Melanin-based skin spots reflect stress responsiveness in salmonid fish

Abstract

Within animal populations, genetic, epigenetic and environmental factors interact to shape individual neuroendocrine and behavioural profiles, conferring variable vulnerability to stress and disease. It remains debated how alternative behavioural syndromes and stress coping styles evolve and are maintained by natural selection. Here we show that individual variation in stress responsiveness is reflected in the visual appearance of two species of teleost fish; rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Salmon and trout skin vary from nearly immaculate to densely spotted, with black spots formed by eumelanin-producing chromatophores. In rainbow trout, selection for divergent hypothalamus–pituitary–interrenal responsiveness has led to a change in dermal pigmentation patterns, with low cortisol-responsive fish being consistently more spotted. In an aquaculture population of Atlantic salmon individuals with more spots showed a reduced physiological and behavioural response to stress. Taken together, these data demonstrate a heritable behavioural–physiological and morphological trait correlation that may be specific to alternative coping styles. This observation may illuminate the evolution of contrasting coping styles and behavioural syndromes, as occurrence of phenotypes in different environments and their response to selective pressures can be precisely and easily recorded.

Introduction

Within the last decade, several influential publications have promoted the recognition of individual differences within a population as biologically meaningful adaptive traits (Koolhaas et al., 1999, Wilson, 1998), and the emerging conceptual framework for individuality has had important consequences to both evolutionary ecology, animal husbandry, and biomedicine (Sih et al., 2004, Cavigelli, 2005, Huntingford and Adams, 2005, Korte et al., 2005, Réale et al., 2007). Individuals differ in the way they react towards stressful situations and novelties, and selection studies in several species show that physiological and behavioural responses to stress are often correlated in a coherent and heritable pattern (Øverli et al., 2005, van Oers et al., 2005). Stress-related physiological–behavioural trait associations are commonly referred to as stress coping styles (Koolhaas et al., 1999), while consistent individual variation in behaviour across other situations has been denoted behavioural syndromes, profiles, axes, temperament, or a shyness–boldness continuum (Gosling, 2001, Sih et al., 2004, Wilson et al., 1994, Réale et al., 2007). Notwithstanding a certain lack of consensus in terminology, the evolution of these analogues of human personality has evoked considerable scientific interest. Among the questions raised are by which mechanisms behavioural syndromes are inherited, how the variation is maintained, which circumstances benefit different complex phenotypes, and what are the costs and benefits of limited plasticity imposed by more or less fixed trait associations (DeWitt et al., 1998, Koolhaas et al., 1999, Sih et al., 2004, Dingemanese and Réale, 2005, McElreath et al., 2007, Réale et al., 2007, Wolf et al., 2007).

Salmonid fish of the genera Oncorhynchus and Salmo attract the attention of both researchers and the general public, on account of their biological characteristics and wide use in sport and recreational fishing, aquaculture, and research (see examples in Thorgaard et al. (2002)). Salmonids are particularly known for their extensive genetic and life-history variation, resulting in part from their homing ability during spawning, with localized sub-populations being adapted to different sites and environments within a river system (Dittman and Quinn, 1996, Garcia de Leaniz et al., 2007). Previously, we have used strains of rainbow trout (Oncorhynchus mykiss) selected for divergent (high-responsive, HR, and low-responsive, LR) post-stress cortisol levels to study heritable variation in neuroendocrine and behavioural stress responses (Øverli et al., 2005, Schjolden and Winberg, 2007). Low post-stress cortisol levels are typically associated with proactive behavioural traits such as social dominance and boldness in new environments (Pottinger and Carrick, 2001, Øverli et al., 2007). In contrast, high cortisol levels are associated with social subordinance and shyness (Pottinger and Carrick, 2001, Øverli et al., 2007). Furthermore, high cortisol levels may confer increased susceptibility to some infectious diseases (Fevolden et al., 1992).

Anybody who has studied, fished for, handled, or consumed salmon or rainbow trout may have noticed the black spots dappling the skin of these fishes. The spots are formed by specialised chromatophores – melanophores (or melanocytes) – which produce the dark pigment eumelanin (Bagnara, 1998). During work with the fourth generation of HR–LR rainbow trout, it became evident that the two strains differed in pigment patterns. Specifically, LR fish exhibited far more eumelanin spots than HR fish. Melanin-based colouration in vertebrates and its association with behavioural syndromes were recently reviewed by Ducrest et al. (2008). This literature review showed that darker wild vertebrates are generally more aggressive, sexually active and resistant to stress than lighter individuals (Ducrest et al., 2008). Furthermore, in the barn owl (Tyto alba) melanin-based colouration is associated with several behavioural, morphological and physiological characteristics that have been linked to stress coping ability (Almasi et al., 2008).

Based on observations that HR and LR trout differed in melanin pigmentation our hypothesis was that spotted fish, in the closely related species Atlantic salmon (Salmo salar), would show a lower cortisol response to stress when compared to a non-spotted group of individuals. Furthermore, several documented changes in the behaviour of the two trout lines made us predict that also behaviour would differ between groups of spotted and non-spotted fish. The main focus of this study was therefore to test the hypothesis that there exists an association between melanin-based pigmentation and hypothalamus–pituitary–interrenal (HPI-axis) reactivity in salmonid fish. Furthermore, we tested the prediction that behavioural differences are present in two groups of fish identified on the basis of divergent melanin pigmentation.