Background Uncovering the mechanisms underlying rapid genetic adaptation can provide insight into adaptive evolution and shed light on conservation, invasive species control, and natural resource management. However, it can be difficult to experimentally explore rapid adaptation due to the challenges associated with propagating and maintaining species in captive environments for long periods of time. By contrast, many introduced species have experienced strong selection when colonizing environments that differ substantially from their native range and thus provide a “natural experiment” for studying rapid genetic adaptation. One such example occurred when sea lamprey (Petromyzon marinus), native to the northern Atlantic, naturally migrated into Lake Champlain and expanded their range into the Great Lakes via man-made shipping canals. Results Utilizing 368,886 genome-wide single nucleotide polymorphisms (SNPs), we calculated genome-wide levels of genetic diversity (i.e., heterozygosity and π) for sea lamprey collected from native (Connecticut River), native but recently colonized (Lake Champlain), and invasive (Lake Michigan) populations, assessed genetic differentiation between all populations, and identified candidate genes that responded to selection imposed by the novel environments. We observed a 14 and 24% reduction in genetic diversity in Lake Michigan and Lake Champlain populations, respectively, compared to individuals from the Connecticut River, suggesting that sea lamprey populations underwent a genetic bottleneck during colonization. Additionally, we identified 121 and 43 outlier genes in comparisons between Lake Michigan and Connecticut River and between Lake Champlain and Connecticut River, respectively. Six outlier genes that contained synonymous SNPs in their coding regions and two genes that contained nonsynonymous SNPs may underlie the rapid evolution of growth (i.e., GHR), reproduction (i.e., PGR, TTC25, STARD10), and bioenergetics (i.e., OXCT1, PYGL, DIN4, SLC25A15). Conclusions By identifying the genomic basis of rapid adaptation to novel environments, we demonstrate that populations of invasive species can be a useful study system for understanding adaptive evolution. Furthermore, the reduction in genome-wide levels of genetic diversity associated with colonization coupled with the identification of outlier genes underlying key life history traits known to have changed in invasive sea lamprey populations (e.g., growth, reproduction) illustrate the utility in applying genomic approaches for the successful management of introduced species.

Understanding the genetic bases of inbreeding depression, heterosis, and genetic load is integral to understanding how genetic diversity is maintained in natural populations. The Pacific oyster Crassostrea gigas, like many long-lived plants, has high fecundity and high early mortality (type-III survivorship), manifesting a large, overt, genetic load; the oyster harbors an even greater concealed genetic load revealed by inbreeding. Here, we map viability QTL (vQTL) in six interrelated F2 oyster families, using high-density linkage maps of single nucleotide polymorphisms generated by genotyping-by-sequencing (GBS) methods. Altogether, we detect 70 vQTL and provisionally infer 89 causal mutations, 11 to 20 per family. Genetic mortality caused by independent (unlinked) vQTL ranges from 94.2% to 97.8% across families, consistent with previous reports. High-density maps provide better resolution of genetic mechanisms, however. Models of one causal mutation present in both identical-by-descent (IBD) homozygotes and heterozygotes fit genotype frequencies at 37 vQTL; consistent with the mutation-selection balance theory of genetic load, 20 are highly deleterious, completely recessive mutations and 17 are less deleterious, partially dominant mutations. Another 22 vQTL require pairs of recessive or partially dominant causal mutations, half showing selection against recessive mutations linked in repulsion, producing pseudo-overdominance. Only eight vQTL appear to support the overdominance theory of genetic load, with deficiencies of both IBD homozygotes, but at least four of these are likely caused by pseudo-overdominance. Evidence for epistasis is absent. A high mutation rate, random genetic drift, and pseudo-overdominance may explain both the oyster’s extremely high genetic diversity and a high genetic load maintained primarily by mutation-selection balance.

Studies of linkage and linkage mapping have advanced genetic and biological knowledge for over 100 years. In addition to their growing role, today, in mapping phenotypes to genotypes, dense linkage maps can help to validate genome assemblies. Previously, we showed that 40% of scaffolds in the first genome assembly for the Pacific oyster Crassostrea gigas were chimeric, containing single nucleotide polymorphisms (SNPs) mapping to different linkage groups. Here, we merge 14 linkage maps constructed of SNPs generated from genotyping-by-sequencing (GBS) methods with five, previously constructed linkage maps, to create a compendium of nearly 69 thousand SNPs mapped with high confidence. We use this compendium to assess a recently available, chromosome-level assembly of the C. gigas genome, mapping SNPs in 275 of 301 contigs and comparing the ordering of these contigs, by linkage, to their assembly by Hi-C sequencing methods. We find that, while 26% of contigs contain chimeric blocks of SNPs, i.e. adjacent SNPs mapping to different linkage groups than the majority of SNPs in their contig, these apparent misassemblies amount to only 0.08% of the genome sequence. Furthermore, nearly 90% of 275 contigs mapped by linkage and sequencing are assembled identically; inconsistencies between the two assemblies for the remaining 10% of contigs appear to result from insufficient linkage information. Thus, our compilation of linkage maps strongly supports this chromosome-level assembly of the oyster genome. Finally, we use this assembly to estimate, for the first time in a Lophotrochozoan, genome-wide recombination rates and causes of variation in this fundamental process.

Introduced and invasive species make excellent natural experiments for investigating rapid evolution. Here, we describe the effects of genetic drift and rapid genetic adaptation in pink salmon (Oncorhynchus gorbuscha) that were accidentally introduced to the Great Lakes via a single introduction event 31-generations ago. Using whole-genome resequencing for 134 fish spanning five sample groups across the native and introduced range, we estimate that the progenitor population’s effective population size was 146,886 at the time of introduction, whereas the founding population’s effective population size was just 72—a 2040-fold decrease. As expected with a severe bottleneck, we show reductions in genome-wide measures of genetic diversity, specifically a 37.7% reduction in the number of SNPs and an 8.2% reduction in observed heterozygosity. Despite this decline in genetic diversity, we provide evidence for putative selection at 47 loci across multiple chromosomes in the introduced populations, including missense variants in genes associated with circadian rhythm, immunological response, and maturation, which match expected or known phenotypic changes in the Great Lakes. For one of these genes, we use a species-specific agent-based model to rule out genetic drift and conclude that a strong response to selection occurred in a period gene (per2) that plays a predominant role in determining an organism’s daily clock, matching large day length differences experienced by introduced salmon during important phenological periods. Together, these results inform how populations might evolve rapidly to new environments, even with a small pool of standing genetic variation.

1The resistance of bacteria, disease vectors, and pests to chemical controls has vast ecological, 2 economic, and human-health costs. In most cases, resistance is only detected after non-3 susceptible phenotypes have spread throughout the entire population. Detecting resistance in its 4 incipient stages, by comparison, provides time to implement preventative strategies. Incipient 5 resistance (IR) can be detected by coupling standard toxicology assays with large-scale gene 6 expression experiments. We apply this approach to a system where an invasive parasite, sea 7 lamprey (Petromyzon marinus), has been treated with the highly-effective pesticide 3-8 trifluoromethyl-4-nitrophenol (TFM) for 60 years. Toxicological experiments revealed that 9 lamprey from treated populations did not have higher survival to TFM exposure than lamprey 10 from their native range, demonstrating that full-fledged resistance has not yet evolved. In stark 11 contrast, we find hundreds of genes differentially expressed in response to TFM in the 12 population with the longest history of exposure, many of which relate to TFM's primary mode of 13 action, the uncoupling of oxidative phosphorylation. One gene critical to oxidative 14 phosphorylation, ATP5PB, which encodes subunit b of ATP synthase, was nearly fixed for 15 alternative alleles in comparisons between native and treated populations (FST > 9 SD from the 16 mean). A gene encoding an additional subunit of ATP synthase, ATP5F1B, was canalized for 17 high expression in treated populations, but remained plastic in response to treatment in sea 18 lamprey from the native range. These combined genomic and transcriptomic results illustrate that 19 an adaptive, genetic response to TFM is driving incipient resistance in a damaging pest species. 20 S3). Remarkably, when comparing samples treated with 0.3 mg/L TFM to control samples, we 113 found 336 genes that were differentially expressed (275 upregulated, 61 downregulated in 114 comparison to control individuals) in muscle tissue in the Lake Michigan population, dwarfing 115 the number of differentially expressed genes (DEGs) found in both the Lake Champlain (n = 21) 116 and the Connecticut River (n = 68) populations (Fig. 3A-C; Table S4). No DEGs were shared 117 among all three populations and different population responses were observed when lower 118 concentrations (i.e., 0.2 mg/L) of TFM were applied and when different tissues were examined 119 (Figures S2-S5). 120The primary mode of action for TFM is to uncouple oxidative phosphorylation in the 121 mitochondria resulting in severe ATP depletion and eventual death (25, 26, 32). Of the 336 122 DEGs identified in Lake Michigan, several genes were directly related to this mode of action 123 including CRCM1 (LogFC = 2.60), a calcium release-activated channel protein that controls the 124 influx of calcium into cells when depleted, and PLCD4 (LogFC = 2.41), an enzyme responsible 125 for hydrolyzing phosphatidylinositol 4,5-bisphosphate into two secondary messenger molecules, 126 one of which (...