Predator-induced maternal effects determine adaptive antipredator behaviors via egg composition

Abstract

In high-risk environments with frequent predator encounters, efficient antipredator behavior is key to survival. Parental effects are a powerful mechanism to prepare offspring for coping with such environments, yet clear evidence for adaptive parental effects on offspring antipredator behaviors is missing. Rapid escape reflexes, or “C-start reflexes,” are a key adaptation in fish and amphibians to escape predator strikes. We hypothesized that mothers living in high-risk environments might induce faster C-start reflexes in offspring by modifying egg composition. Here, we show that offspring of the cichlid fish Neolamprologus pulcher developed faster C-start reflexes and were more risk averse if their parents had been exposed to cues of their most dangerous natural predator during egg production. This effect was mediated by differences in egg composition. Eggs of predator-exposed mothers were heavier with higher net protein content, and the resulting offspring were heavier and had lower igf-1 gene expression than control offspring shortly after hatching. Thus, changes in egg composition can relay multiple putative pathways by which mothers can influence adaptive antipredator behaviors such as faster escape reflexes.

Predator-induced transgenerational plasticity in animals: a meta-analysis

“…Increased growth rate and reaching adult size faster may confer advantages such as escaping gape-limited predators, or accelerating metamorphosis and escape of risky habitats (Dahl and Peckarsky 2003 ; Biro et al 2005 ; Urban 2007 ). Note, however, that whether production of large vs small offspring is viewed as adaptive from the parental and/or offspring perspective will depend on the species and the context; for example, producing offspring larger at birth can also be advantageous in avoiding gape-limited predators (Sharda et al 2021 ).…”

Innate responses to con‐ and heterospecific alarm chemicals in juveniles of a freshwater shrimp

“…Perceived predation risk can affect both parent and offspring phenotype, but it is unclear to what extent offspring behavioral traits are affected when the mother is exposed to predation risk, particularly in bearing species that externally brooded embryos (e.g. Ituarte et al., 2014), where maternal effects could occur during embryogenesis (Cattelan et al., 2020; Sharda et al., 2021). Since we used a repeated exposure mode through the entire embryonic development, mother shrimp and/or their embryos could have learned (through habituation—the simplest form of nonassociative learning‐ and/or sensitization) that something that smelt or tasted familiar (e.g.…”

Ancestral environment determines the current reaction to ultraviolet radiation inDaphnia magna

“…2014; Donelan and Trussell 2015; Freinschlag and Schausberger 2016; Donelan and Trussell 2018; Sharda et al. 2021). However, under certain circumstances, phenotypic changes induced by environmental stressors may be broader than just a parental effect and instead persist over multiple offspring generations, leading to a strong and long‐lasting transgenerational effect on the offspring survival and performance (e.g., Painter et al.…”

“…TGP may be described as a generalization of parental effects in which parental environment drives the transgenerational response and therefore modifies the offspring phenotype. To date, parental, especially maternal, effects are well studied and ample evidence has been found for many organisms in response to a variety of environmental perturbations such as toxins (Beyer and Hambright 2017;Radersma et al 2018), food availability (Harney et al 2017;Coakley et al 2018;Zhou and Declerck 2020), ultraviolet radiation (UVR) (Huebner et al 2013;Ghanizadeh Kazerouni et al 2017), or predation risk (Storm and Lima 2010;Bestion et al 2014;Donelan and Trussell 2015;Freinschlag and Schausberger 2016;Donelan and Trussell 2018;Sharda et al 2021). However, under certain circumstances, phenotypic changes induced by environmental stressors may be broader than just a parental effect and instead persist over multiple offspring generations, leading to a strong and long-lasting transgenerational effect on the offspring survival and performance (e.g., Painter et al 2008;Remy 2010;Groot et al 2016;DeCourten et al 2020).…”