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1. Museum Genomics of an Agricultural Super-Pest, the Colorado Potato Beetle, Leptinotarsa decemlineata (Chrysomelidae), Provides Evidence of Adaptation from Standing Variation

   https://doi.org/10.1093/icb/icac137  

   Cohen, Zachary P. ; François, Olivier ; Schoville, Sean D. ( August 2022 , Integrative and Comparative Biology)

   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.

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2. Genomic islands of divergence infer a phenotypic landscape in Pacific lamprey

   https://doi.org/https://doi.org/10.1111/mec.15605  

   Hess, JE ; Smith, JJ ; Timoshevskaya, N ; Baker, C ; Caudill, C ; Graves, D ; Keefer, M ; Kinziger, A ; Moser, M ; Porter, L ; et al ( October 2020 , Molecular ecology)

   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 spatiotemporalmore »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.« less
3. Genomics of sorghum local adaptation to a parasitic plant

   https://doi.org/10.1073/pnas.1908707117  

   Bellis, Emily S. ; Kelly, Elizabeth A. ; Lorts, Claire M. ; Gao, Huirong ; DeLeo, Victoria L. ; Rouhan, Germinal ; Budden, Andrew ; Bhaskara, Govinal B. ; Hu, Zhenbin ; Muscarella, Robert ; et al ( February 2020 , Proceedings of the National Academy of Sciences)

   Host–parasite coevolution can maintain high levels of genetic diversity in traits involved in species interactions. In many systems, host traits exploited by parasites are constrained by use in other functions, leading to complex selective pressures across space and time. Here, we study genome-wide variation in the staple cropSorghum bicolor(L.) Moench and its association with the parasitic weedStriga hermonthica(Delile) Benth., a major constraint to food security in Africa. We hypothesize that geographic selection mosaics across gradients of parasite occurrence maintain genetic diversity in sorghum landrace resistance. Suggesting a role in local adaptation to parasite pressure, multiple independent loss-of-function alleles at sorghumLOW GERMINATION STIMULANT 1 (LGS1)are broadly distributed among African landraces and geographically associated withS. hermonthicaoccurrence. However, low frequency of these alleles withinS. hermonthica-prone regions and their absence elsewhere implicate potential trade-offs restricting their fixation.LGS1is thought to cause resistance by changing stereochemistry of strigolactones, hormones that control plant architecture and below-ground signaling to mycorrhizae and are required to stimulate parasite germination. Consistent with trade-offs, we find signatures of balancing selection surroundingLGS1and other candidates from analysis of genome-wide associations with parasite distribution. Experiments with CRISPR–Cas9-edited sorghum further indicate that the benefit ofLGS1-mediated resistance strongly depends on parasite genotype and abiotic environment and comesmore »at the cost of reduced photosystem gene expression. Our study demonstrates long-term maintenance of diversity in host resistance genes across smallholder agroecosystems, providing a valuable comparison to both industrial farming systems and natural communities.

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4. Chromosome-Level Assembly of the Atlantic Silverside Genome Reveals Extreme Levels of Sequence Diversity and Structural Genetic Variation

   https://doi.org/10.1093/gbe/evab098  

   Tigano, Anna ; Jacobs, Arne ; Wilder, Aryn P ; Nand, Ankita ; Zhan, Ye ; Dekker, Job ; Therkildsen, Nina Overgaard ( June 2021 , Genome Biology and Evolution)

   Lohmueller, Kirk (Ed.)

   Abstract The levels and distribution of standing genetic variation in a genome can provide a wealth of insights about the adaptive potential, demographic history, and genome structure of a population or species. As structural variants are increasingly associated with traits important for adaptation and speciation, investigating both sequence and structural variation is essential for wholly tapping this potential. Using a combination of shotgun sequencing, 10x Genomics linked reads and proximity-ligation data (Chicago and Hi-C), we produced and annotated a chromosome-level genome assembly for the Atlantic silverside (Menidia menidia)—an established ecological model for studying the phenotypic effects of natural and artificial selection—and examined patterns of genomic variation across two individuals sampled from different populations with divergent local adaptations. Levels of diversity varied substantially across each chromosome, consistently being highly elevated near the ends (presumably near telomeric regions) and dipping to near zero around putative centromeres. Overall, our estimate of the genome-wide average heterozygosity in the Atlantic silverside is among the highest reported for a fish, or any vertebrate (1.32–1.76% depending on inference method and sample). Furthermore, we also found extreme levels of structural variation, affecting ∼23% of the total genome sequence, including multiple large inversions (> 1 Mb and up to 12.6 Mb)more »associated with previously identified haploblocks showing strong differentiation between locally adapted populations. These extreme levels of standing genetic variation are likely associated with large effective population sizes and may help explain the remarkable adaptive divergence among populations of the Atlantic silverside.« less
5. Insights from a comprehensive study of Trypanosoma cruzi: A new mitochondrial clade restricted to North and Central America and genetic structure of TcI in the region

   https://doi.org/10.1371/journal.pntd.0010043  

   Lima-Cordón, Raquel Asunción ; Cahan, Sara Helms ; McCann, Cai ; Dorn, Patricia L. ; Justi, Silvia Andrade ; Rodas, Antonieta ; Monroy, María Carlota ; Stevens, Lori ( December 2021 , PLOS Neglected Tropical Diseases)

   Dutra, Walderez O. (Ed.)

   More than 100 years since the first description of Chagas Disease and with over 29,000 new cases annually due to vector transmission (in 2010), American Trypanosomiasis remains a Neglected Tropical Disease (NTD). This study presents the most comprehensive Trypanosoma cruzi sampling in terms of geographic locations and triatomine species analyzed to date and includes both nuclear and mitochondrial genomes. This addresses the gap of information from North and Central America. We incorporate new and previously published DNA sequence data from two mitochondrial genes, Cytochrome oxidase II (COII) and NADH dehydrogenase subunit 1 (ND1). These T . cruzi samples were collected over a broad geographic range including 111 parasite DNA samples extracted from triatomines newly collected across North and Central America, all of which were infected with T . cruzi in their natural environment. In addition, we present parasite reduced representation (Restriction site Associated DNA markers, RAD-tag) genomic nuclear data combined with the mitochondrial gene sequences for a subset of the triatomines (27 specimens) collected from Guatemala and El Salvador. Our mitochondrial phylogenetic reconstruction revealed two of the major mitochondrial lineages circulating across North and Central America, as well as the first ever mitochondrial data for TcBat from a triatomine collectedmore »in Central America. Our data also show that within mtTcIII, North and Central America represent an independent, distinct clade from South America, named here as mtTcIII NA-CA , geographically restricted to North and Central America. Lastly, the most frequent lineage detected across North and Central America, mtTcI, was also an independent, distinct clade from South America, noted as mtTcI NA-CA . Furthermore, nuclear genome data based on Single Nucleotide Polymorphism (SNP) showed genetic structure of lineage TcI from specimens collected in Guatemala and El Salvador supporting the hypothesis that genetic diversity at a local scale has a geographical component. Our multiscale analysis contributes to the understanding of the independent and distinct evolution of T . cruzi lineages in North and Central America regions.« less