Since the host represents the whole nutritional and physiological environment during immature development of the parasitoid (Colinet et al., 2005), the parasitoid itself may need to alter or modify host physiology and/or development to optimise its own fitness. In such a control of the host physiology by the parasitoid, the host has to adapt its defence and must involve avoidance of parasitism either by escaping detection or through preventing oviposition (Kraaijeveld & Godfray, 2003). This present study examined the impact of V. canescens attacks on P. interpunctella's fitness and following the host response to prevent further parasitism.
Impact of parasitism on the host life-history traits
Our results showed a large impact of parasitism by V. canescens on life-history traits in P. interpunctella. Larval size of the parasitised population increased after the wasp's oviposition of the third and fourth larval instars, and then the growth rate decreased when parasitised individuals significantly reached a smaller size in the last larval instar (L5).
The decrease of the growth rate observed between L3 and L5 parasitised instars in P. interpunctella, is commonly found in other host–parasitoid systems (Thompson, 1982; Slansky, 1986) where growth rates are more severely reduced in later host instars.
Although many larval endoparasitoids adjust their development to certain host endocrine events (Beckage, 1985) following a ‘conformer’ strategy (synchronisation of the parasitoid larval moults, destructive feeding, and emergence on the host larval development) (Lawrence, 1986; Harvey, 1996), the degree of host growth reduction between different instars of P. interpunctella is evidence that parasitism is also disrupting or directing selected host biochemical processes (Vinson & Barras, 1970; Iwantsch & Smilowitz, 1975; Vinson & Iwantsch, 1980; Harvey et al., 1994).
Slansky (1986) and Vinson (1988) argue that parasitoid-mediated changes in host development and physiology increase host quality by reducing constraints, and are therefore beneficial to parasitoid fitness (see Harvey et al., 1999). The amount of resources for parasitoid growth and development are not fixed and parasitoid development depends largely upon feeding rate and capacity for growth during the interaction (Godfray, 1994; Harvey & Thompson, 1995). Therefore, a redirection of host metabolic pathways to shuttle nutrients preferentially to the parasitoids may thus be involved (Alleyne & Beckage, 1997). Indeed, in several koinobiont species, parasitism (mainly Hymenoptera Braconidae, Eulophidae, and Ichneumonidae) induces biochemical alterations in the host's haemolymph by using active agents, including polydnaviruses (PDVs) (Pennacchio & Strand, 2006), venom (Nakamatsu & Tanaka, 2003), and teratocytes (Nakamatsu et al., 2002), which are injected with the parasitoid's egg into the host. During oviposition, V. canescens does not inject such PDVs, but injects other virus-like particles (VLPs) with the parasitoid's egg into its hosts (Schmidt et al., 2005). This suppresses the host's immunity by inducing host haemocyte apoptosis, mainly of the granulocytes (Suzuki & Tanaka, 2006), preventing encapsulation. The effects of such particles on host growth and development are not fully understood, but Harvey (1996) suggests that such VLPs may regulate host physiology more subtly, in addition to the host immunity suppression.
Parasitoid larvae may also release secretions that facilitate host regulation/alteration (Harvey, 1996). In Braconid and Eulophid parasitoid species, these alterations affect host proteogenesis, glucogenesis, and lipogenesis (Bischof & Ortel, 1996; Thompson, 2001; Jervis et al., 2008). Such metabolic changes may also occur in P. interpunctella, which would explain the reduced growth rate in parasitised larvae, but some of these alterations will also be the result of selective tissue feeding by the parasitoid larva.
Simultaneously to the reduced growth rate, our results clearly showed a delay in the developmental time of the third and fourth larval instars in parasitised populations of P. interpunctella, whereas no difference with control population was recorded in the fifth larval instar. Other host–parasitoid studies showed that koinobiont parasitoids may directly or indirectly affect development time of their hosts (Harvey, 1996; Harvey et al., 1996; Berstein et al., 2002). Additionally, Alleyne and Beckage (1997) showed that the L4–L5 moult in parasitised tobacco hornworm (Manduca sexta) larvae that were parasitised at the fourth instar by Cotesia congregata, was delayed by about 24 h. In our study, the significant average delay was about 48 h in both third and fourth larval instars, but this delay disappears in the final larval instar (L5). Therefore, the point at which the parasitoid larva begins destructive feeding (host haemolymph and host tissue subsequently) strongly influences the final size of the adult parasitoid (which is highly correlated with its fertility–Harvey et al., 1994; Harvey & Thompson, 1995). When developing in small or suboptimal host instars, such as L3 and L4 larval instar in P. interpunctella, where there are insufficient resources to optimise parasitoid fitness, early destructive feeding may reduce the developmental time of the parasitoid, but also lead to a reduction in parasitoid adult size (Hemerik & Harvey, 1999). Alternatively, allowing the host to increase the larval development to compensate for the early parasitoid's feeding (haemolymph feeder) may reduce the host size losses and increase parasitoid size and fitness. Host developmental delay in Plodia–Venturia association seems to be a parasitoid-influenced impact on this host life-history trait to improve its own fitness. Such a pattern of development in Venturia suggests that the parasitoid also adopts a ‘regulator’ strategy (Harvey, 1996) by altering host development in order to increase its suitability for parasitoid development. Therefore, our results support the viewpoint of Vinson (1988) and Harvey (1996) that V. canescens may exhibit characteristics of both ‘conformer’ and ‘regulator’ strategies.
At emergence, P. interpunctella adults that successfully encapsulate the parasitoid larvae are smaller, and thus have a reduced fecundity (Mbata, 1985) compared to unparasitised individuals. These reductions in size and related fecundity showed the real cost to mounting of a successful immune response. This major encapsulation cost triggers a trade-off between host survival and fertility. It is interesting to note that Boots and Begon (1993, 1995) found similar results in P. interpunctella infected by its granulosis virus with a significant correlation between resistance to the virus and egg viability. For both cases, there is obviously a trade-off between immunity and other major components of the fitness such as fecundity, due to a resource re-allocation between these biological components.
Adaptive avoidance of parasitism by the host at the next generation
Our study also showed the adaptive response of P. interpunctella population (F1) after parasitisation by V. canescens. We focused on the life-history trait adaptations of this new generation that leads to an avoidance of V. canescens parasitism.
Our results showed that the growth rate of the F1 generation is not affected by the previous parasitism in F0. On the contrary, our results showed a significant reduced developmental time for the ‘resistant’ population in L2 and L3 (reduction about 34 and 22 h, respectively; reduction about 36 h in L4 without significance). Venturia wasps do not parasitise L1P. interpunctella instars. L2 instars could be parasitised but represent a considerable cost to both host and parasitoid due to the host death rate after parasitism, while L3 are very attractive for Venturia and provide a better chance for parasitism success (Sait et al., 1997).
These shortening larval periods of susceptible instars reduced exposure to parasitism. No significant difference was recorded between ‘resistant’ and control populations in L5, the less successful instar for parasitism. Indeed, Harvey et al. (1994) showed that parasitoid survivorship was highest in L3 and L4P. interpunctella hosts, with >90% successful emergence from these instars (85% in our study), but, on the other hand, these authors showed an increased parasitoid mortality to 16% in L5 hosts. In Drosophila–parasitoid pairings, it has been shown that the total number of host haemocytes present is correlated with the ability to encapsulate parasitic invaders (Eslin & Prevost, 1996) and is known to increase during larval development, when haemolymph volume increases (Alleyne & Wiedenmann, 2001). Thus, the number of haemocytes used in the immune response against parasitism is correlated with the global quantity of haemolymph. These could explain why the most successful encapsulation rate occurs when the host is parasitised in the largest instar L5, with enough haemocyte numbers per morphotype (morphotypes have different function in the encapsulation process) (Strand & Johnson, 1996). Consequently, later and bigger L4 and L5 represent the least susceptible larval instar, and the benefit of reducing parasitism in such a less-vulnerable stage may be reduced compared with the cost of such a reduced developmental time.
‘Resistant’ populations also showed a longer developmental time in the pupal instar; they spent on average 4 days more in the pupal instar than the control individuals. In Plodia–Venturia interaction, the koinobiont cannot parasitise the pupal stage of Plodia. An increase of the pupal duration may allow metabolic changes necessary to complete development without taking more risk of being parasitised. ‘Resistant’ adults emerged from these pupae had the same size, and then the same fertility as adults from control populations. This fact confirmed that reduced size and related fertility observed in survival of parasitised adults (F0: encapsulation) was due to the cost of mounting a successful immune response, but also that the host adaptation in F1 on their life-history traits to reduce and/or avoid parasitism risks (shortening of the susceptible instar and lengthening of the invulnerable host instars) has no visible cost in term of host fecundity.
Although there is an obvious impact of parasitism on Plodia populations due to the low encapsulation rate (due to the wasp-injected VLPs), surviving parasitism also shows important sublethal effects (growth rate, adult size related to fecundity) for host population due to the cost of encapsulation. This leads to important consequences for the dynamics of parasitised host populations. The most direct is that fecundity is reduced for survival individuals, which would reduce the host's innate capacity for population increase. However, the fact that ‘resistant’ offspring of the next generation reduced the developmental time of susceptible instars, is likely to decrease the probability that individuals will come into contact with parasitoids.
Natural enemies' interactions, as in the host–parasitoid system, affect the evolutionary trajectory of host populations. When the only alternative is the death of the host, the cost of mounting an immune response has to be paid. Such a cost is clearly visible on the host fecundity in Plodia–Venturia interaction. Adaptive answers have to be found in order to resist parasitism with a lower cost. We found that adaptations may occur on the development time to avoid the highest risk of parasitism without reducing the fecundity.