Development, lifespan and reproduction of spider mites exposed to predator-induced stress across generations

Abstract

Predator-induced stress shows pronounced effects on prey by inducing behavioural, morphological, and physiological responses. Increasing evidence shows that these antipredator responses may also lead to changes in life-history traits such as aging and lifespan. However, little is known about how predator cues influence the fitness of preys and their transgenerational effects. Parental spider mites (Tetranychus urticae) were either raised on a leaf disc with or without cues from a natural predator (Phytoseiulus persimilis). The results showed that predator cues prolonged the development of both sexes, shortened female adult lifespan but not that of males, and reduced lifetime reproductive outputs of the females. The studies with offspring from both cuesexposed and control mothers demonstrated that parental effects were significant in the early developmental stage of offspring, but not in later life stages. The lifespan of offspring was strongly negatively affected by the predator-induced stress when they were directly exposed but not the stress-experienced by their mothers. Additionally, the parental effects in the earlier life stage were sex-specific, with delayed hatching in daughters (but not sons) when parents were exposed to predator-induced stress. This crosstransgenerational study indicated that there were deleterious effects of predator-induced stress on aging and lifespan of prey for both parents and their offspring, although the parental effects appeared to be weak (in the early stage of offspring but diminished in adult stage). This study highlighted the sexdifference of prey in response to predator-induced stress and sex-dependent parental effects on the offspring.

Transgenerational Plasticity in the Context of Predator-Prey Interactions

“…Most traits (e.g., weight, body size, survival, cautiousness) did not show any sex-specific pattern: daughters and sons were equally affected by the parental environment (Coslovsky and Richner, 2011;Stein and Bell, 2014;Basso and Richner, 2015a,b;Hellmann et al, 2019) (pattern c in Figure 4). For the other traits, parental exposure influenced only one sex and not the other (patterns a and b in Figure 4: Coslovsky and Richner, 2011;Basso and Richner, 2015a;Hellmann et al, 2019;Li and Zhang, 2019). For instance, paternal exposure to predator-cues increased activity of sons but not daughters-this could be adaptive, as only males may benefit from higher activity under predation risk in sticklebacks.…”

“…No studies examined TGP expression only in the embryonic stage. To our knowledge, 14 studies (25%) explored TGP expression in response to predation risk at different times in offspring life, either within an offspring stage or among different stages (Tollrian, 1995;Agrawal et al, 1999;Sheriff et al, 2010;Richner, 2011, 2012;Giesing et al, 2011;Basso et al, 2014;Bestion et al, 2014;Stratmann and Taborsky, 2014;Basso and Richner, 2015a,b;St-Cyr and McGowan, 2015;Freinschlag and Schausberger, 2016;Li and Zhang, 2019). Screening these studies, different scenarios are observed (Figure 2).…”

“…Five studies described that parental experience with predation risk can influence offspring traits early in development, but the effect dissipates later in life. Two studies on spider mites (T. urticae) showed that maternal predation experience retarded offspring development in embryonic, larval and early juvenile stages, but the effect disappeared in the late juvenile stage and for reproductive parameters in adults (Freinschlag and Schausberger, 2016;Li and Zhang, 2019). In the same way, offspring of predator-exposed mothers were smaller and lighter during the early juvenile stage in great tits Richner, 2011, 2012;Basso and Richner, 2015a) and grew faster in an African cichlid (Stratmann and Taborsky, 2014), whereas no TGP of these traits was found later in the juvenile and adult stages for both models.…”

“…In the context of predator-induced TGP, sex-specific TGP at the offspring level has been investigated in seven studies: three on great tits (Coslovsky and Richner, 2011;Basso and Richner, 2015a,b), two on sticklebacks (Stein and Bell, 2014;Hellmann et al, 2019), one on spider mites (Li and Zhang, 2019) and one on mice (St-Cyr and McGowan, 2015). As at the parental level, sex-specific TGP patterns were highly dependent on offspring traits.…”

Aging as a consequence of selection to reduce the environmental risk of dying

“…Predator-induced stress (predation risk or the fear of becoming prey) has been shown to have pronounced effects on prey species by inducing behavioral, morphological, and physiological responses (30)(31)(32)(33). In two species of water fleas (Daphnia longispina and Diaphanosoma brachyurum) (34) and in parental spider mites (Tetranychus urticae) (35), it was recently shown that the physiological response to predator-induced stress mediated by predator cues caused pronounced effects on the aging pattern. Our life-history model does not incorporate such effects, as it implies that the rate of somatic damage accumulation may be under deliberate regulatory control driven by perceptual information and anticipatory inference (36).…”