Experimental evidence that matching habitat choice drives local adaptation in a wild population

Matching habitat choice is a unique, flexible form of habitat choice based on self-assessment of local performance. This mechanism is thought to play an important role in adaptation and population persistence in variable environments. Nevertheless, the operation of matching habitat choice in natural populations remains to be unequivocally demonstrated. We investigated the association between body colour and substrate use by ground-perching grasshoppers ( Sphingonotus azurescens ) in an urban mosaic of dark and pale pavements, and then performed a colour manipulation experiment to test for matching habitat choice based on camouflage through background matching. Naturally, dark and pale grasshoppers occurred mostly on pavements that provided matching backgrounds. Colour-manipulated individuals recapitulated this pattern, such that black-painted and white-painted grasshoppers recaptured after the treatment aggregated together on the dark asphalt and pale pavement, respectively. Our study demonstrates that grasshoppers adjust their movement patterns to choose the substrate that confers an apparent improvement in camouflage given their individual-specific colour. More generally, our study provides unique experimental evidence of matching habitat choice as a driver of phenotype–environment correlations in natural populations and, furthermore, suggests that performance-based habitat choice might act as a mechanism of adaptation to changing environments, including human-modified (urban) landscapes.

Behaviour, life history and persistence in novel environments

Understanding what affects population growth in novel environments is fundamental to forecast organisms' responses to global change, including biological invasions and land use intensification. Novel environments are challenging because they can cause maladaptation, increasing the risk of extinction by negative population growth. Animals can avoid extinction by improving the phenotype–environment match through behavioural responses, notably matching habitat choice and learning. However, the demographic consequences of these responses remain insufficiently understood in part because they have not been analysed within a life-history context. By means of an individual-based model, we show here that matching habitat choice and learning interact with life history to influence persistence in novel environments. In maladaptive contexts, the likelihood of persisting is higher for life-history strategies that increase the value of adults over the value of offspring, even at the cost of decreasing reproduction. Such a strategy facilitates persistence in novel environments by reducing the costs of a reproductive failure while increasing the benefits of behavioural responses. Our results reinforce the view that a more predictive theory for extinction risk under rapid environmental changes requires considering behavioural responses and life history as part of a common adaptive strategy to cope with environmental changes. This article is part of the theme issue ‘Linking behaviour to dynamics of populations and communities: application of novel approaches in behavioural ecology to conservation’.

Personality-matching habitat choice, rather than behavioural plasticity, is a likely driver of a phenotype–environment covariance

An emerging hypothesis of animal personality posits that animals choose the habitat that best fits their personality, and that the match between habitat and personality can facilitate population differentiation, and eventually speciation. However, behavioural plasticity and the adjustment of behaviours to new environments have been a classical explanation for such matching patterns. Using a population of dunnocks ( Prunella modularis ), we empirically tested whether personality or behavioural plasticity is responsible for the non-random distribution of shy and bold individuals in a heterogeneous environment. We found evidence for bold individuals settling in areas with high human disturbance, but also that birds became bolder with increasing age. Importantly, personality primarily determines the distribution of individuals, and behavioural adjustment over time contributes very little to the observed patterns. We cannot, however, exclude a possibility of very early behavioural plasticity (a type of developmental plasticity) shaping what we refer to as ‘personality’. Nonetheless, our findings highlight the role personality plays in shaping population structure, lending support to the theory of personality-mediated speciation. Moreover, personality-matching habitat choice has important implications for population management and conservation.