Evolutionary inference from QST-FST comparisons: disentangling local adaptation from altitudinal gradient selection in snapdragon plants

Phenotypic differentiation among natural populations can be explained by natural selection or by neutral processes such as drift. There are many examples in the literature where comparing the effects of these processes on multiple populations has allowed the detection of local adaptation. However, these studies rarely identify the agents of selection. Whether population adaptive divergence is caused by local features of the environment, or by the environmental demand emerging at a more global scale, for example along altitudinal gradients, is a question that remains poorly investigated. Here, we measured neutral genetic (FST) and quantitative genetic (QST) differentiation among 13 populations of snapdragon plants (Antirrhinum majus) in a common garden experiment. We found low but significant genetic differentiation at putatively neutral markers, which supports the hypothesis of either ongoing pervasive homogenisation via gene flow between diverged populations or reproductive isolation between disconnected populations. Our results also support the hypothesis of local adaptation involving phenological, morphological, reproductive and functional traits. They also showed that phenotypic differentiation increased with altitude for traits reflecting the reproduction and the phenology of plants, thereby confirming the role of such traits in their adaptation to environmental differences associated with altitude. Our approach allowed us to identify candidate traits for the adaptation to climate change in snapdragon plants. Our findings imply that environmental conditions changing with altitude, such as the climatic envelope, influenced the adaptation of multiple populations of snapdragon plants on the top of their adaptation to local environmental features. They also have implications for the study of adaptive evolution in structured populations because they highlight the need to disentangle the adaptation of plant populations to climate envelopes and altitude from the confounding effects of selective pressures acting specifically at the local scale of a population.