The physiological cost of colour change: evidence, implications and mitigations.

Animals benefit from phenotypic plasticity in changing environments, but this can come at a cost. Colour change, used for camouflage, communication, thermoregulation and UV protection, represents one of the most common plastic traits in nature and is categorised as morphological or physiological depending on the mechanism and speed of the change. Colour change has been assumed to carry physiological costs, but current knowledge has not advanced beyond this basic assumption. The costs of changing colour will shape the evolution of colour change in animals, yet no coherent research has been conducted in this area, leaving a gap in our understanding. Therefore, in this Review, we examine the direct and indirect evidence of the physiological cost of colour change from the cellular to the population level, in animals that utilise chromatophores in colour change. Our Review concludes that the physiological costs result from either one or a combination of the processes of (i) production, (ii) translocation and (iii) maintenance of pigments within the colour-containing cells (chromatophores). In addition, both types of colour change (morphological and physiological) pose costs as they require energy for hormone production and neural signalling. Moreover, our Review upholds the hypothesis that, if repetitively used, rapid colour change (i.e. seconds-minutes) is more costly than slow colour change (days-weeks) given that rapidly colour-changing animals show mitigations, such as avoiding colour change when possible. We discuss the potential implications of this cost on colour change, behaviour and evolution of colour-changing animals, generating testable hypotheses and emphasising the need for future work to address this gap.

Paternal effects in a wild-type zebrafish implicate a role of sperm-derived small RNAs.

While the importance of maternal effects has long been appreciated, a growing body of evidence now points to the paternal environment having an important influence on offspring phenotype. Indeed, research on rodent models suggests that paternal stress leaves an imprint on the behaviour and physiology of offspring via nongenetic information carried in the spermatozoa; however, fish have been understudied with regard to these sperm-mediated effects. Here, we investigated whether the zebrafish was subjected to heritable influences of paternal stress by exposing males to stressors (conspecific-derived alarm cue, chasing and bright light) before mating and assessing the behavioural and endocrine responses of their offspring, including their behavioural response to conspecific-derived alarm cue. We found that after males are exposed to stress, their larval offspring show weakened responses to stressors. Small RNA sequencing subsequently revealed that the levels of several small noncoding RNAs, including microRNAs, PIWI-interacting RNAs and tRNA-derived small RNAs, were altered in the spermatozoa of stressed fathers, suggesting that stress-induced alterations to the spermatozoal RNA landscape may contribute to shaping offspring phenotype. The work demonstrates that paternal stress should not be overlooked as a source of phenotypic variation and that spermatozoal small RNAs may be important intergenerational messengers in fish.

Premature birth stunts early growth and is a possible driver of stress-induced maternal effects in the guppy Poecilia reticulata.

We tested the effects of gestational stress, principally in the form of alarm cue extracted from the skin of conspecifics, on reproduction in female guppies (Poecilia reticulata) and the growth and behaviour of their offspring. Offspring from mothers exposed to alarm cue exhibited stunted growth in the first few days post-partum, which appeared to be mediated by shortening of the gestation period, the length of which directly correlated with growth rate within the first 6 days post-partum. Mature offspring did not differ in behaviour or stress responses compared with controls and so the effects of maternal predation stress did not appear to persist into adulthood. A different form of gestational stress, dietary restriction, did not significantly affect offspring growth, though brood size was reduced, suggesting that the effects of predation stress were not mediated by differences in resource demand or consumption.

Disrupted-in-Schizophrenia-1 is essential for normal hypothalamic-pituitary-interrenal (HPI) axis function.

Psychiatric disorders arise due to an interplay of genetic and environmental factors, including stress. Studies in rodents have shown that mutants for Disrupted-In-Schizophrenia-1 (DISC1), a well-accepted genetic risk factor for mental illness, display abnormal behaviours in response to stress, but the mechanisms through which DISC1 affects stress responses remain poorly understood. Using two lines of zebrafish homozygous mutant for disc1, we investigated behaviour and functioning of the hypothalamic-pituitary-interrenal (HPI) axis, the fish equivalent of the hypothalamic-pituitary-adrenal (HPA) axis. Here, we show that the role of DISC1 in stress responses is evolutionarily conserved and that DISC1 is essential for normal functioning of the HPI axis. Adult zebrafish homozygous mutant for disc1 show aberrant behavioural responses to stress. Our studies reveal that in the embryo, disc1 is expressed in neural progenitor cells of the hypothalamus, a conserved region of the vertebrate brain that centrally controls responses to environmental stressors. In disc1 mutant embryos, proliferating rx3+ hypothalamic progenitors are not maintained normally and neuronal differentiation is compromised: rx3-derived ff1b+ neurons, implicated in anxiety-related behaviours, and corticotrophin releasing hormone (crh) neurons, key regulators of the stress axis, develop abnormally, and rx3-derived pomc+ neurons are disorganised. Abnormal hypothalamic development is associated with dysfunctional behavioural and neuroendocrine stress responses. In contrast to wild type siblings, disc1 mutant larvae show altered crh levels, fail to upregulate cortisol levels when under stress and do not modulate shoal cohesion, indicative of abnormal social behaviour. These data indicate that disc1 is essential for normal development of the hypothalamus and for the correct functioning of the HPA/HPI axis.

Long-Term Effects of the Periconception Period on Embryo Epigenetic Profile and Phenotype: The Role of Stress and How This Effect Is Mediated.

Stress represents an unavoidable aspect of human life, and pathologies associated with dysregulation of stress mechanisms - particularly psychiatric disorders - represent a significant global health problem. While it has long been observed that levels of stress experienced in the periconception period may greatly affect the offspring's risk of psychiatric disorders, the mechanisms underlying these associations are not yet comprehensively understood. In order to address this question, this chapter will take a 'top-down' approach, by first defining stress and associated concepts, before exploring the mechanistic basis of the stress response in the form of the hypothalamic-pituitary-adrenal (HPA) axis, and how dysregulation of the HPA axis can impede our mental and physical health, primarily via imbalances in glucocorticoids (GCs) and their corresponding receptors (GRs) in the brain. The current extent of knowledge pertaining to the impact of stress on developmental programming and epigenetic inheritance is then extensively discussed, including the role of chromatin remodelling associated with specific HPA axis-related genes and the possible role of regulatory RNAs as messengers of environmental stress both in the intrauterine environment and across the germ line. Furthering our understanding of the role of stress on embryonic development is crucial if we are to increase our predictive power of disease risk and devise-effective treatments and intervention strategies.

Heritability of boldness and aggressiveness in the zebrafish.

Behavioural traits that are consistent over time and in different contexts are often referred to as personality traits. These traits influence fitness because they play a major role in foraging, reproduction and survival, and so it is assumed that they have little or no additive genetic variance and, consequently, low heritability because, theoretically, they are under strong selection. Boldness and aggressiveness are two personality traits that have been shown to affect fitness. By crossing single males to multiple females, we estimated the heritability of boldness and aggressiveness in the zebrafish, Danio rerio. The additive genetic variance was statistically significant for both traits and the heritability estimates (95 % confidence intervals) for boldness and aggressiveness were 0.76 (0.49, 0.90) and 0.36 (0.10, 0.72) respectively. Furthermore, there were significant maternal effects accounting for 18 and 9 % of the proportion of phenotypic variance in boldness and aggressiveness respectively. This study shows that there is a significant level of genetic variation in this population that would allow these traits to evolve in response to selection.

Maternal Chronic Ethanol Exposure Decreases Stress Responses in Zebrafish Offspring.

In humans, prenatal alcohol exposure can cause serious health issues in children, known collectively as Foetal Alcohol Spectrum Disorders (FASD). Despite the high prevalence of FASD and a lack of effective treatments, the underlying mechanisms causing the teratogenic action of ethanol are still obscure. The limitations of human studies necessitate the use of animal models for identifying the underlying processes, but few studies have investigated the effects of alcohol in the female germline. Here, we used the zebrafish Danio rerio to investigate the effects of chronic (repeated for seven days) exposure to alcohol. Specifically, we tested whether the offspring of females chronically exposed to ethanol during oogenesis exhibited hormonal abnormalities when subjected to a stressor (alarm cue) as larvae, and if they exhibited anxiety-like behaviours as adults. Exposure to alarm cue increased whole-body cortisol in control larvae but not in those of ethanol-treated females. Furthermore, adult offspring of ethanol-treated females showed some reduced anxiety-like behaviours. These findings suggest that the offspring of ethanol-treated females had reduced stress responses. This study is the first to investigate how maternal chronic ethanol exposure prior to fertilisation influences hormonal and behavioural effects in a non-rodent model.