skip to main content

Title: Combining Experimental Evolution and Genomics to Understand How Seed Beetles Adapt to a Marginal Host Plant
Genes that affect adaptive traits have been identified, but our knowledge of the genetic basis of adaptation in a more general sense (across multiple traits) remains limited. We combined population-genomic analyses of evolve-and-resequence experiments, genome-wide association mapping of performance traits, and analyses of gene expression to fill this knowledge gap and shed light on the genomics of adaptation to a marginal host (lentil) by the seed beetle Callosobruchus maculatus. Using population-genomic approaches, we detected modest parallelism in allele frequency change across replicate lines during adaptation to lentil. Mapping populations derived from each lentil-adapted line revealed a polygenic basis for two host-specific performance traits (weight and development time), which had low to modest heritabilities. We found less evidence of parallelism in genotype-phenotype associations across these lines than in allele frequency changes during the experiments. Differential gene expression caused by differences in recent evolutionary history exceeded that caused by immediate rearing host. Together, the three genomic datasets suggest that genes affecting traits other than weight and development time are likely to be the main causes of parallel evolution and that detoxification genes (especially cytochrome P450s and beta-glucosidase) could be especially important for colonization of lentil by C. maculatus.
Authors:
; ; ; ; ; ; ;
Award ID(s):
1638768
Publication Date:
NSF-PAR ID:
10186578
Journal Name:
Genes
Volume:
11
Issue:
4
Page Range or eLocation-ID:
400
ISSN:
2073-4425
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    We measured the floral bud transcriptome of 151 fully sequenced lines of Mimulus guttatus from one natural population. Thousands of single nucleotide polymorphisms (SNPs) are implicated as transcription regulators, but there is a striking difference in the allele frequency spectrum of cis-acting and trans-acting mutations. Cis-SNPs have intermediate frequencies (consistent with balancing selection) while trans-SNPs exhibit a rare-alleles model (consistent with purifying selection). This pattern only becomes clear when transcript variation is normalized on a gene-to-gene basis. If a global normalization is applied, as is typically in RNAseq experiments, asymmetric transcript distributions combined with “rarity disequilibrium” produce a superabundance of false positives for trans-acting SNPs. To explore the cause of purifying selection on trans-acting mutations, we identified gene expression modules as sets of coexpressed genes. The extent to which trans-acting mutations influence modules is a strong predictor of allele frequency. Mutations altering expression of genes with high “connectedness” (those that are highly predictive of the representative module expression value) have the lowest allele frequency. The expression modules can also predict whole-plant traits such as flower size. We find that a substantial portion of the genetic (co)variance among traits can be described as an emergent property of genetic effects onmore »expression modules.

    « less
  2. Abstract

    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 Northeastmore »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.

    « less
  3. Hug, Laura A. (Ed.)
    ABSTRACT Secondary metabolite clusters (SMCs) encode the machinery for fungal toxin production. However, understanding their function and analyzing their products requires investigation of the developmental and environmental conditions in which they are expressed. Gene expression is often restricted to specific and unexamined stages of the life cycle. Therefore, we applied comparative genomics analyses to identify SMCs in Neurospora crassa and analyzed extensive transcriptomic data spanning nine independent experiments from diverse developmental and environmental conditions to reveal their life cycle-specific gene expression patterns. We reported 20 SMCs comprising 177 genes—a manageable set for investigation of the roles of SMCs across the life cycle of the fungal model N. crassa —as well as gene sets coordinately expressed in 18 predicted SMCs during asexual and sexual growth under three nutritional and two temperature conditions. Divergent activity of SMCs between asexual and sexual development was reported. Of 126 SMC genes that we examined for knockout phenotypes, al-2 and al-3 exhibited phenotypes in asexual growth and conidiation, whereas os-5 , poi-2 , and pmd-1 exhibited phenotypes in sexual development. SMCs with annotated function in mating and crossing were actively regulated during the switch between asexual and sexual growth. Our discoveries call for attention to rolesmore »that SMCs may play in the regulatory switches controlling mode of development, as well as the ecological associations of those developmental stages that may influence expression of SMCs. IMPORTANCE Secondary metabolites (SMs) are low-molecular-weight compounds that often mediate interactions between fungi and their environments. Fungi enriched with SMs are of significant research interest to agriculture and medicine, especially from the aspects of pathogen ecology and environmental epidemiology. However, SM clusters (SMCs) that have been predicted by comparative genomics alone have typically been poorly defined and insufficiently functionally annotated. Therefore, we have investigated coordinate expression in SMCs in the model system N. crassa , and our results suggest that SMCs respond to environmental signals and to stress that are associated with development. This study examined SMC regulation at the level of RNA to integrate observations and knowledge of these genes in various growth and development conditions, supporting combining comparative genomics and inclusive transcriptomics to improve computational annotation of SMCs. Our findings call for detailed study of the function of SMCs during the asexual-sexual switch, a key, often-overlooked developmental stage.« less
  4. Abstract Background

    Crop improvement through cross-population genomic prediction and genome editing requires identification of causal variants at high resolution, within fewer than hundreds of base pairs. Most genetic mapping studies have generally lacked such resolution. In contrast, evolutionary approaches can detect genetic effects at high resolution, but they are limited by shifting selection, missing data, and low depth of multiple-sequence alignments. Here we use genomic annotations to accurately predict nucleotide conservation across angiosperms, as a proxy for fitness effect of mutations.

    Results

    Using only sequence analysis, we annotate nonsynonymous mutations in 25,824 maize gene models, with information from bioinformatics and deep learning. Our predictions are validated by experimental information: within-species conservation, chromatin accessibility, and gene expression. According to gene ontology and pathway enrichment analyses, predicted nucleotide conservation points to genes in central carbon metabolism. Importantly, it improves genomic prediction for fitness-related traits such as grain yield, in elite maize panels, by stringent prioritization of fewer than 1% of single-site variants.

    Conclusions

    Our results suggest that predicting nucleotide conservation across angiosperms may effectively prioritize sites most likely to impact fitness-related traits in crops, without being limited by shifting selection, missing data, and low depth of multiple-sequence alignments. Our approach—Prediction of mutation Impact by Calibratedmore »Nucleotide Conservation (PICNC)—could be useful to select polymorphisms for accurate genomic prediction, and candidate mutations for efficient base editing. The trained PICNC models and predicted nucleotide conservation at protein-coding SNPs in maize are publicly available in CyVerse (https://doi.org/10.25739/hybz-2957).

    « less
  5. Humans cause widespread evolutionary change in nature, but we still know little about the genomic basis of rapid adaptation in the Anthropocene. We tracked genomic changes across all protein-coding genes in experimental fish populations that evolved pronounced shifts in growth rates due to size-selective harvest over only four generations. Comparisons of replicate lines show parallel allele frequency shifts that recapitulate responses to size-selection gradients in the wild across hundreds of unlinked variants concentrated in growth-related genes. However, a supercluster of genes also rose rapidly in frequency and dominated the evolutionary dynamic in one replicate line but not in others. Parallel phenotypic changes thus masked highly divergent genomic responses to selection, illustrating how contingent rapid adaptation can be in the face of strong human-induced selection.