1.0 INTRODUCTION
Life history theory assumes that there are trade-offs between different traits in organisms, such as growth, reproduction and survival (Roff, 2002). These traits cannot be simultaneously maximized within the same individual because the available amount of nutrients and other resources are in limited supply (Stearns, 1989). Increased resource allocation into one trait will, therefore, come at the cost of reduced allocation into other traits (Agnew et al., 2000). In each given environment, the optimal way to resolve these trade-offs (i.e., the optimal strategy for maximizing fitness) is the one achieving the highest possible reproductive success (Agnew et al., 2000; Pianka, 1976; Stearns, 1989). For instance, if adult mortality increases within a population (e.g., due to increased predation), individuals that mature relatively earlier and invest relatively more into current reproduction versus future survival will be favoured by natural selection (Fredensborg and Poulin, 2006).
For fish, both natural predation and fishing (i.e., predation by humans) are important selective factors that drive adaptive changes in life history traits such as developmental rates and timing of reproduction (Heino and Godø, 2002; Jorgensen et al., 2007; Jørgensen et al., 2009; Sharpe et al., 2012). Fishing practices and predation are usually non-random factors, as gears are often designed to selectively take larger and older fish in the population (Law, 2000). In this case, smaller fish are likely to have a higher probability of survival than the larger ones, and among them, those that can mature and reproduce early will be selected favourably. Assuming that early maturation is heritable to some extent, this should result in life histories changing towards earlier reproduction at smaller sizes.
Parasitism can also affect the future reproductive success of hosts (Fredensborg and Poulin, 2006) and thus select for changes in host life history traits (Adamo, 1999; Agnew et al., 1999; Lafferty, 1993b; McCurdy et al., 1999; Perrin et al., 1996; Polak and Starmer, 1998; Richner and Tripet, 1999; Sorci et al., 1996; Thomas et al., 2000; Yan et al., 1997). For instance, an increase in the prevalence of parasites causing castration (i.e., destruction or alteration of the host’s gonadal tissues by the parasite; (Noble and Noble, 1971)) (Fredensborg and Poulin, 2006; Lafferty, 1993a; Loot et al., 2002; Minchella and Loverde, 1981) can select for earlier maturity. For the infected host, achieving reproduction prior to castration yields clear fitness benefits (Gooderham and Schulte-Hostedde, 2011; Lafferty, 1993a; Minchella and Loverde, 1981), and these benefits increase along with infection risk (Minchella and Loverde, 1981; Polak and Starmer, 1998; Sorci et al., 1996). Increased reproductive effort in hosts exposed to castrating parasites has been reported in a number of species. So far, however, most documented life history changes seem to result from adaptive plastic responses of hosts to parasitic exposure, more than life history evolution following a change in parasite-mediated selection (Chadwick and Little, 2005; Hudson et al., 2019; Vale and Little, 2012).
Ligula intestinalis (L. 1758) is a common and widespread cestode, that use cyprinid fish as intermediate hosts (Dubinina, 1980). In Lake Nyasa this cestode has been increasingly reported since it was first noted by Mwambungu et al. (1996), where it infects the endemic pelagic fish Engraulicypris sardella (Figure 1) (Gabagambi et al., 2019; Gabagambi and Skorping, 2018; Msafiri et al., 2014; Rusuwa et al., 2014). L. intestinalis is known to induce castration in several intermediate hosts (Cowx et al., 2008; Hoole et al., 2010; Kennedy et al., 2001; Loot et al., 2002; Wyatt and Kennedy, 1988) and has therefore been suggested to cause population crashes of its host (Burrough et al., 1979; Kennedy et al., 2001). This could sometimes lead to local extinction of the parasite in small ecosystems (Kennedy et al., 2001). Recent results, however, indicate that local extinction of this parasite is unlikely in Lake Nyasa due to spatial and temporal variations in transmission rates (Gabagambi and Skorping, 2018).
Under such conditions of recent parasite invasion, we hypothesize that the cestode L. intestinalis should select for a shift in resource investment from somatic growth towards reproduction in its intermediate fish host E. sardella . Using data collected from 2005 to 2013 and then in 2015 in the northern part of Lake Nyasa, we address the following three questions:
(i) What are the effects of L. intestinalis on the fecundity ofE. sardella ? (ii) has reproductive investment at maturity ofE. sardella increased over time? and (iii) has the average size at maturity of E. sardella decreased since the parasite was first identified in the lake?
We then further discuss the selective roles of parasitic invasionversus other environmental factors that may recently have changed in Lake Nyasa.