4.0 DISCUSSION
L. intestinalis has 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; Carter et al., 2005; Cowx et al., 2008). We also found that the relative weight of gonads in relation to body size increased over the 10-year duration of this study, and observed a decline in somatic growth at maturity (from stage IV to stage V). These temporal changes were found in non-infected fish, which indicates that they may reflect evolutionary changes in the life history of E. sardella .
Organisms are selected for changes in life history traits when age-specific death or fecundity rates are changed (Forbes, 1993). In our study, we observed an overall 69% lower fecundity in infectedversus uninfected hosts, that is, the cestode L. intestinalis caused a significant partial castration in E. sardella . Reduced host fecundity is a common outcome associated with parasite infection (Hurd, 2001) and contribute to reduced host fitness (Gooderham and Schulte-Hostedde, 2011). Infected hosts may compensate for this fitness loss by shifting their life histories towards earlier reproduction (Jokela and Lively, 1995; Lafferty, 1993b). Many host species have been shown to increase their early reproductive output if their chances for future reproduction are reduced (Adamo, 1999; Minchella and Loverde, 1981).
Our observations of an increase in gonadal weight in relation to fish body size suggest that reproductive investment in E. sardella has increased at the expense of investment in somatic growth after reaching maturity. These findings are consistent with our prediction that their life histories should shift towards earlier reproduction. The fact that they come from an analysis of the non-infected fish indicates that this change is not a secondary effect of infection. More work is warranted, however, to determine whether it is caused by plastic or evolutionary responses.
A parasitic relationship between L. intestinalis and E. sardella in Lake Nyasa was 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). We believe this suggests that this tapeworm was likely absent from Lake Nyasa prior to the late 1990s. After the first observation, E. sardella in the lake kept being found infected byL. 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, where prevalence is estimated at 50%. This indicates that L. intestinalis has spread steadily, and therefore that selection caused by this parasite on its host has increased during the early years after introduction.
A shift towards investment in current reproduction has been reported in many other host-parasite systems, where infected hosts increased their reproductive effort before dying or being castrated by the parasite. 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 that Daphnia 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, induce life history changes in infected hosts, and that these plastic changes are adaptive.
Here we observe a shift towards increased reproductive effort at the expense of somatic growth across generations, in non-infected hosts. This pattern, which cannot be explained by plastic life history responses to infection, might reflect adaptation to recent selective 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. Other potential sources of selection for earlier reproduction include: fishing (Fenberg and Roy, 2008; Heino and Godø, 2002; Hutchings and Fraser, 2008; Jorgensen et al., 2007; Jørgensen et al., 2009; Kuparinen and Merilä, 2007; Sharpe and Hendry, 2009; Sharpe et al., 2012); increased predation by native or introduced species (Hampton et al., 2018; Sharpe et al., 2012); 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). Over the past decades, however, fishing effort catch rates have decreased in Wissman Bay, where the present study was conducted. (Figure S1).
Increased fishing effort has also been reported for other fish species than E. sardella in riparian countries around lake Nyasa such as Tanzania (Irvine et al., 2018; Irvine et al., 2002), Mozambique (Halafo et al., 2004; Irvine et al., 2018) and Malawi (Irvine et al., 2018; Weyl et al., 2010).
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 (Figure S2), which corresponds to mature fish (i.e. from stage IV and above). This suggests that the traditional E. sardellafishing practice is probably size-selective and induces a higher mortality in adults than younger fish. Interestingly, the number of tones landed per fisherman (which can be considered as representing stock density) dramatically decreased in 2013 (Figure S1), following three consecutive years with both high L. intestinalis prevalence (strongly reducing E. sardella fecundity) and sustained fishing effort (increased adult mortality) (Figure S1). Therefore, we argue that parasitism by L. intestinalis may have acted synergistically with fishery-mediated selection in driving what appears like an evolutionary shift towards earlier life history of E. 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 the abundance fluctuations of the natural predators ofE. sardella are lacking. Further research, particularly on the combined effects of parasitism, fishing, and natural predation onE. 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 concomitant increases in the prevalence of other parasites. In their naturally habitats hosts are usually infected by two or more different parasite species (Kotob et al., 2017; Petney and Andrews, 1998). To the best of our knowledge, the only other parasite that has been reported to infect E. sardellais the nematode Camallanus sp. (Mgwede and Msiska, 2018). In the present study, we caught 3,488 wild, i.e. naturally-infectedE. sardella , none of them observed with Camallanus 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 remains correlative, and more work is needed to examine the evolutionary nature of these changes. Yet the cestode L. intestinalis , by strongly reducing the fecundity of its host, appears as likely as fisheries to drive such evolution. Our study suggests that these two types of selective factors may have acted in synergy.