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1. Founder effects shape linkage disequilibrium and genomic diversity of a partially clonal invader

   https://doi.org/10.1111/mec.15854  

   Flanagan, Ben A. ; Krueger‐Hadfield, Stacy A. ; Murren, Courtney J. ; Nice, Chris C. ; Strand, Allan E. ; Sotka, Erik E. ( April 2021 , Molecular Ecology)

   The genomic variation of an invasive species may be affected by complex demographic histories and evolutionary changes during the invasion. Here, we describe the relative influence of bottlenecks, clonality, and population expansion in determining genomic variability of the widespread red macroalgaAgarophyton vermiculophyllum. Its introduction from mainland Japan to the estuaries of North America and Europe coincided with shifts from predominantly sexual to partially clonal reproduction and rapid adaptive evolution. A survey of 62,285 SNPs for 351 individuals from 35 populations, aligned to 24 chromosome‐length scaffolds indicate that linkage disequilibrium (LD), observed heterozygosity (H_o), Tajima's D, and nucleotide diversity (Pi) were greater among non‐native than native populations. Evolutionary simulations indicate LD and Tajima's D were consistent with a severe population bottleneck. Also, the increased rate of clonal reproduction in the non‐native range could not have produced the observed patterns by itself but may have magnified the bottleneck effect on LD. Elevated marker diversity in the genetic source populations could have contributed to the increasedH_oand Pi observed in the non‐native range. We refined the previous invasion source region to a ~50 km section of northeastern Honshu Island. Outlier detection methods failed to reveal any consistently differentiated loci shared among invaded regions, probably because of the complexA. vermiculophyllumdemographic history. Our results reinforce the importance of demographic history, specifically founder effects, in driving genomic variation of invasive populations, even when localized adaptive evolution and reproductive system shifts are observed.

    

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2. Demographic history and genomic signatures of selection in a widespread vertebrate ectotherm

   https://doi.org/10.1111/mec.17269  

   Judson, Jessica M. ; Hoekstra, Luke A. ; Janzen, Fredric J. ( January 2024 , Molecular Ecology)

   Environmental conditions vary greatly across large geographic ranges, and yet certain species inhabit entire continents. In such species, genomic sequencing can inform our understanding of colonization history and the impact of selection on the genome as populations experience diverse local environments. As ectothermic vertebrates are among the most vulnerable to environmental change, it is critical to understand the contributions of local adaptation to population survival. Widespread ectotherms offer an opportunity to explore how species can successfully inhabit such differing environments and how future climatic shifts will impact species' survival. In this study, we investigated the widespread painted turtle (Chrysemys picta) to assess population genomic structure, demographic history, and genomic signatures of selection in the western extent of the range. We found support for a substantial role of serial founder effects in shaping population genomic structure: demographic analysis and runs of homozygosity were consistent with bottlenecks of increasing severity from eastern to western populations during and following the Last Glacial Maximum, and edge populations were more strongly diverged and had less genetic diversity than those from the centre of the range. We also detected outlier loci, but allelic patterns in many loci could be explained by either genetic surfing or selection. While range expansion complicates the identification of loci under selection, we provide candidates for future study of local adaptation in a long‐lived, widespread ectotherm that faces an uncertain future as the global climate continues to rapidly change.

    

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3. Geographic cline analysis as a tool for studying genome‐wide variation: a case study of pollinator‐mediated divergence in a monkeyflower

   https://doi.org/10.1111/mec.13645  

   Stankowski, Sean ; Sobel, James M. ; Streisfeld, Matthew A. ( June 2016 , Molecular Ecology)

   A major goal of speciation research is to reveal the genomic signatures that accompany the speciation process. Genome scans are routinely used to explore genome‐wide variation and identify highly differentiated loci that may contribute to ecological divergence, but they do not incorporate spatial, phenotypic or environmental data that might enhance outlier detection. Geographic cline analysis provides a potential framework for integrating diverse forms of data in a spatially explicit framework, but has not been used to study genome‐wide patterns of divergence. Aided by a first‐draft genome assembly, we combined anF_CTscan and geographic cline analysis to characterize patterns of genome‐wide divergence between divergent pollination ecotypes ofMimulus aurantiacus.F_CTanalysis of 58 872SNPs generated viaRAD‐seq revealed little ecotypic differentiation (meanF_CT = 0.041), although a small number of loci were moderately‐to‐highly diverged. Consistent with our previous results from the geneMaMyb2, which contributes to differences in flower colour, 130 loci have cline shapes that recapitulate the spatial pattern of trait divergence, suggesting that they may reside in or near the genomic regions that contribute to pollinator isolation. In the narrow hybrid zone between the ecotypes, extensive admixture among individuals and low linkage disequilibrium between markers indicate that most outlier loci are scattered throughout the genome, rather than being restricted to one or a few divergent regions. In addition to revealing the genomic consequences of ecological divergence in this system, we discuss how geographic cline analysis is a powerful but under‐utilized framework for studying genome‐wide patterns of divergence.

    

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4. Steep, coincident, and concordant clines in mitochondrial and nuclear‐encoded genes in a hybrid zone between subspecies of Atlantic killifish, Fundulus heteroclitus

   https://doi.org/10.1002/ece3.2324  

   McKenzie, Jessica L. ; Dhillon, Rashpal S. ; Schulte, Patricia M. ( July 2016 , Ecology and Evolution)

   Steep genetic clines resulting from recent secondary contact between previously isolated taxa can either gradually erode over time or be stabilized by factors such as ecological selection or selection against hybrids. We used patterns of variation in 30 nuclear and two mitochondrialSNPs to examine the factors that could be involved in stabilizing clines across a hybrid zone between two subspecies of the Atlantic killifish,Fundulus heteroclitus. Increased heterozygote deficit and cytonuclear disequilibrium in populations near the center of the mtDNAcline suggest that some form of reproductive isolation such as assortative mating or selection against hybrids may be acting in this hybrid zone. However, only a small number of loci exhibited these signatures, suggesting locus‐specific, rather than genomewide, factors. Fourteen of the 32 loci surveyed had cline widths inconsistent with neutral expectations, with twoSNPs in the mitochondrial genome exhibiting the steepest clines. Seven of the 12 putatively non‐neutral nuclear clines were forSNPs in genes related to oxidative metabolism. Among these putatively non‐neutral nuclear clines,SNPs in two nuclear‐encoded mitochondrial genes (SLC25A3 andHDDC2), as well asSNPs in the myoglobin, 40S ribosomal protein S17, and actin‐bindingLIMprotein genes, had clines that were coincident and concordant with the mitochondrial clines. When hybrid index was calculated using this subset of loci, the frequency distribution of hybrid indices for a population located at the mtDNAcline center was non‐unimodal, suggesting selection against advanced‐generation hybrids, possibly due to effects on processes involved in oxidative metabolism.

    

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5. Parallel evolution of gene classes, but not genes: Evidence from Hawai'ian honeycreeper populations exposed to avian malaria

   https://doi.org/10.1111/mec.14891  

   Cassin‐Sackett, Loren ; Callicrate, Taylor E. ; Fleischer, Robert C. ( November 2018 , Molecular Ecology)

   Adaptation in nature is ubiquitous, yet characterizing its genomic basis is difficult because population demographics cause correlations with nonadaptive loci. Introduction events provide opportunities to observe adaptation over known spatial and temporal scales, facilitating the identification of genes involved in adaptation. The pathogen causing avian malaria,Plasmodium relictum, was introduced to Hawai'i in the 1930s and elicited extinctions and precipitous population declines in native honeycreepers. After a sharp initial population decline, the Hawai'i ‘amakihi (Chlorodrepanis virens) has evolved tolerance to the parasite at low elevations whereP. relictumexists, and can sustain infection without major fitness consequences. High‐elevation, unexposed populations of ‘amakihi display little to no tolerance. To explore the genomic basis of adaptation toP. relictumin low‐elevation ‘amakihi, we genotyped 125 ‘amakihi from the island of Hawai'i via hybridization capture to 40,000 oligonucleotide baits containingSNPs and used the reference ‘amakihi genome to identify genes potentially under selection from malaria. We tested for outlier loci between low‐ and high‐elevation population pairs and identified loci with signatures of selection within low‐elevation populations. In some cases, genes commonly involved in the immune response (e.g., major histocompatibility complex) were associated with malaria presence in the population. We also detected several novel candidate loci that may be implicated in surviving malaria infection (e.g., beta‐defensin, glycoproteins and interleukin‐related genes). Our results suggest that rapid adaptation to pathogens may occur through changes in different immune genes, but in the same classes of genes, across populations.

    

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