Despite extensive research on agricultural pests, our knowledge about their evolutionary history is often limited. A mechanistic understanding of the demographic changes and modes of adaptation remains an important goal, as it improves our understanding of organismal responses to environmental change and our ability to sustainably manage pest populations. Emerging genomic datasets now allow for characterization of demographic and adaptive processes, but face limits when they are drawn from contemporary samples, especially in the context of strong demographic change, repeated selection, or adaptation involving modest shifts in allele frequency at many loci. Temporal sampling, however, can improve our ability to reconstruct evolutionary events. Here, we leverage museum samples to examine whether population genomic diversity and structure has changed over time, and to identify genomic regions that appear to be under selection. We focus on the Colorado potato beetle (CPB), Leptinotarsa decemlineata (Say 1824; Coleoptera: Chrysomelidae), which is widely regarded as a super-pest due to its rapid, and repeated, evolution to insecticides. By combining whole genome resequencing data from 78 museum samples with modern sampling, we demonstrate that CPB expanded rapidly in the 19th century, leading to a reduction in diversity and limited genetic structure from the Midwest to Northeast United States. Temporal genome scans provide extensive evidence for selection acting in resistant field populations in Wisconsin and New York, including numerous known insecticide resistance genes. We also validate these results by showing that known selective sweeps in modern populations are identified by our genome scan. Perhaps most importantly, temporal analysis indicates selection on standing genetic variation, as we find evidence for parallel evolution in the two geographical regions. Parallel evolution involves a range of phenotypic traits not previously identified as under selection in CPB, such as reproductive and morphological functional pathways that might be important for adaptation to agricultural habitats.
- Award ID(s):
- 2029959
- NSF-PAR ID:
- 10380825
- Date Published:
- Journal Name:
- Horticulture Research
- Volume:
- 9
- ISSN:
- 2052-7276
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract -
null (Ed.)High rates of dispersal can breakdown coadapted gene complexes. However, concentrated genomic architecture (i.e., genomic islands of divergence) can suppress recombination to allow evolution of local adaptations despite high gene flow. Pacific lamprey (Entosphenus tridentatus) is a highly dispersive anadromous fish. Observed trait diversity and evidence for genetic basis of traits suggests it may be locally adapted. We addressed whether concentrated genomic architecture could influence local adaptation for Pacific lamprey. Using two new whole genome assemblies and genotypes from 7,716 single nucleotide polymorphism (SNP) loci in 518 individuals from across the species range, we identified four genomic islands of divergence (on chromosomes 01, 02, 04, and 22). We determined robust phenotype-by-genotype relationships by testing multiple traits across geographic sites. These trait associations probably explain genomic divergence across the species’ range. We genotyped a subset of 302 broadly distributed SNPs in 2,145 individuals for association testing for adult body size, sexual maturity, migration distance and timing, adult swimming ability, and larval growth. Body size traits were strongly associated with SNPs on chromosomes 02 and 04. Moderate associations also implicated SNPs on chromosome 01 as being associated with variation in female maturity. Finally, we used candidate SNPs to extrapolate a heterogeneous spatiotemporal distribution of these predicted phenotypes based on independent data sets of larval and adult collections. These maturity and body size results guide future elucidation of factors driving regional optimization of these traits for fitness. Pacific lamprey is culturally important and imperiled. This research addresses biological uncertainties that challenge restoration efforts.more » « less
-
more » « less
Abstract Discovering local adaptation, its genetic underpinnings, and environmental drivers is important for conserving forest species. Ecological genomic approaches coupled with next‐generation sequencing are useful means to detect local adaptation and uncover its underlying genetic basis in nonmodel species. We report results from a study on flowering dogwood trees (
Cornus florida L .) using genotyping by sequencing (GBS ). This species is ecologically important to easternUS forests but is severely threatened by fungal diseases. We analyzed subpopulations in divergent ecological habitats within North Carolina to uncover loci under local selection and associated with environmental–functional traits or disease infection. At this scale, we tested the effect of incorporating additional sequencing before scaling for a broader examination of the entire range. To test for biases ofGBS , we sequenced two similarly sampled libraries independently from six populations of three ecological habitats. We obtained environmental–functional traits for each subpopulation to identify associations with genotypes via latent factor mixed modeling (LFMM ) and gradient forests analysis. To test whether heterogeneity of abiotic pressures resulted in genetic differentiation indicative of local adaptation, we evaluatedF stper locus while accounting for genetic differentiation between coastal subpopulations and Piedmont‐Mountain subpopulations. Of the 54 candidate loci with sufficient evidence of being under selection among both libraries, 28–39 were Arlequin–BayeScanF stoutliers. ForLFMM , 45 candidates were associated with climate (of 54), 30 were associated with soil properties, and four were associated with plant health. Reanalysis of combined libraries showed that 42 candidate loci still showed evidence of being under selection. We conclude environment‐driven selection on specific loci has resulted in local adaptation in response to potassium deficiencies, temperature, precipitation, and (to a marginal extent) disease. High allele turnover along ecological gradients further supports the adaptive significance of loci speculated to be under selection. -
more » « less
Abstract Context Processes that shape genomic and ecological divergence can reveal important evolutionary dynamics to inform the conservation of threatened species.
Fontainea is a genus of rainforest shrubs and small trees including critically endangered and threatened species restricted to narrow, but complex geographic and ecological regions. Several species ofFontainea are subject to spatially explicit conditions and experience limited intra-specific gene flow, likely generating genetic differentiation and local adaptation.Objectives Here, we explored the genetic and ecological mechanisms underlying patterns of diversification in two, closely related threatened
Fontainea species. Our aim was to compare spatial patterns of genetic variation between the vulnerableFontainea australis (Southern Fontainea) and critically endangeredF. oraria (Coastal Fontainea), endemic to the heterogeneous subtropical region of central, eastern Australia, where large-scale clearing has severely reduced rainforest habitat to a fraction (< 1%) of its pre-European settlement extent.Methods We used a set of 10,000 reduced-representation markers to infer genetic relationships and the drivers of spatial genetic variation across the two species. In addition, we employed a combination of univariate and multivariate genome-environment association analysis using a set of topo-climatic variables to explore potential patterns of local adaptation as a factor impacting genomic divergence.
Results Our study revealed that Coastal Fontainea have a close genetic relationship with Southern Fontainea. We showed that isolation by distance has played a key role in their genetic variation, indicating that vicariance can explain the spatial genetic distribution of the two species. Genotype-environment analyses showed a strong association with temperature and topographic features, suggesting adaptation to localised thermal environments. We used a multivariate redundancy analysis to identify a range of putatively adapted loci associated with local environmental conditions.
Conclusions Divergent selection at the local-habitat scale as a result of dispersal limitations and environmental heterogeneity (including physical barriers) are likely contributors to adaptive divergence between the two
Fontainea species. Our findings have presented evidence to indicate that Southern and Coastal Fontainea were comprised of distinct genetic groups and ecotypes, that together may form a single species continuum, with further phenotype research suggested to confirm the current species boundaries. Proactive conservation actions, including assisted migration to enhance the resilience of populations lacking stress-tolerant single nucleotide polymorphisms (SNPs) may be required to secure the long-term future of both taxa. This is especially vital for the critically endangered Coastal Fontainea given projections of habitat decline for the species under future climate scenarios. -
more » « less
Abstract Genetic structure and phenotypic variation among populations are affected by both geographic distance and environmental variation across species' distributions. Understanding the relative contributions of isolation by distance (IBD) and isolation by environment (IBE) is important for elucidating population dynamics across habitats and ecological gradients. In this study, we compared phenotypic and genetic variation among Horned Lark (
Eremophila alpestris ) populations from 10 sites encompassing an elevational gradient from low‐elevation desert scrub in Death Valley (285 a.s.l.) to high‐elevation meadows in the White Mountains of the Sierra Nevada of California (greater than 3000 m a.s.l.). Using a ddRAD data set of 28,474 SNPs aligned to a high‐quality reference genome, we compared genetic structure with elevational, environmental, and spatial distance to quantify how different aspects of the landscape drive genomic and phenotypic differentiation in Horned Larks. We found larger‐bodied birds were associated with sites that had less seasonality and higher annual precipitation, and longer spurs occurred in soils with more clay and silt content, less sand, and finer fragments. Larks have large neo‐sex chromosomes, and we found that associations with elevation and environmental variation were much stronger among neo‐sex chromosomes compared to autosomes. Furthermore, we found that putative chromosomal translocations, fusions, and inversions were associated with elevation and may underlie local adaptation across an elevational gradient in Horned Larks. Our results suggest that genetic variation in Horned Larks is affected more by IBD than IBE, but specific phenotypes and genomic regions—particually on neo‐sex chromosomes—bear stronger associations with the environment.
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/hr/uhab059
