Wing polymorphism in insects provides a good model system for investigating evolutionary dynamics and population divergence in dispersal-enhancing traits. This study investigates the contribution of divergent selection, trade-offs, behaviour and spatial sorting to the evolutionary dynamics of wing polymorphism in the pygmy grasshopper Tetrix subulata (Tetrigidae: Orthoptera). We use data for > 2800 wild-caught individuals from 13 populations and demonstrate that the incidence of the long-winged (macropterous) morph is higher and changes faster between years in disturbed habitats characterized by succession than in stable habitats. Common garden and mother-offspring resemblance studies indicate that variation among populations and families is genetically determined and not influenced to any important degree by developmental plasticity in response to maternal condition, rearing density or individual growth rate. Performance trials show that only the macropterous morph is capable of flight and that propensity to fly differs according to environment. Mark-recapture data reveal no difference in the distance moved between free-ranging long-and short-winged individuals. There is no consistent difference across populations and years in number of hatchlings produced by long-and shorter-winged females. Our findings suggest that the variable frequency of the long-winged morph among and within pygmy grasshopper populations may reflect evolutionary modifications driven by spatial sorting due to phenotype-and habitat type-dependent emigration and immigration.

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Genetic diversity within and among populations and species is influenced by complex demographic and evolutionary processes. Despite extensive research, there is no consensus regarding how landscape structure, spatial distribution, gene flow, and population dynamics impact genetic composition of natural populations. Here, we used amplified fragment length polymorphisms (AFLPs) to investigate effects of population size, geographic isolation, immigration, and gene flow on genetic structure, divergence, and diversity in populations of Tetrix subulata pygmy grasshoppers (Orthoptera: Tetrigidae) from 20 sampling locations in southern Sweden. Analyses of 1564 AFLP markers revealed low to moderate levels of genetic diversity (PPL = 59.5–90.1; Hj = 0.23–0.32) within and significant divergence among sampling localities. This suggests that evolution of functional traits in response to divergent selection is possible and that gene flow is restricted. Genetic diversity increased with population size and with increasing proportion of long‐winged phenotypes (a proxy of recent immigration) across populations on the island of Öland, but not on the mainland. Our data further suggested that the open water separating Öland from the mainland acts as a dispersal barrier that restricts migration and leads to genetic divergence among regions. Isolation by distance was evident for short interpopulation distances on the mainland, but gradually disappeared as populations separated by longer distances were included. Results illustrate that integrating ecological and molecular data is key to identifying drivers of population genetic structure in natural populations. Our findings also underscore the importance of landscape structure and spatial sampling scheme for conclusions regarding the role of gene flow and isolation by distance.

Genetic structure among and diversity within natural populations is influenced by a combination of ecological and evolutionary processes. These processes can differently influence neutral and functional genetic diversity and also vary according to environmental settings. To investigate the roles of interacting processes as drivers of population‐level genetic diversity in the wild, we compared neutral and functional structure and diversity between 20 Tetrix undulata pygmy grasshopper populations in disturbed and stable habitats. Genetic differentiation was evident among the different populations, but there was no genetic separation between stable and disturbed environments. The incidence of long‐winged phenotypes was higher in disturbed habitats, indicating that these populations were recently established by flight‐capable colonizers. Color morph diversity and dispersion of outlier genetic diversity, estimated using AFLP markers, were higher in disturbed than in stable environments, likely reflecting that color polymorphism and variation in other functionally important traits increase establishment success. Neutral genetic diversity estimated using AFLP markers was lower in disturbed habitats, indicating stronger eroding effects on neutral diversity of genetic drift associated with founding events in disturbed compared to stable habitats. Functional diversity and neutral diversity were negatively correlated across populations, highlighting the utility of outlier loci in genetics studies and reinforcing that estimates of genetic diversity based on neutral markers do not infer evolutionary potential and the ability of populations and species to cope with environmental change.