Genome Resequencing Reveals Rapid, Repeated Evolution in the Colorado Potato Beetle.

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.

Pre-invasion history and demography shape the genetic variation in the insecticide resistance-related acetylcholinesterase 2 gene in the invasive Colorado potato beetle.

BACKGROUND: Invasive pest species offers a unique opportunity to study the effects of genetic architecture, demography and selection on patterns of genetic variability. Invasive Colorado potato beetle (Leptinotarsa decemlineata) populations have experienced a rapid range expansion and intense selection by insecticides. By comparing native and invasive beetle populations, we studied the origins of organophosphate (OP) resistance-associated mutations in the acetylcholinesterase 2 (AChE2) gene, and the role of selection and demography on its genetic variability. RESULTS: Analysis of three Mexican, two US and five European populations yielded a total of 49 haplotypes. Contrary to the expectations all genetic variability was associated with a point mutation linked to insecticide resistance (S291G), this mutation was found in 100% of Mexican, 95% of US and 71% of European beetle sequences analysed. Only two susceptible haplotypes, genetically very differentiated, were found, one in US and one in Europe. The genetic variability at the AChE2 gene was compared with two other genes not directly affected by insecticide selection, diapause protein 1 and juvenile hormone esterase. All three genes showed reduction in genetic variability indicative of a population bottleneck associated with the invasion. CONCLUSIONS: Stochastic effects during invasion explain most of the observed patterns of genetic variability at the three genes investigated. The high frequency of the S291G mutation in the AChE2 gene among native populations suggests this mutation is the ancestral state and thus, either a pre-adaptation of the beetle for OP resistance or the AChE2 is not the major gene conferring OP resistance. The long historical association with host plant alkaloids together with recombination may have contributed to the high genetic variation at this locus. The genetic diversity in the AChE2 locus of the European beetles, in turn, strongly reflects founder effects followed by rapid invasion. Our results suggest that despite the long history of insecticide use in this species, demographic events together with pre-invasion history have been strongly influential in shaping the genetic diversity of the AChE2 gene in the invasive beetle populations.

Transposable elements differ between geographic populations of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae).

Agricultural insect herbivores show a remarkable ability to adapt to modern agroecosystems, making them ideal for the study of the mechanisms underlying rapid evolution. The mobilization of transposable elements is one mechanism that may help explain this ability. The Colorado potato beetle, Leptinotarsa decemlineata, is a highly adaptable species, as shown by its wide host range, broad geographic distribution, and tolerance to insecticides. However, beetle populations vary in insecticide tolerance, with Eastern US beetle populations being more adaptable than Western US ones. Here, we use a community ecology approach to examine how the abundance and diversity of transposable elements differs in 88 resequenced genomes of L. decemlineata collected throughout North America. We tested if assemblages and mobilization of transposable elements differed between populations of L. decemlineata based on the beetle's geography, host plant, and neonicotinoid insecticide resistance. Among populations of North American L. decemlineata, individuals collected in Mexico host more transposable elements than individuals collected in the United States. Transposable element insertion locations differ among geographic populations, reflecting the evolutionary history of this species. Total transposable element diversity between L. decemlineata individuals is enough to distinguish between populations, with more TEs found in beetles collected in Mexico than in the United States. Transposable element diversity does not appear to differ between beetles found on different host plants, or relate to different levels of insecticide resistance.

Origin of Pest Lineages of the Colorado Potato Beetle (Coleoptera: Chrysomelidae).

Colorado potato beetle (Leptinotarsa decemlineata Say [Coleoptera: Chrysomelidae]) is a pest of potato throughout the Northern Hemisphere, but little is known about the beetle's origins as a pest. We sampled the beetle from uncultivated Solanum host plants in Mexico, and from pest and non-pest populations in the United States and used mitochondrial DNA and nuclear loci to examine three hypotheses on the origin of the pest lineages: 1) the pest beetles originated from Mexican populations, 2) they descended from hybridization between previously divergent populations, or 3) they descended from populations that are native to the Plains states in the United States. Mitochondrial haplotypes of non-pest populations from Mexico and Arizona differed substantially from beetles collected from the southern plains and potato fields in the United States, indicating that beetles from Mexico and Arizona did not contribute to founding the pest lineages. Similar results were observed for AFLP and microsatellite data . In contrast, non-pest populations from the states of Colorado, Kansas, Nebraska, New Mexico, and Texas were genetically similar to U.S. pest populations, indicating that they contributed to the founding of the pest lineages. Most of the pest populations do not show a significant reduction in genetic diversity compared to the plains populations in the United States. We conclude that genetically heterogeneous beetle populations expanded onto potato from native Solanum hosts. This mode of host range expansion may have contributed to the abundant genetic diversity of contemporary populations, perhaps contributing to the rapid evolution of climate tolerance, host range, and insecticide resistance.

Population level "flipperedness" in the eastern Pacific leatherback turtle.

Limb preference is a behavioral indicator of lateralized brain function that was recently elucidated experimentally in lower vertebrates. We assessed natural spontaneous limb use of nesting eastern Pacific leatherback turtles by recording which hindlimb flipper was extended overtop the cloaca to cover the egg chamber during oviposition. We found a population level right bias in 1889 observations of 361 individuals. This is the first report of a limb preference in Testudinata.