Adaptive potential and evolutionary divergence of scototaxis in juvenile Trinidadian Guppies

Habitat choice and resource acquisition represent an intrinsic trade-off, resulting in variation among individuals and potentially local adaptation among populations. Here, we quantify scototaxis, or preference for dark versus light backgrounds, in juvenile guppies. Scototaxis assays, in which individuals choose between safer dark and riskier light backgrounds, are widely used as a measure of boldness in small fishes, but they can equally be interpreted as choice between two habitats. By rearing and testing 586 fish descended from ten natural populations from Trinidad under common garden conditions, we first quantify (broad sense) heritable variation, i.e. evolutionary potential, within populations. Next, we test for evolutionary divergence among populations in mean preference, and if present, whether ancestral predation regime is a mediator of divergence. Finally, we ask whether families and/or populations differ in the amount of behavioural variation they contain. Preference varied among families (12% of total variance), consistent with broad-sense heritable variation. We also found that mean preference varied among populations (11% of total variance explained). Evolutionary divergence among-populations is partly explained by ancestral predation regime, with populations from low-predation sites showing a stronger preference for dark backgrounds than high-predation populations from the same river. Additionally, we find that within-population behavioural variation is greater in high-predation populations. We conclude that guppy populations contain heritable variation that could facilitate adaptive evolution if scototaxis is subject to natural selection. Furthermore, while genetic drift may also contribute to evolutionary divergence among-populations, observed patterns are qualitatively consistent with local adaption to predation regime. Our results suggests that high predation sites favour ‘bolder’ habitat choice on average, but also that local predation regime shapes the evolutionary dynamics of variation, perhaps by maintaining shy-bold variation among individuals, or by favouring individuals with less-predictable behaviour.