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Understanding the evolutionary origins and factors maintaining alternative life history strategies (ALHS) within species is a major goal of evolutionary research. While alternative alleles causing discrete ALHS are expected to purge or fix over time, one-third of the ~90 species of Colias butterflies are polymorphic for a female-limited ALHS called Alba. Whether Alba arose once, evolved in parallel, or has been exchanged among taxa is currently unknown. Using comparative genome-wide association study (GWAS) and population genomic analyses, we placed the genetic basis of Alba in time-calibrated phylogenomic framework, revealing that Alba evolved once near the base of the genus and has been subsequently maintained via introgression and balancing selection. CRISPR-Cas9 mutagenesis was then used to verify a putative cis-regulatory region of Alba, which we identified using phylogenetic foot printing. We hypothesize that this cis-regulatory region acts as a modular enhancer for the induction of the Alba ALHS, which has likely facilitated its long evolutionary persistence.

Despite considerable research, efforts to manage insecticide resistance continue to fail. The Colorado potato beetle (CPB), Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae), epitomizes this problem, as it has repeatedly and rapidly evolved resistance to50 insecticides. The patterns of resistance evolution are intriguing, as they defy models where resistance evolves from rare mutations. Here we synthesize recent research on insecticide resistance in CPB showing that polygenic resistance drawn from standing genetic diversity explains genomic patterns of insecticide resistance evolution. However, rapid gene regulatory evolution suggests that other mechanisms might also facilitate adaptive change. We explore the hypothesis that sublethal stress from insecticide exposure could alter heritable epigenetic modifications, and discuss the range of experimental approaches needed to fully understand insecticide resistance evolution in this super pest.

Insecticide resistance and rapid pest evolution threatens food security and the development of sustainable agricultural practices, yet the evolutionary mechanisms that allow pests to rapidly adapt to control tactics remains unclear. Here, we examine how a global super-pest, the Colorado potato beetle (CPB), Leptinotarsa decemlineata, rapidly evolves resistance to insecticides. Using whole-genome resequencing and transcriptomic data focused on its ancestral and pest range in North America, we assess evidence for three, nonmutually exclusive models of rapid evolution: pervasive selection on novel mutations, rapid regulatory evolution, and repeated selection on standing genetic variation. Population genomic analysis demonstrates that CPB is geographically structured, even among recently established pest populations. Pest populations exhibit similar levels of nucleotide diversity, relative to nonpest populations, and show evidence of recent expansion. Genome scans provide clear signatures of repeated adaptation across CPB populations, with especially strong evidence of selection on insecticide resistance genes in different populations. Analyses of gene expression show that constitutive upregulation of candidate insecticide resistance genes drives distinctive population patterns. CPB evolves insecticide resistance repeatedly across agricultural regions, leveraging similar genetic pathways but different genes, demonstrating a polygenic trait architecture for insecticide resistance that can evolve from standing genetic variation. Despite expectations, we do not find support for strong selection on novel mutations, or rapid evolution from selection on regulatory genes. These results suggest that integrated pest management practices must mitigate the evolution of polygenic resistance phenotypes among local pest populations, in order to maintain the efficacy and sustainability of novel control techniques.

Past glacial cycles have generated lineage diversity in alpine habitats, acting as a climate-driven species pump. It is not clear how much this process contributes to ecological diversification of alpine species. To examine this problem, we test patterns of genetic and phenotypic divergence in two co-distributed species complexes of flightless alpine ground beetles. Greater differentiation in functional traits would indicate that ecological selection is an outcome of oscillating climate change, whereas greater differentiation in non-ecological traits would indicate niche conservatism. Location: The Cascades Range and Trinity Mountains of western North America. Taxon: Nebria paradisi and N. vandykei species complexes (Insecta: Coleoptera: Carabidae: Nebriinae). Methods: We generated genome-wide single nucleotide polymorphism data and mitochondrial sequence data, as well as morphological and physiological data, to compare populations spanning the range of both species. Phylogenetic and population genetic analyses were used to infer relationships among taxa and populations in each species complex, as well as historical demography. Support vector machines were used to test for classification of taxa and populations based on ecomorphological, ecophysiological and male reproductive traits. Mantel tests were then used to assess associations between phenotypic and genetic divergence among populations. Results: The N. vandykei and N. paradisi species complexes are each comprised of genetically distinctive populations exhibiting long-term demographic declines. Each phylogeny supports multiple monophyletic groups with geographical cohesion. By examining phenotypic traits among populations in both species’ complexes, we show that reproductive trait divergence can discriminate species and population status more effectively than ecomorphological or ecophysiological traits. Reproductive and genetic divergence are significantly correlated in the N. vandykei species complex. Main Conclusions: We found limited evidence of ecological selection acting on functional traits. Instead, reproductive and genetic divergence evolved among isolated populations in both species complexes, suggesting niche conservatism may be a common outcome in alpine species diversification.