4.0 DISCUSSION
L. intestinalis had a strong negative effect on the fecundity of
its intermediate host, E. sardella . Such an effect, which was
also found in other fish host species, thus seems widespread throughout
the species range of this parasite (Barson and Marshall, 2003; Carteret al. , 2005; Cowx et al. , 2008). We also found that the
relative weight of gonads increased, while body size at maturity
decreased, over the 10-year duration of this study. These temporal
changes, found in non-infected fish, indicate that investment ofE. sardella into early reproduction has increased at the expense
of somatic growth.
This study took place a few years only after the arrival of L.
intestinalis in the lake. A parasitic relationship between L.
intestinalis and E. sardella in Lake Nyasa was indeed first
observed in 1996 (Mwambungu et al. , 1996). An earlier study
investigating the breeding biology and in particular examining the
ovaries of E. sardella between 1992 and 1994, did not report any
case of L. intestinalis infection (Thompson, 1996). This tapeworm
was thus likely absent from Lake Nyasa prior to the late 1990s. After
the first observation, E. sardella in the lake kept being found
infected by L. intestinalis , as manifested by the work of J. K.
Kihedu (MSc thesis, Sokoine University of Agriculture, Tanzania, 2006,
unpublished data). The earliest sampling year in our study is 2005, when
prevalence is estimated at 50% (Table 1). This indicates that L.
intestinalis had spread, and therefore that the selection caused by
this parasite on its host had increased steadily during the early years
after introduction. Our study remains correlative, yet given the timing
of the observed life history shift relative to the invasion of the lake
by L. intestinalis , it seems legitimate to consider parasitism as
a likely contributing factor.
In general, changes in age-specific mortality or fecundity rates lead to
changes in selection on life history traits. In our study, we observed
an overall 69% lower fecundity in infected versus uninfected
hosts, that is, the cestode L. intestinalis caused a significant
partial castration in E. sardella . Reduced host fecundity is a
common outcome of parasite infection (Hurd, 2001; Gooderham and
Schulte-Hostedde, 2011), but is especially severe for castrating
parasites. Castration selects for higher, earlier reproductive effort,
as those individuals that are able to reproduce before castration are
clearly favoured (Forbes, 1993). A number of host species have been
shown to increase their early reproductive effort when parasitism
reduces their chances for future reproduction (Minchella and Loverde,
1981; Lafferty, 1993b; Jokela and Lively, 1995; Adamo, 1999). This kind
of adaptive response can result from two distinct mechanisms, namely
plasticity or evolution, and distinguishing between the two can reveal
challenging.
Plastic life history shifts towards increased investment in early
reproduction in exposed and / or infected hosts have been reported for a
range of host-parasite systems. In insects, Polak and Starmer (1998)
observed that experimentally parasitized male Drosophila
nigrospiracula infected with a mite (Macrocheles subbadius )
lived shorter lives, but before dying they courted females significantly
more than non-parasitized controls. Further, Adamo (1999) observed that
female crickets (Acheta domesticus ) increased egg laying in
response to infection with the bacterium Serratia marcescens . In
snails, Minchella and Loverde (1981) and Thornhill et al. (1986)
observed an increase in reproductive output in female Biophalaria
glabrata parasitized by a castrating trematode Schistosoma
mansoni . In crustaceans, Chadwick and Little (2005) observed thatDaphnia magna infected with a microsporidian Glugoides
intestinalis shifted their life-history towards early reproduction. In
birds, Sanz et al. (2001) observed that female pied flycatchers
(Ficedula hypoleuca ) with hemoparasite infection initiated egg
laying earlier and laid larger clutches. In reptiles, Sorci et
al. (1996) observed that common lizards (Lacerta vivipara )
increased their reproductive investment after being infected with
haematozoans. More examples where reproduction is seen to increase with
the onset of infection have been reviewed in Schwanz (2008). Taken
together, these studies show that parasites, by affecting the future
reproductive success of their hosts, can induce plastic life history
changes in infected hosts that are adaptive.
Here we observe a shift towards increased reproductive effort at the
expense of somatic growth across generations. This pattern is found in
non-infected hosts and therefore cannot be explained by plastic
responses to infection. In addition, given the empirical evidence
available at this stage, plastic responses to exposure appear unlikely,
given the lack of clear correlation between yearly fluctuations in
prevalence and life history trends, as one would expect under such a
scenario. We therefore cannot exclude that our results may reflect
adaptation to recent changes in Lake Nyasa.
Importantly, increased parasite pressure may not be the only
environmental change that has taken place in Lake Nyasa over the last
couple of decades, and that might have triggered life history responses
in E. sardella . Other potential sources of selection for earlier
reproduction include: fishing (Heino and Godø, 2002; Jorgensen et
al. , 2007; Kuparinen and Merilä, 2007; Fenberg and Roy, 2008; Hutchings
and Fraser, 2008; Jørgensen et al. , 2009; Sharpe and Hendry,
2009; Sharpe et al. , 2012); increased predation by native or
introduced species (Sharpe et al. , 2012; Hampton et al. ,
2018); and fluctuations in zooplankton abundance that may induce earlier
maturation.
Most evidence of fishery-induced evolution comes from large, heavily
exploited fish population stocks (e.g., North Arctic cod) where
industrial fishing using trawlers has been in practice for many years.
On the contrary, the Lake Nyasa E. sardella fishery is mainly
traditional, operating in near-shore lake zones using paddled dugout
canoe crafts (Mwambungu and Ngatunga, 2001). In the last years of this
study, however, E. sardella stocks have collapsed, despite no
sudden changes in fishing effort. As a consequence fishing pressure has
dramatically increased in Wissman bay (Supplementary Figure S3).
In the present study, E. sardella were sampled using the
traditional fishing method. The majority of the sampled fish was
composed of individuals of the body sizes between 50-100 mm in length,
which corresponds to mature fish (i.e., from stage IV and above).
This suggests that the traditional E. sardella fishing practice
is probably size-selective and induces a higher mortality in adults than
younger fish, thus possibly reinforcing the selective effects of
parasitism. Interestingly, the dramatic decrease in landings in 2013 was
preceded by three consecutive years with high L. intestinalisprevalence (Supplementary Figure S3), further suggesting that parasitism
is a strong selective factor. In this system L. intestinalis may
have acted synergistically with fishery-mediated selection in driving
what appears like an evolutionary shift towards earlier reproduction ofE. sardella in Lake Nyasa.
Increased predation by native or introduced organisms could also be one
factor affecting selection on life history traits of E. sardella .
In the native cyprinid fish Rastrineobola argentea in Napoleon
Gulf of Lake Victoria, Sharpe et al. (2012) observed decreased
body size, maturation at smaller sizes and increased reproductive effort
in response to the introduced predator fish Lates niloticus .
However, in contrast to Lake Victoria and many other ancients lakes
where dozens of non-native species have been introduced over the past
decade (Hampton et al. , 2018), in Lake Nyasa no new introduced
predator for E. sardella has been reported so far. The primary
natural piscivorours predators of E. sardella in this lake are
the pelagic haplochromine cichlids from the genera Ramphochromis,
Diplotaxodon, and Copadichromis, as well as the larger cyprinidsOpsaridium microlepis and O. microcephalum . Increased
abundance of the native predators of E. sardella over time in the
lake could have selected for life history changes similar to those
observed here. Unfortunately, the area where the present study was
conducted is a data-poor region; the last pelagic ecosystem stock
assessment was conducted between 1991-1994 (Menz (1995). Recent time
series on abundance fluctuations of the natural predators of E.
sardella are lacking. Further research, particularly on the combined
effects of parasitism, fishing, and natural predation on E.
sardella in Lake Nyasa, would be highly valuable, given the ecological
and economical importance of this fish species.
Another factor that could have affected selection on the life history
traits of E. sardella in Lake Nyasa may be parallel increases in
the prevalence of other parasites. In their natural habitats hosts are
usually infected by two or more different parasite species (Petney and
Andrews, 1998; Kotob et al. , 2017). To the best of our knowledge,
the only other parasite that has been reported to infect E.
sardella is the nematode Camallanus sp. (Mgwede and Msiska,
2018). In the present study we caught 3,488 wild, i.e.,naturally-infected E. sardella , none of them observed withCamallanus sp. infection.
Overall, this study reveals that life history of E. sardella in
Lake Nyasa has been shifting, over a period corresponding to the
invasion of this lake by a castrating parasite. It is correlative, and
the causative links between parasitism and life history changes remain
to be established. Yet the cestode L. intestinalis , by strongly
reducing the fecundity of its host, appears as a likely driver of life
history evolution, similar in its effects to size-selective fisheries.
In Lake Nyasa these two types of selective factors may have acted
concomittantly. More work is now warranted to examine the origin of
these changes and determine whether they represent plastic or
evolutionary responses.