Antipredator defences of young are independently determined by genetic inheritance, maternal effects and own early experience in mouthbrooding cichlids

Abstract

Summary1. Predation is a prime force of natural selection. Vulnerability to predation is typically highest early in life, hence effective antipredator defences should work already shortly after birth. Such early defences may be innate, transmitted through non-genetic parental effects or acquired by own early experience. 2. To understand potential joint effects of these sources of antipredator defences on phenotypic expression, they should be manipulated within the same experiment. We investigated innate, parental and individual experience effects within a single experiment. Females of the African cichlid Simochromis pleurospilus were exposed to the offspring predator Ctenochromis horei or a benign species until spawning. Eggs and larvae were hand-reared, and larvae were then exposed to odour cues signalling the presence or absence of predators in a split-brood design. 3. Shortly after independence of maternal care, S. pleurospilus undergo a habitat shift from a deeper, adult habitat to a shallow juvenile habitat, a phase where young are thought to be particularly exposed to predation risk. Thus, maternal effects induced by offspring predators present in the adult habitat should take effect mainly shortly after independence, whereas own experience and innate antipredator responses should shape behaviour and life history of S. pleurospilus during the later juvenile period. 4. We found that the manipulated environmental components independently affected different offspring traits. (i) Offspring of predator-exposed mothers grew faster during the first month of life and were thus larger at termination of maternal care, when the young migrate from the adult to the juvenile habitat. (ii) The offspring's own experience shortly after hatching exerted lasting effects on predator avoidance behaviour. (iii) Finally, our results suggest that S. pleurospilus possess a genetically inherited ability to distinguish dangerous from benign species. 5. In S. pleurospilus, maternal effects were limited to a short but critical time window, when young undergo a niche shift. Instead, own environmental sampling of predation risk combined with an innate predisposition to correctly identify predators appears to prepare the young best for the environment, in which they grow up as juveniles.

Developmental temperatures and phenotypic plasticity in reptiles: a systematic review and meta‐analysis

“…Parental effects can include changes in yolk hormone concentrations, transfer of mRNA and immunological factors, changes in lipid and protein concentrations in the egg, clutch size and epigenetic programming (Mousseau & Fox, 1998;Morgan et al, 1999;Bowden et al, 2004;Groothuis & Schwabl, 2008;Hesselquist & Nilsson, 2009;Burton & Metcalfe, 2014;Tschirren, 2015). The impact of parental effects on phenotypic development can be complex, particularly when considering the interaction between parental effects and early offspring environment (Stratmann & Taborsky, 2014). These interactions may account for the large unpredictable effects of incubation environment on offspring phenotype and may even mediate the magnitude of response to early thermal conditions (Miller et al, 2012;Allan et al, 2014).…”

Adaptive trans‐generational phenotypic plasticity and the lack of an experimental control in reciprocal match/mismatch experiments

“…Appleton & Palmer ; Brönmark & Miner ; Tollrian ; Weisser, Braendle & Minoretti ; Relyea ; Frommen et al . ; Stratmann & Taborsky ).…”

“…; Shama et al . ; Stratmann & Taborsky ). There are many different names used in the literature to describe such parentally mediated adaptive plasticity (Uller, Nakagawa & English ).…”

“…Arguably the most prominent and illustrative evidence comes from phenotypic plasticity in response to a changing risk of predation (see, e.g. Appleton & Palmer 1988;Br€ onmark & Miner 1992;Tollrian 1995;Weisser, Braendle & Minoretti 1999;Relyea 2001;Frommen et al 2011;Stratmann & Taborsky 2014).…”

“…Often, the parental environment is predictive of the environment likely to be faced by their offspring. If this is the case, trans-generational cues would provide an effective channel in which offspring could potentially receive adequate information very early in their development (Mousseau & Dingle 1991;Mousseau & Fox 1998;Fox et al 1999;Kuijper & Hoyle 2015) and as a consequence could modify their phenotype adaptively according to the provided parental information (Fox, Thakar & Mousseau 1997;Agrawal, Laforsch & Tollrian 1999;Bateson et al 2004;Gustafsson, Rengefors & Hansson 2005;Moret 2006;Cleal et al 2007;Galloway & Etterson 2007;Marshall 2008;Hasselquist & Nilsson 2009;Sultan, Barton & Wilczek 2009;Latzel et al 2014;Shama et al 2014;Stratmann & Taborsky 2014). There are many different names used in the literature to describe such parentally mediated adaptive plasticity (Uller, Nakagawa & English 2013).…”