With ongoing global change, life is continuously forced to move to novel areas, which leads to dynamically changing species ranges. As dispersal is central to range dynamics, factors promoting fast and distant dispersal are key to understanding and predicting species ranges. During range expansions, genetic variation is depleted at the expanding front. Such conditions should reduce evolutionary potential, while increasing kin competition. Organisms able to recognise relatives may be able to assess increased levels of relatedness at expanding range margins and to increase their dispersal in a plastic manner. Using individual-based simulations and experimental range expansions of a spider mite, we demonstrate that plastic responses to kin structure can be at least as important as evolution in driving range expansion speed. Because recognition of kin or kind is increasingly documented across the tree of life, we anticipate it to be a highly important but neglected driver of range expansions.
In the context of climate change and species invasions, range shifts increasingly gain attention because the rates at which they occur in the Anthropocene induce rapid changes in biological assemblages. During range shifts, species experience multiple selection pressures. For poleward expansions in particular, it is difficult to interpret observed evolutionary dynamics because of the joint action of evolutionary processes related to spatial selection and to adaptation toward local climatic conditions. To disentangle the effects of these two processes, we integrated stochastic modeling and data from a common garden experiment, using the spider mite Tetranychus urticae as a model species. By linking the empirical data with those derived form a highly parameterized individual-based model, we infer that both spatial selection and local adaptation contributed to the observed latitudinal lifehistory divergence. Spatial selection best described variation in dispersal behavior, while variation in development was best explained by adaptation to the local climate. Divergence in life-history traits in species shifting poleward could consequently be jointly determined by contemporary evolutionary dynamics resulting from adaptation to the environmental gradient and from spatial selection. The integration of modeling with common garden experiments provides a powerful tool to study the contribution of these evolutionary processes on life-history evolution during range expansion.
2During range expansion, the most dispersive individuals make up the range front, and 3 assortative mating between these dispersive phenotypes leads to increased dispersiveness (i.e. 4 spatial sorting). The precise inheritance of dispersal, however, is to date largely unknown in 5 many organisms, thereby hampering any progress in evaluating the adaptive potential of 6 species during range expansion. 7Using the spider mite Tetranychus urticae, we therefore empirically simulated spatial 8 sorting by means of artificial selection on a unique pre-dispersal behaviour, tightly related to 9 emigration. To separate directionality of the response from potential drift, we mimicked a 10 recurrent low number of founders in replicated selection regimes. Afterwards, we inferred the 11 mode of inheritance of the pre-dispersal behaviour by performing reciprocal crosses between 12 selected (i.e. dispersive) and non-selected (i.e. non-dispersive) mites and by screening for 13 endosymbionts known to be associated with changes in dispersal behaviour. 14 Despite the recurrent low number of founders, the aerial dispersal behaviour 15 responded strongly to the imposed selection pressure. The behaviour furthermore showed a 16 maternal inheritance, though independent of any known dispersal-related endosymbionts. 17Though cytoplasmic inheritance cannot fully be excluded, we attribute the observed strong 18 and rapid, maternally influenced response in dispersal to transgenerational epigenetic effects. 19Consequently, we can expect fast evolutionary dynamics during range expansion in the 20 species. 21 22 4
Despite an increasing number of studies documenting life-history evolution during range expansions or shifts, we lack a mechanistic understanding of the underlying physiological processes. In this explorative study, we used a metabolomics approach to study physiological changes associated with the recent range expansion of the two-spotted spider mite (Tetranychus urticae). Mite populations were sampled along a latitudinal gradient from range core to edge and reared under benign common garden conditions for two generations. Using gas chromatography-mass spectrometry, we obtained metabolic population profiles, which showed a gradual differentiation along the latitudinal gradient, indicating (epi)genetic changes in the metabolome in association with range expansion. These changes seemed not related with shifts in the mites' energetic metabolism, but rather with differential use of amino acids. Particularly, more dispersive northern populations showed lowered concentrations of several essential and nonessential amino acids, suggesting a potential downregulation of metabolic pathways associated with protein synthesis.
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