceptible
Sharp 13 2 4 14 >50 Dead – Highly susceptible
population builds up by reproduction but the host slowly
recovers and the parasite is eliminated’. Because the life
expectancy of the fluke is short (as discussed above),
observation of more than two flukes at day 5 or any
flukes at day 10 demonstrates reproduction. Finally,
highly susceptible hosts are ones ‘on which the parasite Fig. 1. The mean number of flukes for different census days
population grows rapidly and the infection results in host for fish from the four populations.
death’. For some of these fish, as for Sharp 13 in Table
1, the number of flukes increased greatly, generally to
more than 50 (at this point it became difficult to accu- rapid with only five infected on day 15 and only one fish
rately count all flukes), and the fish died. In a few oth- infected at day 20 (out of 35 infected on day 5). Second,
ers, the numbers of flukes increased but were not this the number of flukes was highest for either Bylas Spring
high during our counts. Because we had extremely low or Sharp Spring for all sampling days except day 20 or
mortality in our controls, if these fish died, we classified 25 when few fish remained infected. In particular, a
them as highly susceptible. very high medium number of 25 flukes was observed
on the 15 infected fish in the Bylas sample at day 15.
Although there are these trends, all t-tests between
Comparison between populations
different populations for the different census times are
We compared 41 fish from each of the four populations non-significant.
for resistance to flukes (actually one fish was eliminated The impact of infection can also be described by com-
from further consideration from both Monkey and Sharp paring the proportion of fish with different numbers of
Springs because they died though no flukes were flukes (no flukes, 1–10 flukes, >10 flukes) or where the
observed on day 5). Let us first examine the number of fish are dead. Again, infection appeared most severe,
flukes observed at different days by considering the based on the number of flukes in the different categories
mean and medium number of flukes over the course of and the proportion of mortality, in either the Bylas or
the experiment (Fig. 1, Table 2). Because the growth of Sharp Spring samples. Infection in Cienega Creek and
the fluke appears exponential and, as a result, the cate- Monkey Spring seemed less severe, with lower numbers
gory > 50 flukes (called 50 here) greatly increases the of flukes in most categories and a lower proportion of
mean, examining the medium number is also useful. mortality. The cumulative mortality over time for the
Note that the sample size declined over days, either four populations is given in Fig. 2. χ2 tests showed no
because fish eliminated the fluke or because fish died. significant heterogeneity for any of these comparisons.
First, the number of flukes is lowest for the Monkey A complementary pattern was seen for fish that had
Spring sample at the 5-, 10- and 15-day censuses. Also recovered from initial infection with flukes, i.e., the
the course of infection for the Monkey Spring fish was cumulative proportion of fish that had no flukes was
Table 2. The mean (± standard error) and medium number of flukes, on fish that had flukes, for the
four different populations at 5-day intervals (N is the sample number of fish). – indicates that there
were no fish with flukes
Number of flukes on day
Population Measure 5 10 15 20 25
Bylas Spring Mean 12.2 ± 2.4 13.0 ± 1.7 28.3 ± 5.1 6.0 –
Medium 6 14 25 6 –
N 36 21 15 2 –
Cienega Creek Mean 5.8 ± 0.7 14.0 ± 2.8 14.3 ± 4.1 10.0 ± 4.9 2.0
Medium 5 9 9 2 2
N 39 27 15 5 1
Monkey Spring Mean 5.6 ± 0.4 7.2 ± 2.2 13.0 ± 9.4 10 –
Medium 3 2 2 10 –
N 35 19 5 1 –
Sharp Spring Mean 8.7 ± 1.1 20.6 ± 3.0 16.7 ± 5.5 – –
Medium 7 23 6 – –
N 38 27 13 – –
106 P. W. HEDRICK ET AL.
the SSCP (single-stranded confirmation polymorphism)
approach as given by Hedrick & Parker (1998) for this
class II MHC locus. For various technical reasons, we
were able to determine genotypes of only 77 of the 121
fish from Cienega, Monkey and Sharp Springs (all Bylas
were assumed homozygous; see Hedrick & Parker,
1998). Overall, there were 87 fish homozygous and 31
heterozygous (Table 3). For all three populations in
which both heterozygotes and homozygotes were
present, survival of heterozygotes was higher. The over-
all survival of heterozygotes was 15.5% higher than that
of homozygotes. However, χ2 = 1.64 (1 df) and is non-
significant.
Observed MHC heterozygosity was 0.00, 0.41, 019
and 0.60 for Bylas, Cienega, Monkey and Sharp sam-
ples, respectively, similar to that found by Hedrick &
Fig. 2. The cumulative mortality for different census days for
Parker (1998). Although Bylas had both the lowest MHC
fish from the four populations.
heterozygosity and a low survival, Sharp had the high-
est MHC heterozygosity and low survival. In addition,
higher (although non-significantly so) for days 15 Monkey had the second lowest heterozygosity but sur-
through 25 for Cienega Creek and Monkey Spring than vival nearly as high as Cienega Creek. In other words,
for Bylas and Sharp Springs. there appears no positive association between MHC het-
The overall effect of fluke infection is summarized for erozygosity and survival from fluke infection.
the three categories, resistant, moderately susceptible
and highly susceptible, in Fig. 3. Note the Bylas and
Comparison of inbred versus outbred fish
Sharp Springs samples have the lowest proportion of
resistant fish (0.15 in both populations) and the highest The largest difference in the apparent effect of fluke
proportion of highly susceptible fish (0.46 in Bylas and infection was observed between the 13 inbred and 13
0.45 in Sharp). The highest proportion of resistant fish outbred fish we examined simultaneously from Cienega
was in Monkey Spring (0.30). However, χ2 = 6.7 (6 df) Creek. Inbred fish had a much higher infection of flukes
and is non-significant. Proportions of fish that survived than the simultaneously assessed outbred fish (and the
the infection were 0.54, 0.71, 0.68 and 0.55 for the previously examined population sample discussed above
Bylas, Cienega, Monkey and Sharp samples, respec- in Table 2). In addition, mortality of the inbred fish, 69%,
tively. In other words, survival in Cienega Creek fish was much higher than in the outbred control, 31% (χ2
was 31%, 4% and 29% higher than in Bylas, Monkey = 3.84, 1 df, P = 0.05). In other words, survival of inbred
and Sharp, respectively. fish was more than twice as high as that of the simulta-
neously assessed outbred sample (the survival of the pre-
viously examined population sample, 0.71, was even
Comparison of MHC heterozygotes versus
slightly more different from the inbred).
homozygotes
The fish examined from the four populations were cat-
CONCLUSIONS AND DISCUSSION
egorized as either heterozygous or homozygous using
More and more evidence is accumulating that exotic par-
asites may be a major detrimental factor in extinction of
endangered species. To evaluate this effect under con-
Table 3. The survival status at 25 days for homozygotes and
heterozygotes at the class II MHC locus for fish from the four
populations (proportions in parentheses).
Genotypes
Population Status Homozygotes Heterozygotes
Bylas Spring Alive 22 (0.54) –
Dead 19 (0.46) –
Cienega Creek Alive 12 (0.71) 9 (0.75)
Dead 5 (0.29) 3 (0.25)
Monkey Spring Alive 15 (0.71) 4 (0.80)
Dead 6 (0.29) 1 (0.20)
Sharp Spring Alive 3 (0.38) 7 (0.58)
Fig. 3. The proportion of fish from the four populations that Dead 5 (0.62) 5 (0.42)
were classified as resistant, moderately susceptible and highly Total Alive 52 (0.60) 22 (0.71)
Dead 35 (0.40) 9 (0.29)
susceptible.
Parasite resistance in topminnows 107
trolled experimental conditions, we examined the impact homozygotes observed in the previous samples). In other
of an exotic guppy parasite, G. turnbulli, on the endan- words, nearly a doubling of the population experiment
gered Gila topminnow. A topminnow population from and more than a tripling of the genotype experiment
Bylas Spring, earlier found to have lower genetic vari- would have been necessary to have statistical signifi-
ation than other samples, appears to have relatively low cance for the size of effects that we observed.
resistance to the fluke. However, a Sharp Spring sam- Overall, these studies demonstrate Gila topminnows
ple, which has the highest genetic variation, also had as generally susceptible to infection by the exotic guppy
similarly low resistance. Survival of Bylas and Sharp fluke, with 42.6% of fish tested moderately susceptible
samples (54.5%) was approximately 30% lower than that and 38.3% highly susceptible. Although it is difficult to
in the other two samples from Cienega Creek and compare susceptibility and mortality across various stud-
Monkey Spring (69.5%) although none of these differ- ies because of differences in protocols, particularly the
ences was significantly different. number and strain of flukes used to initiate infection, it
In addition, MHC heterozygotes appeared to have appears that Gila topminnows suffer relatively high mor-
higher resistance (although non-significant) to the flukes tality from such infection. For example, although Leberg
than do MHC homozygotes in all three polymorphic & Vrijenhoek (1994) monitored their topminnows for
populations. Overall, MHC heterozygotes had an only 9 days, when their fish were inoculated with two
approximately 15% higher survival than MHC homozy- parasites only five (13.2%) were moderately susceptible
gotes. We cannot tell whether this effect is the result of and only two (5.2%) highly susceptible.
the MHC gene that we examined or effects of loci sta- In several simple experiments, we showed Gila top-
tistically associated with the MHC locus. However, minnows can acquire the guppy fluke by casual contact
because we randomly drew these individuals from our with infected guppies and suffer significant subsequent
large raceway populations after about ten generations in mortality. This is contrary to earlier findings by Leberg
captivity, the likelihood of such statistical association is & Vrijenhoek (1994) in related topminnows in which
probably only significant for closely linked loci (Houle, they found a low rate of infection and no evidence of
1989; Savolainen & Hedrick, 1995). transmission by casual contact. For example, we placed
The strongest effect observed was a lower resistance, two fluke-infected guppies in a 10-gallon tank with 25
as measured by both fluke infection level and mortality, uninfected guppies, and after 2 weeks six topminnows
of inbred fish from Cienega Creek as compared to simul- were placed in the tank (a density of poeciliids in nature
taneous outbred Cienega control. Even though the sam- this high is not uncommon). After 3 more weeks two of
ple size for this experiment was lower than for the the topminnows were lightly infected with flukes, and
population study, the difference in mortality was statis- after another week two topminnows were dead. Both
tically significant. In this case, survival of the outbred dead topminnows were infected with flukes, one quite
fish was more than twice as high as that for the simul- heavily. Three days later another topminnow was dead,
taneous control. also infected by flukes. One of the three survivors was
Although there were differential effects between pop- infected while the other two living topminnows were not.
ulations and MHC genotypes, these effects did not reach Overall, four out of six topminnows were infected and
statistical significance. As a result, it is important to three died, suggesting flukes may present a strong selec-
determine sample sizes that would have been necessary tive pressure on natural populations of topminnows in
to statistically detect the level of effect found with our contact with fluke-infected guppies.
experimental design. For the population study, for sta- In mammals, all major genes in the MHC appear to
tistical significance (P < 0.05) for the level of hetero- be clustered in one relatively small linkage group
geneity that we observed, the total sample would have (Edwards & Hedrick, 1998). However, in fishes, the
to have been 308, or 77 fish per population, instead of class I MHC genes (primarily involved in recognition of
the 164 total fish that we used. For MHC heterozygotes intracellular pathogens, such as viruses) and the class II
versus homozygotes, a sample size of 375 would have MHC genes, as the one that we investigated (primarily
been necessary rather than the 118 that we assayed involved in recognition of extracellular parasites, such
(assuming the same proportions of heterozygotes and as bacteria), are unlinked (Sato et al., 2000). Even the
class II genes in fishes appear to be in at least two link-
Table 4. The mean (± standard error) and medium number of flukes age groups (Bingulac-Popovic et al., 1997; McConnell
on fish that had flukes for the inbred sample and the simultaneous et al., 1998) spread out over more than ten map units in
outbred control from Cienega Creek at 5-day intervals (N is the sam- cichlids (Malaga-Trillo et al., 1998) and 30 map units
ple number of fish). – indicates that there were no fish with flukes in sticklebacks (Sato et al., 2000). Relevant to our find-
Number of flukes on day ings of only a 15% difference in survival between MHC
Population Measure 5 10 15 20 25
heterozygotes and homozygotes is that genes unlinked
to the class II locus we examined, or linked but in link-
Inbred Mean 5.5 ± 1.5 12.3 ± 3.1 29.8 ± 9.1 35.3 ± 14.7 50
Medium 6.5 12 30 50 50
age equilibrium with the class II locus, may influence
N 8 7 5 3 1 parasite resistance. As a result, the signal from examin-
Outbred Mean 4.9 ± 0.9 5.9 ± 2.3 3.3 ± 1.2 – – ing MHC genetic variation at a single gene influencing
Medium 5 3 4 – – parasite resistance would be expected to be less in fish
N 11 9 3 – –
than in mammals because of the lower level of linkage
108 P. W. HEDRICK ET AL.
disequilibrium expected. Even so we did find a trend in Acknowledgements
the effect of MHC heterozygotes having a higher para-
We thank Helen Rodd for providing the stock of flukes
site resistance than MHC homozygotes.
from Davis, CA. We appreciate support for this research
This study provides further evidence that inbred ani-
from the National Science Foundation, Arizona Heritage
mals may have lowered parasite resistance. In our study,
Fund, Bureau of Reclamation and Ullman Distinguished
the inbred line had undergone seven generations of
Professorship. We also appreciate comments on the man-
brother–sister mating, had an inbreeding coefficient of
uscript from W. L. Minckley and two anonymous
greater than 0.7, and was fixed for allele Pooc 1 (Hedrick
reviewers and assistance from Richard Fredrickson in
& Parker, 1998). Although the line had no noticeable
producing the figures. This research was carried out
loss of fitness for several other traits (Sheffer et al.,
using appropriate US Fish and Wildlife Service and
1999), it apparently had become susceptible to fluke
Arizona Department of Game and Fish permits.
infection. Lyles (1990) also found inbred guppies had
increased susceptibility to infection by the same fluke
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