Small Variations in Early-Life Environment Can Affect Coping Behaviour in Response to Foraging Challenge in the Three-Spined Stickleback

Abstract

ContextAn increasing concern in the face of human expansion throughout natural habitats is whether animal populations can respond adaptively when confronted with challenges like environmental change and novelty. Behavioural flexibility is an important factor in estimating the adaptive potential of both individuals and populations, and predicting the degree to which they can cope with change.Study DesignThis study on the three-spined stickleback (Gasterosteus aculeatus) is an empiric illustration of the degree of behavioural variation that can emerge between semi-natural systems within only a single generation. Wild-caught adult sticklebacks (P, N = 400) were randomly distributed in equal densities over 20 standardized semi-natural environments (ponds), and one year later offspring (F1, N = 652) were presented with repeated behavioural assays. Individuals were challenged to reach a food source through a novel transparent obstacle, during which exploration, activity, foraging, sociability and wall-biting behaviours were recorded through video observation. We found that coping responses of individuals from the first generation to this unfamiliar foraging challenge were related to even relatively small, naturally diversified variation in developmental environment. All measured behaviours were correlated with each other. Especially exploration, sociability and wall-biting were found to differ significantly between ponds. These differences could not be explained by stickleback density or the turbidity of the water.FindingsOur findings show that a) differences in early-life environment appear to affect stickleback feeding behaviour later in life; b) this is the case even when the environmental differences are only small, within natural parameters and diversified gradually; and c) effects are present despite semi-natural conditions that fluctuate during the year. Therefore, in behaviourally plastic animals like the stickleback, the adaptive response to human-induced habitat disturbance may occur rapidly (within one generation) and vary strongly based on the system’s (starting) conditions. This has important implications for the variability in animal behaviour, which may be much larger than expected from studying laboratory systems, as well as for the validity of predictions of population responses to change.

Effects of genetics and early-life mild hypoxia on size variation in farmed gilthead sea bream (Sparus aurata)

“…By contrast, growth compensatory constraints became evident with recurrent or late hypoxia episodes, which impaired, to a different extent, the capacity to reduce size variation during the dominant phase of muscle growth hyperplasia. However, it remains to be established the precise links between these phenotypic outputs and the early events, which affect both physiological (Pittman et al 2013) and social behavior (Garduño-Paz et al 2010;Bell et al 2011;Langenhof et al 2016) traits in fish.…”

Effects of Cheliped Amputation on the Personality of Crayfish

“…Behavioral ontogeny is a long-term process, and the effects of behavioral factors differ at different developmental stages [23,24]. The early life stage is commonly considered a key "sensitive window" during which behavioral traits are expected to be strongly shaped by experience [25]. Growing up in certain environments can induce animals to exhibit permanent personality traits.…”

Environmental temperature during early life affects the personality of mosquitofish in adulthood

“…The influence of environmental factors on animals’ behavior can occur throughout their lives, with different effects between sexes and among ontogenic stages ( Langenhof et al 2016 ). Special attention is suggested to be focused on the “sensitive windows” that are often present in animals’ early growth ( Fawcett and Frankenhuis 2015 ).…”

“…For example, exposure to predation risk during early life can affect the growth of 3-spined stickleback Gasterosteus aculeatus , resulting in smaller body size in adulthood ( Bell et al 2011 ). As one of the behavioral phenotypes, adult personality can be consolidated and shaped by the environmental factors experienced during early life stages ( Langenhof et al 2016 ; Amat et al 2018 ). Therefore, investigating the influence of environmental temperature during early life on personality may provide important insights into the ontogeny of this phenotypic trait ( Killen et al 2010 ; Gracceva et al 2011 ).…”