Blackwell Publishing LtdOxford, UKBIJBiological Journal of the Linnean Society0024-40662007 The Linnean Society of London? 2007
914
711718
Original Articles
GEOGRAPHIC PARTHENOGENESIS IN A FRESHWATER SNAIL
F. BEN-AMI and J. HELLER
Biological Journal of the Linnean Society, 2007, 91, 711–718. With 2 figures
Temporal patterns of geographic parthenogenesis in a
freshwater snail
FRIDA BEN-AMI* and JOSEPH HELLER
Department of Evolution, Systematics and Ecology, The Hebrew University, Jerusalem 91904, Israel
Received 17 March 2006; accepted for publication 4 November 2006
Geographic parthenogenesis describes the observation that parthenogenetic organisms tend to occupy environments
different from those of their close, sexually reproducing relatives. These environments are often described as extreme
or disturbed habitats. We examined whether patterns of geographical parthenogenesis persist over time, by conducting a 3-year life-history survey and comparing two very proximate habitats of the freshwater snail Melanoides
tuberculata: Nahal Arugot, a desert stream naturally disturbed by flash floods, and Or Ilan, a stable freshwater pond.
Both sites occur in a xeric environment and are subject to otherwise similar biotic (e.g. parasites, predators) and
climatic conditions. In the stable habitat, male frequencies and snail densities were significantly higher than in the
disturbed one, whereas infection levels, mean embryo counts, and water temperatures were similar at both sites.
Additionally, male frequencies declined after density decreased, thereby providing evidence for geographical parthenogenesis via reproductive assurance. Infection prevalence was very low regardless of reproduction mode.
Although further genetic work is required, the apparent metapopulation structure of M. tuberculata in the Judean
desert may be suitable for evaluating other possible explanations of geographical parthenogenesis. © 2007 The
Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 711–718.
ADDITIONAL KEYWORDS: flash flood – Melanoides tuberculata – recolonization – reproductive assurance.
INTRODUCTION
Geographic parthenogenesis describes the observation
that parthenogenetic organisms tend to occupy ranges
different from those of their close, sexually reproducing relatives. Asexuals tend to have more northerly
distributions, or occur at higher altitudes, on islands,
in xeric environments, or in disturbed habitats
(Vandel, 1928; Ghiselin, 1974; Cuellar, 1977; Glesener
& Tilman, 1978; Lynch, 1984). Evidence supporting
geographical parthenogenesis has been found in
plants (O’Connell & Eckert, 2001; Verduijn, Van Dijk
& Van Damme, 2004), insects (Niklasson & Parker,
1994; Kramer & Templeton, 2001; Jensen et al., 2002;
Law & Crespi, 2002; Knebelsberger & Bohn, 2003),
worms (Christensen, Hvilsom & Pedersen, 1992), and
lizards (Moritz, 1991; Kearney et al., 2003), but see
also Palmer & Norton (1991) and Bloszyk et al. (2004).
*Corresponding author. Current address: Zoologisches Institut
Evolutionsbiologie, Universität Basel, Vesalgasse 1, 4051
Basel, Switzerland. E-mail: [email protected]
Several non-exclusive hypotheses have been proposed to explain the observed patterns of geographical
parthenogenesis (Kearney, 2005). Among these explanations are the existence of relatively few biotic interactions in sparse habitats, thereby minimizing the
advantages of sexual over asexual reproduction in the
coevolutionary arms races with parasites and predators (Levin, 1975; Glesener & Tilman, 1978; Jaenike,
1978; Hamilton, 1980; Bell, 1982; Hamilton, Axelrod
& Tanese, 1990); the ability of an asexual mutant arising from a sexual population to ‘freeze’ the phenotypic
niche of the sexual individual from which it mutated
(frozen-niche variation; Vrijenhoek, 1979); the difficulties of sexuals in finding a mate in marginal or
disturbed habitats (reproductive assurance; Stalker,
1956; Gerritsen, 1980; Barrett & Richardson, 1986);
and the innate advantage of asexuals from marginal
habitats to genetically isolate themselves from nonadapted sexuals migrating from core habitats (Peck,
Yearsley & Waxman, 1998).
During colonizing stages parthenogenesis is the
most favourable mode of reproduction because a single
© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 711–718
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F. BEN-AMI and J. HELLER
female can establish a new population (Gerritsen,
1980; Bell, 1982). Genetic bottlenecks, resulting from
recolonization events, cause genetic drift in both asexual and sexual organisms. However, in sexuals subject
to genetic drift, the reduction in fitness is higher due
to increased homozygosity and subsequent inbreeding depression (Charlesworth & Charlesworth, 1987).
Haag & Ebert (2004) proposed recently that, in
marginal habitats, where population structure often
resembles a metapopulation with increased subdivision and frequent local extinction and recolonization,
the contradictory effects of inbreeding depression
(following founder bottlenecks) and heterosis
(increase of fitness of sexuals as a result of hybridization with immigrants; Whitlock, Ingvarsson & Hatfield, 2000; Ebert et al., 2002) may ultimately favour
asexuals over sexuals.
Flash floods are a typical cause of a local extinction
event in semidry habitats. In desert streams, they are
characteristically sudden, short and have extensive
physical and biological impacts, causing great mortality in animal populations and removing large amounts
of detritus (John, 1964; Fisher et al., 1982). These
unpredictable and very local mass mortality events
stress the importance of recolonization mechanisms (Lytle, 2000) and the recovery from extreme
bottlenecks.
As its name implies, most of the empirical evidence
supporting geographical parthenogenesis is spatial in
nature (Lynch, 1984; Parker, 2002). More specifically,
demographic data (from variable habitats) coupled
with life-history or genetic information (about reproduction mode) are often collected in discrete points in
time and their distributions are then analysed.
Although such analyses provide valuable information,
differences in environmental factors (i.e. xeric vs.
sparse vs. disturbed habitat) and biotic effects (e.g.
parasites, predators) may obscure the relationship
between geography and reproduction mode. Furthermore, long-term studies of habitats with similar
environmental or biotic conditions, which may reduce
outlier effects, have rarely been conducted.
The present study aimed to examine whether
geographical parthenogenesis persists over time in
natural populations of Melanoides tuberculata , by
investigating how sexuality levels and snail densities
vary over time as a result of disturbances (e.g. flash
floods). We selected two very proximate habitats in the
Judean desert, near the Dead Sea: Nahal Arugot, a
desert stream naturally disturbed by flash floods, and
Or Ilan, a stable freshwater pond. Both sites occur in
a xeric environment and are subject to otherwise similar biotic and climatic conditions. We confined our
analyses to these specific populations because we are
unaware of other Melanoides habitats in Israel that
differ solely by their disturbance levels and not, for
example, by other biotic factors such as predators
and parasites. At the same time, we recorded biotic
(e.g. trematode prevalence, embryo counts) and abiotic
(e.g. temperature) parameters to test whether these
factors influence sexuality levels within a habitat or
vary between habitats over time.
The study organism is the freshwater gastropod
M. tuberculata (Müller, 1774; Thiaridae), which ranges
widely from northern and eastern Africa to southern
Asia (Neck, 1985). It is typically found in warm temperate to tropical freshwater bodies (Murray, 1971;
Livshits & Fishelson, 1983; Dudgeon, 1986), in shallow
slow running water, and on soft mud and sand substrata, where it primarily feeds on benthic microalgae
(Roessler, Beardsley & Tabb, 1977), fine detritus, epiphytic algae, and decaying plants (Madsen, 1992). In
detritus-rich conditions (silt behind overhanging stems
and protruding roots of bank vegetation), M. tuberculata can reach high densities (2700 snails m−2, Dundee
& Paine, 1977; 37 500 snails m−2, Roessler et al., 1977).
It is also found in deep zones of freshwater pools
(3–3.7 m) where the substrates are composed largely of
rocks (Murray, 1975).
Most populations reproduce via apomictic parthenogenesis (Jacob, 1957, 1958; Berry & Kadri, 1974) but
evidence of sexual reproduction has been found in
Israel (Livshits & Fishelson, 1983) and in Martinique
(Samadi et al., 1999). Males have ripe gonads and
motile sperm (Hodgson & Heller, 1990) and male frequencies reach up to 66% in Israel (Livshits & Fishelson, 1983; Heller & Farstey, 1990; Ben-Ami & Heller,
2005). Heller & Farstey (1990) argued that a higher
frequency of fertile males, combined with the higher
genetic diversity of bisexual populations (Livshits,
Fishelson & Wise, 1984), is indicative of sexual
reproduction.
Melanoides tuberculata is ovoviviparous. The eggs,
which are small (50 × 70 μm; Berry & Kadri, 1974),
contain large amounts of glycogen and protein yolk
(Hodgson, Ben-Ami & Heller, 2002). They develop in
the cephalic brood pouch of the female, from where
juveniles are released. Energy for embryonic development may in part be derived from sibling cannibalism
(Berry & Kadri, 1974; Dudgeon, 1986) or from the
mother, although the general absence of secretory cells
suggests that embryos derive little nutrition from the
mother (Ben-Ami & Hodgson, 2005). Embryo numbers
reach up to 71 embryos per snail (Berry & Kadri, 1974;
Livshits & Fishelson, 1983). The length of embryo
incubation is negatively correlated with population
density (Livshits & Fishelson, 1983).
MATERIAL AND METHODS
Nahal Arugot is a desert stream running to the
Dead Sea (−120 m a.s.l.; 31°27′N, 35°22′E). Although
© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 711–718
GEOGRAPHIC PARTHENOGENESIS IN A FRESHWATER SNAIL
annual rainfall is relatively low, seasonal flash floods
normally occur once or twice per year and often wipe
out the entire flora and fauna within hours, sweeping
boulders and sediments, and uprooting much of the
vegetation. Or Ilan is a stable freshwater pond
located 2.3 km north of Nahal Arugot (−202 m a.s.l.;
31°27′N, 35°22′E). Climatic conditions are similar to
those in Nahal Arugot (F. Ben-Ami & J. Heller, pers.
observ.).
Both populations were sampled bi-monthly over a
3-year period (Nahal Arugot: February 1999 to February 2002; Or Ilan: September 1998 to November
2001). In each sampling, all snails found within 15
random squares (20 × 20 cm) were collected and measured, to an accuracy of 0.01 mm. Snails were sexed
by holding an intact snail up to a strong light (i.e. the
colour of the gonads allows distinguishing males from
females; Heller & Farstey, 1989). Most snails were
returned to the spot within 2 h. However, to estimate
reproduction rates as suggested by Berry & Kadri
(1974), 20–40 randomly chosen individuals were
transported alive to the laboratory, where the number
of embryos in the brood pouch was counted. Additionally, trematode infection (by Centrocestus sp.; BenAmi & Heller, 2005) was determined by examining
the gonad and digestive gland under a light microscope. On several occasions, especially after a major
flash flood, we found only very few live specimens.
In such cases, snails were only measured and sexed,
upon which they were immediately returned to the
spot to minimize interference with population dynamics. Furthermore, because we could not estimate the
proportion of males in samples where snail density
was zero, these data points were excluded from the
analysis and degrees of freedom were adjusted
accordingly.
Statistical analysis was performed using SPSS for
Windows, version 12.0.2. Data are means ± SD and
probabilities are two-tailed. Frequency data were arcsine (square root)-transformed and mean data were
log-transformed before analysis. To examine withinhabitat correlations, all data were tested for departure from normality using Shapiro–Wilks’ W-test
and, when necessary, nonparametric tests were
employed. Additionally, when comparing male frequencies, snail densities, embryo counts, and water
temperatures between the two habitats, we verified
the equality of variances assumption using Levene’s
test of homogeneity of variances. However, the temporal nature of our data implies that the observations
are not independent, with the possible autocorrelation of residuals. Therefore, we chose a mixed analysis of variance model with restricted maximum
likelihood estimation, instead of the traditional
general linear model, to perform between-habitat
comparisons.
713
RESULTS
In Nahal Arugot, the study began after a 1-year
drought without any floods, and the stream was
undisturbed in terms of flood effects. The frequency
of M. tuberculata males varied between 0–15.9%
during the survey, with a mean of 7.2 ± 6.1% males
per sample (Fig. 1A). Snail densities reached up to
44.6 snails per sampling square in October 1999
(equivalent to 1115 snails m−2), with a mean of
10.3 ± 13.3 snails per sampling square (Fig. 1A).
However, during the survey a total of six flash floods
occurred. Densities were always low after flash
floods, driving the population almost to extinction in
October 2000 (the population recovered only after a
year) and December 2001 (Fig. 1A). Infected snails
were found only in the samples from October 1999
(3.3%) and December 1999 (3.9%). This infection
peak coincided with a peak in host density (Fig. 1A).
Mean embryo counts varied between 0 and 6.0
embryos throughout the survey, with a mean of
2.8 ± 1.8 embryos per female (Fig. 2). Water temperatures were in the range 21.5–32.0 °C
(mean = 25.7 ± 3.3 °C).
Across samples, in Nahal Arugot, male frequencies
were not significantly correlated with snail densities
(Spearman rho = 0.432; N = 10; P = 0.213). A higher,
though still nonsignificant correlation, was found
between male frequencies and snail densities in
the previous sample (Spearman rho = 0.600; N = 9;
P = 0.088). Mean embryo counts were neither correlated with male frequencies (Spearman rho = −0.302;
N = 10; P = 0.397), nor with snail densities (Spearman
rho = 0.219; N = 10; P = 0.544). Furthermore, there
were no correlations between water temperatures and
male frequencies, snail densities, and mean embryo
counts.
In Or Ilan, male frequencies varied between 10.8–
36.6%, with a mean of 25.3 ± 6.4% males per sample
(Fig. 1B). Snail densities during the same period
reached up to 263.0 snails per sampling square in July
1999 (equivalent to 6575 snails m−2), with a mean of
117.7 ± 76.0 snails per sampling square (Fig. 1B).
Infected snails were found only once in September
2001 (2.5%; Fig. 1B). Mean embryo counts varied
between 1.4 and 6.9 embryos throughout the survey,
with a mean of 3.1 ± 1.6 embryos per female (Fig. 2).
Water temperatures were in the range 20.0–30.0 °C
(mean = 25.1 °C ± 2.9 °C).
Across samples, in Or Ilan, male frequencies
were significantly correlated with snail densities
within the same sample (Pearson r = 0.632; N = 19;
P < 0.01), and with densities in the previous sample
(Pearson r = 0.729; N = 18; P < 0.001) and two samples before (Pearson r = 0.557; N = 17; P < 0.05).
These P-values remained significant after applying
© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 711–718
714
F. BEN-AMI and J. HELLER
A
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Percentage males
Trematode prevalence
Snail density
Figure 1. A, percentage males, trematode prevalence, and snail density in Nahal Arugot. The occurrence of a flash flood
is marked by an arrow. The samples for October 2000 and December 2001 were taken immediately after a flash flood. The
percentage of males at June 2000, August 2000 and October 2001 were zero. B, percentage males, trematode prevalence,
and snail density in Or Ilan.
Number of embryos
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Nahal Arugot
Or Ilan
Figure 2. Mean embryo counts in Nahal Arugot and Or Ilan.
© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 711–718
GEOGRAPHIC PARTHENOGENESIS IN A FRESHWATER SNAIL
the sharpened Benjamini and Hochberg false discovery rate adjustment for multiple comparisons
(Verhoeven, Simonsen & McIntyre, 2005). Mean
embryo counts were not correlated with male frequencies (Pearson r = −0.034; N = 19; P = 0.889), but
tended to correlate negatively with snail densities
(Pearson r = −0.446; N = 19; P = 0.056). Once again,
there were no correlations between water temperatures and male frequencies, snail densities, and
mean embryo counts.
Male frequencies were significantly lower in Nahal
Arugot than in Or Ilan (mixed model: F = 42.31;
d.f. = 27; P < 0.001), and so were snail densities (mixed
model: F = 45.61; d.f. = 27; P < 0.001). However, neither mean embryo counts differed among habitats
(mixed model: F = 0.52; d.f. = 27; P = 0.477), nor did
water temperatures (mixed model: F = 1.26; d.f. = 27;
P = 0.271).
DISCUSSION
Observations on geographical parthenogenesis found
that asexuals prevail in xeric, sparse, or disturbed
habitats, whereas sexuals predominate in stable environments or in habitats where biotic interactions are
common. In the present study, we examined such a
pattern on a local scale (i.e. two sites), but with
repeated samples over time, to control for environmental and biotic effects. Over 3 years, we followed
two populations that differ in their frequency of disturbance, yet are subject to otherwise similar climatic
and biotic conditions. Our findings are consistent with
the known correlates for geographical parthenogenesis (i.e. we found that the more disturbed habitat has
lower levels of sexuality).
In Nahal Arugot, the disturbed habitat, male frequencies and snail densities were significantly lower
than in Or Ilan, our stable habitat. In both habitats,
male frequencies declined following a decrease in density levels, as predicted by reproductive assurance.
Mean embryo counts did not differ among the habitats, although they were negatively but insignificantly
correlated with male frequencies (Ben-Ami & Heller,
2005). Infection prevalence and water temperatures
were similar at both sites and neither correlated with
male frequencies, nor with snail densities, suggesting
that these biotic and abiotic factors do not influence
sexuality strongly. The observed correlations between
snail densities and male frequencies within each of
the populations, as well as between populations, suggest that this correlation is rather robust, and may not
simply be a chance observation caused by the low
number of populations in this study.
At both sites, mean embryo counts were relatively
low, reaching a maximum of 13 embryos per female in
715
Nahal Arugot and 19 embryos per female in Or Ilan,
compared to 71 embryos per female in Malaysia
(Berry & Kadri, 1974) and 49 embryos per female
in the Mediterranean regions of Israel (Livshits &
Fishelson, 1983). This low number of embryos suggests that torrential desert streams and ponds may
not be optimal habitats for M. tuberculata. Given that
average snail densities in Or Ilan were more than tenfold higher than in Nahal Arugot, the statistically
equivalent mean embryo counts at both sites may suggest that the nutritional resources available per snail
were similar in both habitats. Hence, disturbance by
flash floods may indeed be the most differentiating
factor between the two habitats.
The observed male frequencies may be the product
of other independent processes, such as sex differential mortality, sex ratio adaptation, and age structure
effects. For example, males may be more prone to flash
floods caused mortality because they search for mates,
whereas females may hide in crevices. Nevertheless,
we are unaware of any study describing differential
male vs. female mortality resulting from mating
behaviour in freshwater snails. Males may be more
susceptible to parasites and predators than females.
However, during the study period, we rarely found any
parasites in both habitats. There were also no specific
molluscivores in either site; hence the predation pressure appears to be low. We are unaware of any evidence of sex-biased predation in freshwater snails,
especially in M. tuberculata where there is no visible
difference between males and females (Brande et al.,
1996).
Age structure effects, such as differential survival of
male vs. female juveniles, may also alter the sex ratio
within each habitat. These effects may be caused by
additional environmental and biotic factors, including
within- and between-species competition, predation,
and parasitism. Hence, the proportion of males surviving to a certain age and their survival curves by
themselves may account for the sex ratio variation, via
intrinsic or extrinsic sources. Notwithstanding, these
two sites were chosen due to their relative biotic and
climatic similarity, and thus we have no reason to
assume that there is sex differential juvenile survival
between the habitats. Furthermore, even though factors such as temperature, day length, or food availability may also cause sex ratio variation (Bull, 1983),
these factors do not appear to differ significantly
between the sites.
Despite the relative proximity of the habitats, gene
flow between populations is limited to random dispersal by birds or mammals such as the ibex and the
hyrax (F. Ben-Ami & J. Heller, pers. observ.), due to the
low vagility of adult M. tuberculata and the lack of
effective dispersal stages (Myers, Meyer & Resh, 2000).
Hence, the population structure in Nahal Arugot and
© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 711–718
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F. BEN-AMI and J. HELLER
Or Ilan may be similar to that of a marginal habitat,
resembling a metapopulation with increased subdivision and frequent local extinction and recolonization,
as envisioned by Haag & Ebert (2004).
Although classical observations of geographical parthenogenesis were based upon either entirely asexual
or sexual populations, current views of geographical
parthenogenesis (Haag & Ebert, 2004) consider a
spectrum of sexuality levels, ranging from purely
asexual, via mixed populations, and up to entirely sexual habitats. The present study of two mixed populations, with different levels of sexuality, appears to
support geographical parthenogenesis via reproductive assurance on the one hand but, on the other hand,
the existence of few biotic interactions, as is evident
from the low infection levels in both habitats, does not
corroborate geographical parthenogenesis via coevolutionary host–parasite interactions. A larger selection
of disturbed and stable M. tuberculata habitats from
geographically diverse locations may provide greater
statistical power and thus stronger inference on the
long-term relationship between sexual reproduction
and disturbed habitats. Additionally, detailed genetic
studies may assess the actual population structure of
M. tuberculata in the Judean desert and provide further clues as to the forces driving sexual vs. asexual
reproduction. Such information may also allow the
evaluation of other possible explanations for geographical parthenogenesis.
ACKNOWLEDGEMENTS
T. Benton and D. Ebert kindly criticized earlier versions of this manuscript. We are grateful to G. Horgan
for statistical advice, D. Wiener for assistance during
the sampling, the Nahal Arugot Nature Reserve and
Ein Gedi Field School for their generous hospitality,
and two anonymous reviewers for useful comments.
Specimens for this study were collected under permit
6094 from the Israeli Authority for Nature Reserves
and National Parks. This study was supported by a
Horwitz Foundation Fellowship to F.B.A.
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