Going beyond SNPs: The role of structural genomic variants in adaptive evolution and species diversification

Molecular Ecology, Journal Year: 2019, Volume and Issue: 28(6), P. 1203 - 1209

Published: March 1, 2019

Although single-nucleotide polymorphism (SNPs) were initially thought to make-up the majority of selectable variation (Morin, Luikart, & Wayne, 2004; Sachidanandam et al., 2001), it is becoming increasingly recognized that structural represents a significant, yet often poorly understood, source genetic variation. It only within past 10 years, aided by development genomic technologies such as high throughput and later third generation sequencing, extent intra- interspecific has been investigated in number nonmodel species (Chain Feulner, 2014; Fan Meyer, 2014). The term used define region DNA shows change copy (deletions, insertions duplications), orientation (inversions), or chromosomal location (translocations, fusions) between individuals. Structural may occur both coding noncoding gene genome, including highly repetitive elements, transposons. In other words, variants can be balanced show no specific loss gain information, inversions fragment translocations stretch chromosomes, they unbalanced, where part genome lost (insertions/deletions) duplicated (duplications), which termed (CNV). This Special Issue Molecular Ecology provides platform showcase highlight very recent progress understanding role adaptive evolution diversification. contributions are varied, covering animals plants, range from comparison different kind bioinformatic approaches characterize variants, experimental test adaptation diversification population-level studies document ecological determinants their significance nature. history goes back beginning this century, many years before scientists even had an what was. all started with discovery inversions, regions flipped orientation, leads suppression recombination inversion heterozygotes (Butlin, 2005; Dobzhansky Sturtevant, 1938). inverted was made when Alfred Sturtevant compared chromosome maps Drosophila melanogaster those D. simulans, closely related he described earlier (Sturtevant, 1913). He found interspecies similar, except for on chromosome, one large sequence 1921). follow, able obtain sufficient numbers mutants various inversion-containing chromosomes establish dominant crossover suppressors indeed (Sturtevant Mather, Afterwards, additional discovered variety species, notable transposable elements maize (e.g., McClintock, 1931, 1950). McClintock's work revolutionary suggested organism's not stationary entity, but rather subject alteration rearrangement changed way think about patterns inheritance. At time concept met criticism scientific community; however, transposons eventually became widely appreciated community accept replication does always follow consistent pattern. McClintock awarded Nobel Prize 1983 recognition her field genetics (Ravindran, 2012). Yet, starting 1970s, rich literature largely sank view rise molecular markers, microsatellites, amplified length (AFLPs) more recently SNPs. particular, latest techniques provide cheap, methods genotyping SNP markers Elshire 2011), leading being dominated However, present at significant frequencies populations contribute important processes. For example, evidence accumulating dosage heavily affected CNV profound effect functionality resulting evolutionary trajectories (Ha, Kim, Chen, 2009). CNVs go mostly undetected standard methods. Likewise, young sequencing analyses, because merely linear order bases breakpoints carry variants; consequences pronounced have long-term effects fitness genotypes (Wellenreuther Bernatchez, 2018). study gained momentum we currently witnessing major advances computational genomics quality whole-genome data assemblies available species. Furthermore, long-read optical mapping novel assembly algorithms now incredible resolution presence absence (Chakraborty 2018; Lee 2016). accompanied simultaneous fast improvements statistical tools together allow extraction reliable information phenotype Boetzer Pirovano, Koren Phillippy, 2015; 2017). Using these bioinformatics dissect nucleotide contained well unprecedented detail. As consequence discoveries, growing geneticists biologists shifted attention towards bigger complex alterations architecture thus going some oldest markers. witnessed dramatic increase reporting involvement several disorders (Sanchis-Juan Xia 24 articles Ecology, embody diverse collection systems, offer valuable lessons contribution Catanach, Deng, Charles, Wellenreuther (2019) highlights frequent nature nonrandom distribution underscoring emergent tenet sources fuel Specifically, use replicate Australasian snapper Chrysophrys auratus quantify locations prevalence SNPs varied sizes, showed while most common, base pairs almost three times higher indicates impact further supported finding sizeable portion located under putative selection, intersected genes. genome-wide also Lucek, Gompert, Nosil using mate-pair population framework stick insect Timema cristinae. authors describe numerous deletions, duplications throughout genome. detected approach, considers variant formerly described, reduced harbours genes controlling colour-pattern therewith accentuated differentiation ecotypes. prime example need beyond mere measure studying processes knowledge relevant understand intraspecific level during early divergence. They would expected priori involved ecotype differentiation, characteristics, size protect flow inversions) likelihood them others. Many fulfil criteria partly reason why seen surge popularity over last decade due clear association phenotypes, behaviour, mating strategies speciation first Cheng Kirkpatrick investigates intriguing observation taxa fix faster rate X autosomes. system X-linked larger than autosomal counterparts capture staggering 67% inversions. combine empirical result model showing same conditions favour fixation rates Together results indicate strongly influence sex chromosomes. Hooper, Griffith, Price explore two subspecies long-tailed finches integrating associated differences, bill colour. With this, detail Z-linked subspecies; find frequency cline coincide autosome nor colour; phenotypic difference subspecies. integrate findings argue could serve good candidates tightly linked reproductive isolation. special issue, Kapun Flatt revisit vinegar fruitfly melanogaster. Since original discovery, come indepth thorough review until today. include meta-analysis geographic four cosmopolitan worldwide clinality. put suggests balancing selection. Fuller, Koury, Phadnis, Schaeffer complementary research pseudoobscura persimilis, notably details suppressed heterozygotes. By summarizing body level, concludes underlie heterogeneous environments, governed how transition fixed differences Korunes Noor pair noncrossover conversion crosses. detect holds true, near breakpoints. considerably lower divergence, still similar collinear claim force us rethink affect build-up nuanced exchange occurring, level. That said, homogenisation remains limited fragments homogenized short overall rearrangement, true crossovers. Puig Giribets al. examine responses heat shock subobscura flies homokaryotypic warm-climate arrangement exhibit basal Hsp70 protein levels after treatment attained cold-climate counterpart. common pattern cytological location, cis-regulatory copies among evolve concert through conversion. concerted evolution, structured idiosyncratic across lineages barriers interchromosomal exchange. points previously unrealized link potentially implications evolution. Newly arisen disrupt existing via altering relative distance genes, impose constraints position size. Or alternatively, newly derived positively selected if promote intrachromosomal effects. A key problem systems selection inside hard identify typically strong linkage disequilibrium. technically challenging Ayala tries address applies GWAS approach causative malaria vector Anopheles gambiae. do measuring phenotypes desiccation resistance homokaryotypes performing pool-seq phenotypically extreme doing so basis proof-of-concept method genotype-phenotype rearrangement. Similar, Coughlan Willis empirically investigate known differentiate annual perennial forms yellow monkeyflower Mimulus guttatus. tested hypothesis loci contributing local should predate inversion, theoretically predicted (Kirkpatrick Barton, 2006). To mapped QTLs life traits differ M. guttatus distantly related, Interestingly, containing least inversion. few cases support date. Another long-standing challenge describing new characterisation Christmas characteristics combination short-read honeybee Apis mellifera. comparing lowland haplotypes conserved, indicating likely ancient altitude, chromosome. composed repeat sequences line formation process nonallelic homologous recombination. Faria another difficulty commonly encountered research, biased largest reported, makes difficult assess biological importance change. based disequilibrium combines analysis controlled crosses diversity field, less 17 polymorphic rearrangements coastal marine snail Littorina saxatilis. Most clinal habitats, suggestive adaptation. rigorously confirm nevertheless efficient means multiple relatively low cost. noted, ecotypes straightforward map, particularly characterized effective flow, Atlantic cod Gadus morhua. Barth idea mechanism maintaining isolation face flow. differed genetically distinct groups, tie suggest contributed divergence system. holistic demonstrates sometimes factors working generate Arostegui, Quinn, Seeb, McKinney associating specialisation migratory behaviour fluvial adfluvial rainbow trout Oncorhynchus mykiss. sampled wild occupying connected stream lake habitats Omy05 contains exerting control its streams migrated lake. behavioural sustains ecotypic diversity, direct straightforward. Inverted so-called supergenes. Here, Avril Purcell Brelsford Chapuisat supergene divergent social Alpine silver ant Formica selysi, colonies either headed single queens. differs whether cause arrest Their reveal asymmetry degree assortative generates unidirectional male-mediated monogynous polygynous forms. such, convincingly organization components dynamics Chromosomal fusions featured Issue, Wellband fusion 8 29, salmon (Salmo salar) populations. Such act akin reduce residing tributaries Miramichi River (Canada) resolve versus relationships report extremely weak structuring (Fst < 0.01) fail hierarchical structure river's main branches. investigating fusion, disequilibrium, heterozygosity fused unfused Moreover, karyotypes five stronger neutral summer precipitation. implicates despite differentiation. processes, independent river branching, influencing path stems reshaping structure. Nelson dissects tRNA ligase type fluctuating plant ligases mediate stress-responsive life-history traits, introduces mechanisms amplification. Prunier black cottonwood tree P. trichocarpa design custom hybridization array balsam poplar balsamifera, relate phenological characters. 34 individuals mixed-parentage families northern Quebec southern Saskatchewan 1,721 ca. 20,000 tested, identified 23 having connections ecophysiological traits. attribute disease south abiotic stress north. advance analysis, variation, demonstrating much (ca. 9% genes), identifying potential physiological roles detected. lead driven (TEs), ubiquitous virtually eukaryotes move (or jump) another. While next-generation opened opportunity TE scale, far comprised Dennenmoser studied transposon hybrid fish lineage ("invasive Cottus") parental Cottus rhenanus perifretum reference assembled long molecule PacBio reads. transposition bursts recombination-based revealed increased significantly, suggesting proliferated hundred generations since admixture began. appeared added remain assemble, making ascertain explain proliferation lineage. Lerat took advantage European consortium set TEs sample natural allowed "mobilome landscape" specific, geographical observed element abundance rate, candidate targets positive parallel temporal North American populations, play continents. Adrion, Begun, Hahn along classic America sampling six nine simulans latitudes America. nearly two-fold excess latitude total average allele Despite necessarily imply uncovered relationship TEs, chromatin state calls investigation. Schrader Schmitz examines ways disentangling basic underlying changes arise. discuss defence against activity environmental challenges, might invasive, pathogenic parasitic quickly adapt environments. Choudhury, Rogivue, Gugerli, Parisod rock-cress (Arabis alpina) enrichment recombinationally inert reflects inefficient removal purifying modify rate. interact fine scale 28 blocks up 5.5 Mb enriched ecologically functions cold salt stress. selective sweeps site spectrum haplotype These landscapes driving Lastly, Yoshida better selfish drive intragenomic conflict sterility Japan Sea (Gasterosteus nipponicus) Pacific Ocean sticklebacks (G. aculeatus) encoding heterochromatin-binding expression indicated over-expression retrotransposons, hence providing sterility. increasing awareness raw material resources speciation, slowly changing researchers analyse landscape Whereas considered rare, interindividual SNPs, variable tandem repeats small variants. inclusion ecology will complete On hand, critical isolating (Hooper 2019), facilitate coexistence (Arostegui 2019; Lucek contain (Ayala Willis, 2019). New showcased issue reduction potent accounted (Korunes Noor, When (TEs, sizes types mixed (Adrion Catanach outliers putatively plenty possibly elsewhere learned nature, consider simply longer ignored. Therefore, detection priority evaluate something become feasible cost technologies. current poor defining determine aspect help spread Accumulating disproportionate adaptation, bias, span unclear deserves future attention. ability accurately genotype make limitations, essentially any organism screened implications. MW drafted version paper, edited draft.

Language: Английский

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Chromosome fusions repatterned recombination rate and facilitated reproductive isolation during Pristionchus nematode speciation

Nature Ecology & Evolution, Journal Year: 2023, Volume and Issue: unknown

Published: Jan. 30, 2023

Abstract Large-scale genome-structural evolution is common in various organisms. Recent developments speciation genomics revealed the importance of inversions, whereas role other rearrangements, including chromosome fusions, have not been well characterized. We study genomic divergence and reproductive isolation closely related nematodes: androdioecious (hermaphroditic) model Pristionchus pacificus its dioecious sister species exspectatus . A chromosome-level genome assembly P. using single-molecule Hi-C sequencing a chromosome-wide rearrangement relative to Strikingly, characterization cytogenetic studies outgroup occultus indicated two independent fusions involving same chromosome, ChrIR, between these species. Genetic linkage analysis that altered pattern recombination, resulting large low-recombination regions probably facilitated coevolution some ~14.8% genes across entire genomes. Quantitative trait locus analyses for hybrid sterility all three sexes major quantitative loci mapped fused ChrIR. While abnormal segregations partially explain female sterility, hybrid-specific recombination breaks region was associated with male sterility. Thus, recent repatterned rate drove during speciation.

Language: Английский

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Hybridization increases population variation during adaptive radiation

Proceedings of the National Academy of Sciences, Journal Year: 2019, Volume and Issue: 116(46), P. 23216 - 23224

Published: Oct. 28, 2019

Adaptive radiations are prominent components of the world's biodiversity. They comprise many species derived from one or a small number ancestral in geologically short time that have diversified into variety ecological niches. Several authors proposed introgressive hybridization has been important generation new morphologies and even species, but how happens throughout evolutionary history is not known. Interspecific gene exchange expected to greatest impact on variation if it occurs after diverged genetically phenotypically before genetic incompatibilities arise. We use dated phylogeny infer populations Darwin's finches Galápagos became more variable morphological traits through time, consistent with hypothesis, then declined reaching peak. Some vary substantially than others. Phylogenetic inferences supported by field observations contemporary hybridization. Morphological effects investigated island Daphne Major documenting changes hybridizing Geospiza fortis scandens over 30-y period. G. showed evidence admixture Beaks progressively blunter, while length increased, depth decreased. These imply independent introgression 2, correlated, beak dimensions. Our study shows can alter ecologically traits, increase as radiation proceeds, enhance potential for future evolution changing environments.

Language: Английский

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Eukaryote hybrid genomes

PLoS Genetics, Journal Year: 2019, Volume and Issue: 15(11), P. e1008404 - e1008404

Published: Nov. 27, 2019

Interspecific hybridization is the process where closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that common, it may represent an important source of novel variation. Although most interspecific hybrids are sterile or less fit than their parents, some survive reproduce, enabling transfer adaptive variants across boundary, even result in formation evolutionary lineages. There two main hybrid genomes: allopolyploid, which have one full chromosome set from each parent species, homoploid, a mosaic genomes no increase number. establishment requires development reproductive isolation against parental species. Allopolyploid often strong intrinsic barriers due to differences number, homoploid can become reproductively isolated through assortment genetic incompatibilities. However, both types further isolated, gaining extrinsic barriers, by exploiting ecological niches, relative parents. Hybrids merging divergent thus face problems arising incompatible combinations genes. Thus highly dynamic undergo rapid change, including genome stabilization selection results fixation compatible ancestry block within potential for adaptation speciation makes particularly exciting subject biology. Here we summarize how introgressed alleles establish resulting evolve.

Language: Английский

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Avian Coloration Genetics: Recent Advances and Emerging Questions

Journal of Heredity, Journal Year: 2021, Volume and Issue: 112(5), P. 395 - 416

Published: March 23, 2021

Abstract The colorful phenotypes of birds have long provided rich source material for evolutionary biologists. Avian plumage, beaks, skin, and eggs—which exhibit a stunning range cryptic conspicuous forms—inspired early work on adaptive coloration. More recently, avian color has fueled discoveries the physiological, developmental, and—increasingly—genetic mechanisms responsible phenotypic variation. relative ease with which traits can be quantified made an attractive system uncovering links between phenotype genotype. Accordingly, field coloration genetics is burgeoning. In this review, we highlight recent advances emerging questions associated genetic underpinnings bird color. We start by describing breakthroughs related to 2 pigment classes: carotenoids that produce red, yellow, orange in most psittacofulvins similar colors parrots. then discuss structural colors, are produced interaction light nanoscale materials greatly extend plumage palette. Structural remain understudied—but paradigm changing. next explore how arise from interactions among pigmentary may controlled genes co-expressed or co-regulated. also identify opportunities investigate mediating within-feather micropatterning bare parts eggs. conclude spotlighting research areas—mechanistic vision production, speciation—that been invigorated insights, trend likely continue as new genomic approaches applied non-model species.

Language: Английский

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Comparative transcriptomics reveals candidate carotenoid color genes in an East African cichlid fish

BMC Genomics, Journal Year: 2020, Volume and Issue: 21(1)

Published: Jan. 16, 2020

Abstract Background Carotenoids contribute significantly to animal body coloration, including the spectacular color pattern diversity among fishes. Fish, as other animals, derive carotenoids from their diet. Following uptake, transport and metabolic conversion, allocated coloration are deposited in chromatophore cells of integument. The genes involved these processes largely unknown. Using RNA-Sequencing, we tested for differential gene expression between carotenoid-colored white skin regions a cichlid fish, Tropheus duboisi “Maswa”, identify associated with carotenoid-based integumentary coloration. To control positional differences that were independent presence/absence carotenoid conducted same analyses closely related population, which both white. Results A larger number ( n = 50) showed higher yellow compared tissue than vice versa 9). Of particular interest was elevated level bco2a samples, enzyme encoded by this catalyzes cleavage into colorless derivatives. set levels region included xanthophore formation (e.g., pax7 sox10 ), intracellular pigment mobilization tubb , vim kif5b well uptake scarb1 ) storage plin6 carotenoids, conversion lipids retinoids dgat2, pnpla2, akr1b1 dhrs ). Triglyceride concentrations similar regions. Extracts contained zeaxanthin, lutein beta-cryptoxanthin unidentified structures. Conclusion Our results suggest role Bco2 fish analogous previous findings birds. carotenoid-rich functions retinol lipid metabolism supports hypotheses concerning analogies shared mechanisms pathways. Overlaps sets differentially expressed (including dgat2 bscl2 faxdc2 retsatl present study previous, comparable studies species provide useful hints potential candidate genes.

Language: Английский

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Comparative studies on speciation: 30 years since Coyne and Orr

Evolution, Journal Year: 2021, Volume and Issue: 75(4), P. 764 - 778

Published: Jan. 25, 2021

Understanding the processes of population divergence and speciation remains a core question in evolutionary biology. For nearly hundred years geneticists have characterized reproductive isolation (RI) mechanisms specific barriers to gene flow required for species formation. The seminal work Coyne Orr provided first comprehensive comparative analysis speciation. By combining phylogenetic hypotheses range data with estimates genetic multiple RI across Drosophila, Orr's influential meta-analyses answered fundamental questions motivated new analyses that continue push field forward today. Now 30 later, we revisit five addressed by Orr, identifying results remain well supported others seem less robust data. We then consider future research, emphasis on areas where novel methods motivate potential progress. While literature biased towards Drosophila other model systems, are enthusiastic about field.

Language: Английский

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A mechanism for red coloration in vertebrates

Current Biology, Journal Year: 2022, Volume and Issue: 32(19), P. 4201 - 4214.e12

Published: Aug. 31, 2022

Language: Английский

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How Important Are Structural Variants for Speciation?

Genes, Journal Year: 2021, Volume and Issue: 12(7), P. 1084 - 1084

Published: July 17, 2021

Understanding the genetic basis of reproductive isolation is a central issue in study speciation. Structural variants (SVs); that is, structural changes DNA, including inversions, translocations, insertions, deletions, and duplications, are common broad range organisms have been hypothesized to play role Recent advances molecular statistical methods identified variants, especially underlying ecologically important traits; thus, suggesting these mutations contribute adaptation. However, contribution between species—and mechanism by which most often speciation—remain unclear. Here, we review (i) different mechanisms can generate or maintain isolation; (ii) patterns expected with mechanisms; (iii) relevant empirical examples each. We also summarize available sequencing bioinformatic detect variants. Lastly, suggest approaches new research directions help obtain more complete assessment

Language: Английский

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Extensive hybridization reveals multiple coloration genes underlying a complex plumage phenotype

Proceedings of the Royal Society B Biological Sciences, Journal Year: 2021, Volume and Issue: 288(1943), P. 20201805 - 20201805

Published: Jan. 20, 2021

Coloration is an important target of both natural and sexual selection. Discovering the genetic basis colour differences can help us to understand how this visually striking phenotype evolves. Hybridizing taxa with clear shallow genomic divergences are unusually tractable for associating coloration phenotypes their causal genotypes. Here, we leverage extensive admixture between two common North American woodpeckers—yellow-shafted red-shafted flickers—to identify bases six distinct plumage patches involving melanin carotenoid pigments. Comparisons flickers across approximately 7.25 million genome-wide SNPs show that these forms differ at only a small proportion genome (mean F ST = 0.008). Within few highly differentiated regions, 368 significantly associated four patches. These linked multiple genes known be involved in pigmentation. For example, gene ( CYP2J19 ) cause yellow red transitions other birds strongly versus wing tail feathers flickers. Additionally, our analyses suggest novel links coloration. Our finding patch-specific control adds growing body literature suggesting diversity animals could created through selection acting on combinations genes.

Language: Английский

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