With the global rise of human‐mediated translocations and invasions, it is critical to understand the genomic consequences of hybridization and mechanisms of range expansion. Conventional wisdom is that high genetic drift and loss of genetic diversity due to repeated founder effects will constrain introduced species. However, reduced genetic variation can be countered by behavioral aspects and admixture with other distinct populations. As planned invasions, classical biological control (biocontrol) agents present important opportunities to understand the mechanisms of establishment and spread in a novel environment. The ability of biocontrol agents to spread and adapt, and their effects on local ecosystems, depends on genomic variation and the consequences of admixture in novel environments. Here, we use a biocontrol system to examine the genome‐wide outcomes of introduction, spread, and hybridization in four cryptic species of a biocontrol agent, the tamarisk beetle (Diorhabda carinata, D. carinulata, D. elongata, and D. sublineata), introduced from six localities across Eurasia to control the invasive shrub tamarisk (Tamarix spp.) in western North America. We assembled a de novo draft reference genome and applied RADseq to over 500 individuals across laboratory cultures, the native ranges, and the introduced range. Despite evidence of a substantial genetic bottleneck among D. carinulata in N. America, populations continue to establish and spread, possibly due to aggregation behavior. We found that D. carinata, D. elongata, and D. sublineata hybridize in the field to varying extents, with D. carinata × D. sublineata hybrids being the most abundant. Genetic diversity was greater at sites with hybrids, highlighting potential for increased ability to adapt and expand. Our results demonstrate the complex patterns of genomic variation that can result from introduction of multiple ecotypes or species for biocontrol, and the importance of understanding them to predict and manage the effects of biocontrol agents in novel ecosystems.

Evolutionary theory predicts that the process of range expansion will lead to differences in life‐history and dispersal traits between the core and edge of a population. At the edge, selection and genetic drift can have opposing effects on reproductive ability, while spatial sorting by dispersal ability can increase dispersal. However, the context that individuals experience, including population density and mating status, also impacts dispersal behavior. We seek to understand the shifts in traits of populations expanding across natural, heterogenous environments, and the evolutionary and behavioral factors that may drive those shifts. We evaluated theoretical predictions for evolution of reproductive life‐history and dispersal traits using the range expansion of a biological control agent, Diorhabda carinulata, or northern tamarisk beetle. We find that individuals from the edge had increased fecundity and female body mass, and reduced age at first reproduction, indicating that genetic load is low and suggesting that selection has acted at the edge. We also find that density of conspecifics during rearing and mating status influence dispersal of males and that dispersal increases at the edge of the range under certain conditions, particularly when males were unmated and reared at low density. The restricted conditions in which dispersal has increased suggest that spatial sorting has exerted weak effects relative to other potential processes. Our results support most theoretical predictions about evolution during range expansion, even across a heterogeneous environment, especially when the ecological context is considered.

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Evolutionary theory predicts that the process of range expansion will lead to differences between core and edge populations in life-history and dispersal traits. Selection and genetic drift can influence reproductive ability, while spatial sorting by dispersal ability can increase dispersal at the edge. However, the context individuals experience (e.g., population density and mating status) also impacts dispersal behavior. We evaluated theoretical predictions for evolution of reproductive life-history and dispersal traits using the range expansion of a biological control agent, Diorhabda carinulata, or northern tamarisk beetle. We found divergence between core and edge populations in fecundity, age at first reproduction, and female body mass. We also show that density and mating status influence dispersal and that dispersal increases at the edge of the range under some conditions. We find support for most predictions about evolution during range expansion, even across a heterogeneous environment, especially when the ecological context is considered.

With the global rise of human-mediated translocations and invasions, it is critical to understand the genomic consequences of hybridization and mechanisms of range expansion. Conventional wisdom is that high genetic drift and loss of genetic diversity due to repeated founder effects will constrain introduced species. However, reduced genetic variation can be countered by behavioral aspects and admixture with other distinct populations. As planned invasions, classical biological control (biocontrol) agents present important opportunities to understand the mechanisms of establishment and spread in a novel environment. The ability of biocontrol agents to spread and adapt, and their effects on local ecosystems, depends on genomic variation and the consequences of admixture in novel environments. Here we use a biocontrol system to examine the genome-wide outcomes of introduction, spread, and hybridization in four cryptic species of a biocontrol agent, the tamarisk beetle (Diorhabda carinata, D. carinulata, D. elongata, and D. sublineata), introduced from six localities across Eurasia to control the invasive shrub tamarisk (Tamarix spp.) in western North America. We assembled a de novo draft reference genome and applied RADseq to over 500 individuals from laboratory cultures, the native ranges, and across the introduced range. Despite evidence of a substantial genetic bottleneck among D. carinulata in N. America, populations continue to establish and spread, possibly due to aggregation behavior. We found that D. carinata, D. elongata, and D. sublineata hybridize in the field to varying extents, with D. carinata x D. sublineata hybrids being the most abundant. Genetic diversity was greater at sites with hybrids, highlighting potential for increased ability to adapt and expand. Our results demonstrate the complex patterns of genomic variation that can result from introduction of multiple ecotypes or species for biocontrol, and the importance of understanding them to predict and manage the effects of biocontrol agents in novel ecosystems.