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, as manifested by the work of J. K. Kihedu (MSc thesis, Sokoine University of Agriculture, Tanzania, 2006, unpublished data).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.