Local adaptation and embryonic plasticity affect antipredator traits in hatchling pond snails

Abstract

SUMMARY1. The biology of induced defences in very early life history stages is poorly understood in freshwater invertebrates, but may be equally, if not more, important than later stages in influencing population dynamics and survival. Here, we investigated how exposure of embryos of the pond snail Lymnaea stagnalis to predator kairomones altered traits associated with protection (crawl out behaviour and shell size) in hatchling snails. We also investigated whether levels of plasticity were influenced by habitat of origin by comparing reaction norms from sites with different levels of predation risk: three high risk (predatory fish present) and three low risk (predatory fish absent). 2. F2 embryos from snails from each population were exposed to kairomones from a predatory fish (Tinca tinca) or control conditions for their entire development up to the point of hatching. Their avoidance behaviour and size (spire height) were then measured 1 day and 7 days after hatching. 3. One day post-hatching, levels of predator avoidance, primarily time spent at the water line, were significantly greater in high-risk versus low-risk populations; however, avoidance was also increased in hatchling snails exposed to predator cues as embryos, compared with those developing in control conditions. Snails exposed to predator cues during development were smaller, and there was a strong negative relationship between size and avoidance behaviour, suggesting a trade-off or trait compensation between growth and behaviour. 4. At 7 days post-hatching, a similar pattern in avoidance behaviour was found, with increased avoidance in snails from high-risk habitats and in those exposed to predator kairomones during their development. The primary avoidance response switched to crawling above the waterline at 7 days post-hatching. There was no significant difference in shell size between treatments, suggesting that predator-exposed snails had exhibited 'catch-up' growth. This enhanced investment in growth between 1 day and 7 days post-hatching was positively correlated with elevated avoidance behaviour across treatment groups, demonstrating that snails switched to trait co-specialisation of defence traits. 5. During the first few days post-hatching, snails alter the type of avoidance behaviour and also the relationship between morphological and behavioural defence traits. The degree of expression of these defensive traits in hatchling snails is influenced by both their developmental environment and local adaptation to their predation habitat that may have large implications for survival.

Fear is the mother of invention: anuran embryos exposed to predator cues alter life-history traits, post-hatching behaviour, and neuronal activity patterns

“…In short, we documented an overall decline of ontogenetic effects on anti-predator behaviour during tadpole development, while ontogenetic effects on neuronal activity apparently persisted over time. Moreover, we never observed a difference in contextual behavioural plasticity according to embryonic kairomone treatment (Dalesman et al, 2015), while the contextual neuronal response was strongly modified by prenatal predator exposure. The decline of ontogenetic behavioural effects over time and the lack of a differential contextual behavioural response to predator cues according to embryonic treatment may be due to the fact that, unlike neural activity, the defensive behaviour should be continuously adjusted to the current level of predation risk.…”

“…This implies also a long-term neuronal memory of embryonic experiences. Although experienced individuals may improve survival chances (Mathis and Smith, 1993), growing a more efficient anti-predator response in early life, by, for example, increasing the neurotransmission between ORNs and MCs, may incur energetic costs, because deviations from the developmental norm impose trade-offs in resource allocation (Steiner and Van Buskirk, 2008;Callahan et al, 2008;Auld et al, 2010;Dalesman et al, 2015). Actually, we observed a significantly smaller body size in treated hatchlings than in their control siblings, though development stage at hatching was almost identical for both.…”

Challenges and opportunities in developmental integrative physiology

“…This demonstrates that using an event sequence-based approach to select a functional trait shows potential for investigating the evolutionary role of heterokairy. The substantial knowledge of the adaptive importance of crawling post-hatching in this clade of freshwater snails, including local adaptation in this trait (Dalesman et al, 2009, 2015), alongside its importance in heterochrony (Smirthwaite et al, 2007) and heterokairy (Rundle et al, 2011) add further to the utility of this group of invertebrates for studying event timing.…”

The effects of embryonic experience with predation risk vary across a wave exposure gradient

“…, Dalesman et al. ) and continue to impact prey performance, both positively and negatively, throughout ontogeny (Relyea , Orizaola and Braña ). For example, red‐eyed tree frogs emerge earlier and smaller from development when they are exposed to egg predators (Touchon et al.…”