Population Genomic Analysis of a Pitviper Reveals Microevolutionary Forces Underlying Venom Chemistry.

Abstract:

:Venoms are among the most biologically active secretions known, and are commonly believed to evolve under extreme positive selection. Many venom gene families, however, have undergone duplication, and are often deployed in doses vastly exceeding the LD50 for most prey species, which should reduce the strength of positive selection. Here, we contrast these selective regimes using snake venoms, which consist of rapidly evolving protein formulations. Though decades of extensive studies have found that snake venom proteins are subject to strong positive selection, the greater action of drift has been hypothesized, but never tested. Using a combination of de novo genome sequencing, population genomics, transcriptomics, and proteomics, we compare the two modes of evolution in the pitviper, Protobothrops mucrosquamatus. By partitioning selective constraints and adaptive evolution in a McDonald-Kreitman-type framework, we find support for both hypotheses: venom proteins indeed experience both stronger positive selection, and lower selective constraint than other genes in the genome. Furthermore, the strength of selection may be modulated by expression level, with more abundant proteins experiencing weaker selective constraint, leading to the accumulation of more deleterious mutations. These findings show that snake venoms evolve by a combination of adaptive and neutral mechanisms, both of which explain their extraordinarily high rates of molecular evolution. In addition to positive selection, which optimizes efficacy of the venom in the short term, relaxed selective constraints for deleterious mutations can lead to more rapid turnover of individual proteins, and potentially to exploration of a larger venom phenotypic space.

journal_name

Genome Biol Evol

authors

Aird SD,Arora J,Barua A,Qiu L,Terada K,Mikheyev AS

doi

10.1093/gbe/evx199

subject

Has Abstract

pub_date

2017-10-01 00:00:00

pages

2640-2649

issue

10

issn

1759-6653

pii

4259791

journal_volume

9

pub_type

杂志文章
  • Network-Based Analysis of eQTL Data to Prioritize Driver Mutations.

    abstract::In clonal systems, interpreting driver genes in terms of molecular networks helps understanding how these drivers elicit an adaptive phenotype. Obtaining such a network-based understanding depends on the correct identification of driver genes. In clonal systems, independent evolved lines can acquire a similar adaptive...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evw010

    authors: De Maeyer D,Weytjens B,De Raedt L,Marchal K

    更新日期:2016-01-23 00:00:00

  • Distinctive Genome Reduction Rates Revealed by Genomic Analyses of Two Coxiella-Like Endosymbionts in Ticks.

    abstract::Genome reduction is a hallmark of symbiotic genomes, and the rate and patterns of gene loss associated with this process have been investigated in several different symbiotic systems. However, in long-term host-associated coevolving symbiont clades, the genome size differences between strains are normally quite small ...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evv108

    authors: Gottlieb Y,Lalzar I,Klasson L

    更新日期:2015-05-28 00:00:00

  • Nonlinear dynamics of nonsynonymous (dN) and synonymous (dS) substitution rates affects inference of selection.

    abstract::Selection modulates gene sequence evolution in different ways by constraining potential changes of amino acid sequences (purifying selection) or by favoring new and adaptive genetic variants (positive selection). The number of nonsynonymous differences in a pair of protein-coding sequences can be used to quantify the ...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evp030

    authors: Wolf JB,Künstner A,Nam K,Jakobsson M,Ellegren H

    更新日期:2009-08-13 00:00:00

  • Multiple Roots of Fruiting Body Formation in Amoebozoa.

    abstract::Establishment of multicellularity represents a major transition in eukaryote evolution. A subgroup of Amoebozoa, the dictyosteliids, has evolved a relatively simple aggregative multicellular stage resulting in a fruiting body supported by a stalk. Protosteloid amoeba, which are scattered throughout the amoebozoan tree...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evy011

    authors: Hillmann F,Forbes G,Novohradská S,Ferling I,Riege K,Groth M,Westermann M,Marz M,Spaller T,Winckler T,Schaap P,Glöckner G

    更新日期:2018-02-01 00:00:00

  • Comparative Genomics of All Three Campylobacter sputorum Biovars and a Novel Cattle-Associated C. sputorum Clade.

    abstract::Campylobacter sputorum is a nonthermotolerant campylobacter that is primarily isolated from food animals such as cattle and sheep. C. sputorum is also infrequently associated with human illness. Based on catalase and urease activity, three biovars are currently recognized within C. sputorum: bv. sputorum (catalase neg...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evx112

    authors: Miller WG,Yee E,Chapman MH,Bono JL

    更新日期:2017-06-01 00:00:00

  • Centromere remodeling in Hoolock leuconedys (Hylobatidae) by a new transposable element unique to the gibbons.

    abstract::Gibbons (Hylobatidae) shared a common ancestor with the other hominoids only 15-18 million years ago. Nevertheless, gibbons show very distinctive features that include heavily rearranged chromosomes. Previous observations indicate that this phenomenon may be linked to the attenuated epigenetic repression of transposab...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evs048

    authors: Carbone L,Harris RA,Mootnick AR,Milosavljevic A,Martin DI,Rocchi M,Capozzi O,Archidiacono N,Konkel MK,Walker JA,Batzer MA,de Jong PJ

    更新日期:2012-01-01 00:00:00

  • Nephromyces Encodes a Urate Metabolism Pathway and Predicted Peroxisomes, Demonstrating That These Are Not Ancient Losses of Apicomplexans.

    abstract::The phylum Apicomplexa is a quintessentially parasitic lineage, whose members infect a broad range of animals. One exception to this may be the apicomplexan genus Nephromyces, which has been described as having a mutualistic relationship with its host. Here we analyze transcriptome data from Nephromyces and its parasi...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evy251

    authors: Paight C,Slamovits CH,Saffo MB,Lane CE

    更新日期:2019-01-01 00:00:00

  • Evolution of Sphingomonad Gene Clusters Related to Pesticide Catabolism Revealed by Genome Sequence and Mobilomics of Sphingobium herbicidovorans MH.

    abstract::Bacterial degraders of chlorophenoxy herbicides have been isolated from various ecosystems, including pristine environments. Among these degraders, the sphingomonads constitute a prominent group that displays versatile xenobiotic-degradation capabilities. Four separate sequencing strategies were required to provide th...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evx185

    authors: Nielsen TK,Rasmussen M,Demanèche S,Cecillon S,Vogel TM,Hansen LH

    更新日期:2017-09-01 00:00:00

  • Evolutionary Dynamics of Regulatory Changes Underlying Gene Expression Divergence among Saccharomyces Species.

    abstract::Heritable changes in gene expression are important contributors to phenotypic differences within and between species and are caused by mutations in cis-regulatory elements and trans-regulatory factors. Although previous work has suggested that cis-regulatory differences preferentially accumulate with time, technical r...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evx035

    authors: Metzger BPH,Wittkopp PJ,Coolon JD

    更新日期:2017-04-01 00:00:00

  • Expansion and Functional Divergence of the SHORT VEGETATIVE PHASE (SVP) Genes in Eudicots.

    abstract::SHORT VEGETATIVE PHASE (SVP) genes are members of the well-known MADS-box gene family that regulates vital developmental processes in plants. In Arabidopsis, there are two SVP paralogs, SVP/AGAMOUS-LIKE22 (SVP/AGL22) and AGL24. SVP protein suppresses the flowering process, whereas AGL24 acts as a flowering activator. ...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evy235

    authors: Liu X,Sun Z,Dong W,Wang Z,Zhang L

    更新日期:2018-11-01 00:00:00

  • Sex Chromosome Evolution: So Many Exceptions to the Rules.

    abstract::Genomic analysis of many nonmodel species has uncovered an incredible diversity of sex chromosome systems, making it possible to empirically test the rich body of evolutionary theory that describes each stage of sex chromosome evolution. Classic theory predicts that sex chromosomes originate from a pair of homologous ...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evaa081

    authors: Furman BLS,Metzger DCH,Darolti I,Wright AE,Sandkam BA,Almeida P,Shu JJ,Mank JE

    更新日期:2020-06-01 00:00:00

  • The genomic signal of partial sweeps in Mimulus guttatus.

    abstract::The molecular signature of selection depends strongly on whether new mutations are immediately favorable and sweep to fixation (hard sweeps) as opposed to when selection acts on segregating variation (soft sweeps). The prediction of reduced sequence variation around selected polymorphisms is much stronger for hard tha...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evt100

    authors: Kelly JK,Koseva B,Mojica JP

    更新日期:2013-01-01 00:00:00

  • Contrasting Patterns of Genomic Diversity Reveal Accelerated Genetic Drift but Reduced Directional Selection on X-Chromosome in Wild and Domestic Sheep Species.

    abstract::Analyses of genomic diversity along the X chromosome and of its correlation with autosomal diversity can facilitate understanding of evolutionary forces in shaping sex-linked genomic architecture. Strong selective sweeps and accelerated genetic drift on the X-chromosome have been inferred in primates and other model s...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evy085

    authors: Chen ZH,Zhang M,Lv FH,Ren X,Li WR,Liu MJ,Nam K,Bruford MW,Li MH

    更新日期:2018-04-01 00:00:00

  • The Accelerated Evolution of Lagging Strand Genes Is Independent of Sequence Context.

    abstract::We previously discovered that lagging strand genes evolve faster in Bacillus subtilis (and potentially other bacteria). Lagging strand genes are transcribed in the head-on orientation with respect to DNA replication, leading to collisions between the two machineries that stall replication and can destabilize genomes. ...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evw274

    authors: Merrikh CN,Weiss E,Merrikh H

    更新日期:2016-12-01 00:00:00

  • Selfish Mitochondrial DNA Proliferates and Diversifies in Small, but not Large, Experimental Populations of Caenorhabditis briggsae.

    abstract::Evolutionary interactions across levels of biological organization contribute to a variety of fundamental processes including genome evolution, reproductive mode transitions, species diversification, and extinction. Evolutionary theory predicts that so-called "selfish" genetic elements will proliferate when the host e...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evv116

    authors: Phillips WS,Coleman-Hulbert AL,Weiss ES,Howe DK,Ping S,Wernick RI,Estes S,Denver DR

    更新日期:2015-06-24 00:00:00

  • The Huperzia selago Shoot Tip Transcriptome Sheds New Light on the Evolution of Leaves.

    abstract::Lycopodiophyta-consisting of three orders, Lycopodiales, Isoetales and Selaginellales, with different types of shoot apical meristems (SAMs)-form the earliest branch among the extant vascular plants. They represent a sister group to all other vascular plants, from which they differ in that their leaves are microphylls...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evx169

    authors: Evkaikina AI,Berke L,Romanova MA,Proux-Wéra E,Ivanova AN,Rydin C,Pawlowski K,Voitsekhovskaja OV

    更新日期:2017-09-01 00:00:00

  • Developmental Constraints on Genome Evolution in Four Bilaterian Model Species.

    abstract::Developmental constraints on genome evolution have been suggested to follow either an early conservation model or an "hourglass" model. Both models agree that late development strongly diverges between species, but debate on which developmental period is the most conserved. Here, based on a modified "Transcriptome Age...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evy177

    authors: Liu J,Robinson-Rechavi M

    更新日期:2018-09-01 00:00:00

  • Mitochondrial Genome Evolution and a Novel RNA Editing System in Deep-Branching Heteroloboseids.

    abstract::Discoba (Excavata) is an evolutionarily important group of eukaryotes that includes Jakobida, with the most bacterial-like mitochondrial genomes known, and Euglenozoa, many of which have extensively fragmented mitochondrial genomes. However, little is known about the mitochondrial genomes of Heterolobosea, the third m...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evx086

    authors: Yang J,Harding T,Kamikawa R,Simpson AGB,Roger AJ

    更新日期:2017-05-01 00:00:00

  • Extensive Capsule Locus Variation and Large-Scale Genomic Recombination within the Klebsiella pneumoniae Clonal Group 258.

    abstract::Klebsiella pneumoniae clonal group (CG) 258, comprising sequence types (STs) 258, 11, and closely related variants, is associated with dissemination of the K. pneumoniae carbapenemase (KPC). Hospital outbreaks of KPC CG258 infections have been observed globally and are very difficult to treat. As a consequence, there ...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evv062

    authors: Wyres KL,Gorrie C,Edwards DJ,Wertheim HF,Hsu LY,Van Kinh N,Zadoks R,Baker S,Holt KE

    更新日期:2015-04-10 00:00:00

  • A broad genomic survey reveals multiple origins and frequent losses in the evolution of respiratory hemerythrins and hemocyanins.

    abstract::Hemerythrins and hemocyanins are respiratory proteins present in some of the most ecologically diverse animal lineages; however, the precise evolutionary history of their enzymatic domains (hemerythrin, hemocyanin M, and tyrosinase) is still not well understood. We survey a wide dataset of prokaryote and eukaryote gen...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evt102

    authors: Martín-Durán JM,de Mendoza A,Sebé-Pedrós A,Ruiz-Trillo I,Hejnol A

    更新日期:2013-01-01 00:00:00

  • Trends in the Evolution of Snake Toxins Underscored by an Integrative Omics Approach to Profile the Venom of the Colubrid Phalotris mertensi.

    abstract::Only few studies on snake venoms were dedicated to deeply characterize the toxin secretion of animals from the Colubridae family, despite the fact that they represent the majority of snake diversity. As a consequence, some evolutionary trends observed in venom proteins that underpinned the evolutionary histories of sn...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evw149

    authors: Campos PF,Andrade-Silva D,Zelanis A,Paes Leme AF,Rocha MM,Menezes MC,Serrano SM,Junqueira-de-Azevedo Ide L

    更新日期:2016-08-16 00:00:00

  • The potential role of sexual conflict and sexual selection in shaping the genomic distribution of Mito-nuclear genes.

    abstract::Mitochondrial interactions with the nuclear genome represent one of life's most important co-evolved mutualisms. In many organisms, mitochondria are maternally inherited, and in these cases, co-transmission between the mitochondrial and nuclear genes differs across different parts of the nuclear genome, with genes on ...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evu063

    authors: Dean R,Zimmer F,Mank JE

    更新日期:2014-05-01 00:00:00

  • Nonrandom survival of gene conversions among yeast ribosomal proteins duplicated through genome doubling.

    abstract::By comparing the patterns of evolution in the coding and upstream noncoding regions of yeast ribosomal protein (RP) genes duplicated in a genome duplication, we find that although nonsynonymous sites in the coding sequences show strong evidence for the fixation of recent gene conversion events, similar patterns are le...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evq067

    authors: Evangelisti AM,Conant GC

    更新日期:2010-01-01 00:00:00

  • Gene frequency distributions reject a neutral model of genome evolution.

    abstract::Evolution of prokaryotes involves extensive loss and gain of genes, which lead to substantial differences in the gene repertoires even among closely related organisms. Through a wide range of phylogenetic depths, gene frequency distributions in prokaryotic pangenomes bear a characteristic, asymmetrical U-shape, with a...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evt002

    authors: Lobkovsky AE,Wolf YI,Koonin EV

    更新日期:2013-01-01 00:00:00

  • Defense Response in Brazilian Honey Bees (Apis mellifera scutellata × spp.) Is Underpinned by Complex Patterns of Admixture.

    abstract::In 1957, an invasive and highly defensive honey bee began to spread across Brazil. In the previous year, Brazilian researchers hoped to produce a subtropical-adapted honey bee by crossing local commercial honey bees (of European origin) with a South African honey bee subspecies (Apis mellifera scutellata; an A-lineage...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evaa128

    authors: Harpur BA,Kadri SM,Orsi RO,Whitfield CW,Zayed A

    更新日期:2020-08-01 00:00:00

  • Phylogenomic data support a seventh order of Methylotrophic methanogens and provide insights into the evolution of Methanogenesis.

    abstract::Increasing evidence from sequence data from various environments, including the human gut, suggests the existence of a previously unknown putative seventh order of methanogens. The first genomic data from members of this lineage, Methanomassiliicoccus luminyensis and "Candidatus Methanomethylophilus alvus," provide in...

    journal_title:Genome biology and evolution

    pub_type: 信件

    doi:10.1093/gbe/evt128

    authors: Borrel G,O'Toole PW,Harris HM,Peyret P,Brugère JF,Gribaldo S

    更新日期:2013-01-01 00:00:00

  • Sex-Biased Gene Expression and Dosage Compensation on the Artemia franciscana Z-Chromosome.

    abstract::Males and females of Artemia franciscana, a crustacean commonly used in the aquarium trade, are highly dimorphic. Sex is determined by a pair of ZW chromosomes, but the nature and extent of differentiation of these chromosomes is unknown. Here, we characterize the Z chromosome by detecting genomic regions that show lo...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evz053

    authors: Huylmans AK,Toups MA,Macon A,Gammerdinger WJ,Vicoso B

    更新日期:2019-04-01 00:00:00

  • Reconstructing the Phylogeny of Corynebacteriales while Accounting for Horizontal Gene Transfer.

    abstract::Horizontal gene transfer is a common mechanism in Bacteria that has contributed to the genomic content of existing organisms. Traditional methods for estimating bacterial phylogeny, however, assume only vertical inheritance in the evolution of homologous genes, which may result in errors in the estimated phylogenies. ...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evaa058

    authors: Coimbra NDR,Goes-Neto A,Azevedo V,Ouangraoua A

    更新日期:2020-04-01 00:00:00

  • Genome-Level Analysis of Selective Constraint without Apparent Sequence Conservation.

    abstract::Conservation of function can be accompanied by obvious similarity of homologous sequences which may persist for billions of years (Iyer LM, Leipe DD, Koonin EV, Aravind L. 2004. Evolutionary history and higher order classification of AAA+ ATPases. J Struct Biol. 146:11-31.). However, presumably homologous segments of ...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evt023

    authors: Vakhrusheva OA,Bazykin GA,Kondrashov AS

    更新日期:2013-01-01 00:00:00

  • Emergence and Spread of Epidemic Multidrug-Resistant Pseudomonas aeruginosa.

    abstract::Pseudomonas aeruginosa (P. aeruginosa) is one of the most common nosocomial pathogens worldwide. Although the emergence of multidrug-resistant (MDR) P. aeruginosa is a critical problem in medical practice, the key features involved in the emergence and spread of MDR P. aeruginosa remain unknown. This study utilized wh...

    journal_title:Genome biology and evolution

    pub_type: 杂志文章

    doi:10.1093/gbe/evx243

    authors: Miyoshi-Akiyama T,Tada T,Ohmagari N,Viet Hung N,Tharavichitkul P,Pokhrel BM,Gniadkowski M,Shimojima M,Kirikae T

    更新日期:2017-12-01 00:00:00