Large-scale coding sequence change underlies the evolution of postdevelopmental novelty in honey bees.

Abstract:

:Whether coding or regulatory sequence change is more important to the evolution of phenotypic novelty is one of biology's major unresolved questions. The field of evo-devo has shown that in early development changes to regulatory regions are the dominant mode of genetic change, but whether this extends to the evolution of novel phenotypes in the adult organism is unclear. Here, we conduct ten RNA-Seq experiments across both novel and conserved tissues in the honey bee to determine to what extent postdevelopmental novelty is based on changes to the coding regions of genes. We make several discoveries. First, we show that with respect to novel physiological functions in the adult animal, positively selected tissue-specific genes of high expression underlie novelty by conferring specialized cellular functions. Such genes are often, but not always taxonomically restricted genes (TRGs). We further show that positively selected genes, whether TRGs or conserved genes, are the least connected genes within gene expression networks. Overall, this work suggests that the evo-devo paradigm is limited, and that the evolution of novelty, postdevelopment, follows additional rules. Specifically, evo-devo stresses that high network connectedness (repeated use of the same gene in many contexts) constrains coding sequence change as it would lead to negative pleiotropic effects. Here, we show that in the adult animal, the converse is true: Genes with low network connectedness (TRGs and tissue-specific conserved genes) underlie novel phenotypes by rapidly changing coding sequence to perform new-specialized functions.

journal_name

Mol Biol Evol

authors

Jasper WC,Linksvayer TA,Atallah J,Friedman D,Chiu JC,Johnson BR

doi

10.1093/molbev/msu292

subject

Has Abstract

pub_date

2015-02-01 00:00:00

pages

334-46

issue

2

eissn

0737-4038

issn

1537-1719

pii

msu292

journal_volume

32

pub_type

杂志文章
  • Phylogenetic analysis of the alpha-globin pseudogene-4 (Hba-ps4) locus in the house mouse species complex reveals a stepwise evolution of t haplotypes.

    abstract::A parsimony analysis was performed on restriction sites at the Hba-ps4 pseudogene locus within one of four inversions associated with mouse t haplotypes. The results suggest that all t haplotypes form a monophyletic group and that the in (17)4 inversion originated before the radiation of the Mus musculus species compl...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a040051

    authors: Hammer MF,Silver LM

    更新日期:1993-09-01 00:00:00

  • Evolution of the TIR domain-containing adaptors in humans: swinging between constraint and adaptation.

    abstract::Natural selection is expected to act strongly on immune system genes as hosts adapt to novel, diverse, and coevolving pathogens. Population genetic studies of host defense genes with parallel functions in model organisms have revealed distinct evolutionary histories among the different components-receptors, adaptors, ...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msr137

    authors: Fornarino S,Laval G,Barreiro LB,Manry J,Vasseur E,Quintana-Murci L

    更新日期:2011-11-01 00:00:00

  • Phylogenomic analysis of the uracil-DNA glycosylase superfamily.

    abstract::The spontaneous deamination of cytosine produces uracil mispaired with guanine in DNA, which will produce a mutation, unless repaired. In all domains of life, uracil-DNA glycosylases (UDGs) are responsible for the elimination of uracil from DNA. Thus, UDGs contribute to the integrity of the genetic information and the...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msq318

    authors: Lucas-Lledó JI,Maddamsetti R,Lynch M

    更新日期:2011-03-01 00:00:00

  • Conservation of alternative splicing and genomic organization of the myosin alkali light-chain (Mlc1) gene among Drosophila species.

    abstract::The Mlc1 gene of Drosophila melanogaster encodes two MLC1 isoforms via developmentally regulated alternative pre-mRNA splicing. In larval muscle and tubular and abdominal muscles of adults, all of the six exons are included in the spliced mRNA, whereas, in the fibrillar indirect flight muscle of adult, exon 5 is exclu...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a040043

    authors: Leicht BG,Lyckegaard EM,Benedict CM,Clark AG

    更新日期:1993-07-01 00:00:00

  • The relative contributions of recombination and mutation to the divergence of clones of Neisseria meningitidis.

    abstract::Multilocus sequence typing (MLST) is a recently developed nucleotide sequence-based method for the definitive assignment of isolates within bacterial populations to specific clones. MLST uses the same principles as multilocus enzyme electrophoresis and provides data that can be used to investigate aspects of the popul...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a026061

    authors: Feil EJ,Maiden MC,Achtman M,Spratt BG

    更新日期:1999-11-01 00:00:00

  • Positively selected disease response orthologous gene sets in the cereals identified using Sorghum bicolor L. Moench expression profiles and comparative genomics.

    abstract::Disease response genes (DRGs) diverge under recurrent positive selection as a result of a molecular arms race between hosts and pathogens. Most of these studies were conducted in animals, and few defense genes have been shown to evolve adaptively in plants. To test for adaptation in the molecules mediating disease res...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msp114

    authors: Zamora A,Sun Q,Hamblin MT,Aquadro CF,Kresovich S

    更新日期:2009-09-01 00:00:00

  • Emergent complexity in Myosin V-based organelle inheritance.

    abstract::How is adaptability generated in a system composed of interacting cellular machineries, each with a separate and functionally critical job to perform? The machinery for organelle inheritance is precisely one such system, requiring coordination between robust and ancient cellular modules, including the cell cycle, cyto...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msr264

    authors: Mast FD,Rachubinski RA,Dacks JB

    更新日期:2012-03-01 00:00:00

  • IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era.

    abstract::IQ-TREE (http://www.iqtree.org, last accessed February 6, 2020) is a user-friendly and widely used software package for phylogenetic inference using maximum likelihood. Since the release of version 1 in 2014, we have continuously expanded IQ-TREE to integrate a plethora of new models of sequence evolution and efficien...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msaa015

    authors: Minh BQ,Schmidt HA,Chernomor O,Schrempf D,Woodhams MD,von Haeseler A,Lanfear R

    更新日期:2020-05-01 00:00:00

  • Discovery and expression analysis of alternative splicing events conserved among plant SR proteins.

    abstract::The high frequency of alternative splicing among the serine/arginine-rich (SR) family of proteins in plants has been linked to important roles in gene regulation during development and in response to environmental stress. In this article, we have searched and manually annotated all the SR proteins in the genomes of ma...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/mst238

    authors: Rauch HB,Patrick TL,Klusman KM,Battistuzzi FU,Mei W,Brendel VP,Lal SK

    更新日期:2014-03-01 00:00:00

  • Phylogenetic relationships and evolution of the KNOTTED class of plant homeodomain proteins.

    abstract::Knotted-like (KNOX) proteins constitute a group of homeodomain proteins involved in pattern formation in developing tissues of angiosperms and other green plants. We conducted phylogenetic analyses of nucleotide and amino acid sequences of all known KNOX proteins in order to examine their evolution. Our analyses revea...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a026136

    authors: Bharathan G,Janssen BJ,Kellogg EA,Sinha N

    更新日期:1999-04-01 00:00:00

  • Chromosome-specific distribution of nucleotide substitutions in telomeric repeats of rice (Oryza sativa L.).

    abstract::Examination of the genomic sequence of the telomere region makes it possible to understand the evolution of the structure of chromosomal ends. We compared the genomic sequences of 14 chromosomal ends of rice, Oryza sativa, L., on the basis of the variation in TTTAGGG repeats. In the proximal telomere repeats, nucleoti...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msm227

    authors: Mizuno H,Wu J,Katayose Y,Kanamori H,Sasaki T,Matsumoto T

    更新日期:2008-01-01 00:00:00

  • Evolution of paralogous genes: Reconstruction of genome rearrangements through comparison of multiple genomes within Staphylococcus aureus.

    abstract::Analysis of evolution of paralogous genes in a genome is central to our understanding of genome evolution. Comparison of closely related bacterial genomes, which has provided clues as to how genome sequences evolve under natural conditions, would help in such an analysis. With species Staphylococcus aureus, whole-geno...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msk013

    authors: Tsuru T,Kawai M,Mizutani-Ui Y,Uchiyama I,Kobayashi I

    更新日期:2006-06-01 00:00:00

  • The robustness of two phylogenetic methods: four-taxon simulations reveal a slight superiority of maximum likelihood over neighbor joining.

    abstract::The robustness (sensitivity to violation of assumptions) of the maximum-likelihood and neighbor-joining methods was examined using simulation. Maximum likelihood and neighbor joining were implemented with Jukes-Cantor, Kimura, and gamma models of DNA substitution. Simulations were performed in which the assumptions of...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a040261

    authors: Huelsenbeck JP

    更新日期:1995-09-01 00:00:00

  • DNA sequence variation in the mitochondrial control region of red-backed voles (Clethrionomys).

    abstract::The complete mitochondrial DNA (mtDNA) control region was sequenced for 71 individuals from five species of the rodent genus Clethrionomys both to understand patterns of variation and to explore the existence of previously described domains and other elements. Among species, the control region ranged from 942 to 971 b...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a003935

    authors: Matson CW,Baker RJ

    更新日期:2001-08-01 00:00:00

  • Evolution of DNA base composition under no-strand-bias conditions when the substitution rates are not constant.

    abstract::The evolution of DNA base composition evolution is simplified to a six-parameter model when there are no strand biases for mutation and selection. We analyzed the dynamics of this model with special attention to the influence of a change in substitution rates. The G + C content of the DNA sequence tends to an equilibr...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a026156

    authors: Lobry JR,Lobry C

    更新日期:1999-06-01 00:00:00

  • Directional evolution for microsatellite size in maize.

    abstract::Directional evolution in microsatellites is the tendency for microsatellites either to increase or to decrease in size over time between populations. We analyzed 99 microsatellite loci in a sample of 193 maize plants representing the entire pre-Columbian range of this crop for evidence of directional evolution. We too...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msg156

    authors: Vigouroux Y,Matsuoka Y,Doebley J

    更新日期:2003-09-01 00:00:00

  • Relative Evolutionary Rates in Proteins Are Largely Insensitive to the Substitution Model.

    abstract::The relative evolutionary rates at individual sites in proteins are informative measures of conservation or adaptation. Often used as evolutionarily aware conservation scores, relative rates reveal key functional or strongly selected residues. Estimating rates in a phylogenetic context requires specifying a protein su...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msy127

    authors: Spielman SJ,Kosakovsky Pond SL

    更新日期:2018-09-01 00:00:00

  • Bayesian Inference of Species Networks from Multilocus Sequence Data.

    abstract::Reticulate species evolution, such as hybridization or introgression, is relatively common in nature. In the presence of reticulation, species relationships can be captured by a rooted phylogenetic network, and orthologous gene evolution can be modeled as bifurcating gene trees embedded in the species network. We pres...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msx307

    authors: Zhang C,Ogilvie HA,Drummond AJ,Stadler T

    更新日期:2018-02-01 00:00:00

  • Lokiarchaeota Marks the Transition between the Archaeal and Eukaryotic Selenocysteine Encoding Systems.

    abstract::Selenocysteine (Sec) is the 21st amino acid in the genetic code, inserted in response to UGA codons with the help of RNA structures, the SEC Insertion Sequence (SECIS) elements. The three domains of life feature distinct strategies for Sec insertion in proteins and its utilization. While bacteria and archaea possess s...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msw122

    authors: Mariotti M,Lobanov AV,Manta B,Santesmasses D,Bofill A,Guigó R,Gabaldón T,Gladyshev VN

    更新日期:2016-09-01 00:00:00

  • Mitochondrial genome of the colorless green alga Polytomella parva: two linear DNA molecules with homologous inverted repeat Termini.

    abstract::Most of the well-characterized mitochondrial genomes from diverse green algal lineages are circular mapping DNA molecules; however, Chlamydomonas reinhardtii has a linear 15.8 kb unit mitochondrial genome with 580 or 581 bp inverted repeat ends. In mitochondrial-enriched fractions prepared from Polytomella parva (=P. ...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a004180

    authors: Fan J,Lee RW

    更新日期:2002-07-01 00:00:00

  • Evolution of programmed DNA rearrangements in a scrambled gene.

    abstract::Gene unscrambling in spirotrichous ciliates involves massive genome-wide DNA deletion and rearrangement events during development. During each sexual cycle, the somatic nucleus (macronucleus) regenerates from the germ line nucleus (micronucleus). Development of the polyploid somatic genome requires programmed DNA dele...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msj089

    authors: Wong LC,Landweber LF

    更新日期:2006-04-01 00:00:00

  • Adaptive Radiation of the Flukes of the Family Fasciolidae Inferred from Genome-Wide Comparisons of Key Species.

    abstract::Liver and intestinal flukes of the family Fasciolidae cause zoonotic food-borne infections that impact both agriculture and human health throughout the world. Their evolutionary history and the genetic basis underlying their phenotypic and ecological diversity are not well understood. To close that knowledge gap, we c...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msz204

    authors: Choi YJ,Fontenla S,Fischer PU,Le TH,Costábile A,Blair D,Brindley PJ,Tort JF,Cabada MM,Mitreva M

    更新日期:2020-01-01 00:00:00

  • Evolutionary origin and diversification of epidermal barrier proteins in amniotes.

    abstract::The evolution of amniotes has involved major molecular innovations in the epidermis. In particular, distinct structural proteins that undergo covalent cross-linking during cornification of keratinocytes facilitate the formation of mechanically resilient superficial cell layers and help to limit water loss to the envir...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msu251

    authors: Strasser B,Mlitz V,Hermann M,Rice RH,Eigenheer RA,Alibardi L,Tschachler E,Eckhart L

    更新日期:2014-12-01 00:00:00

  • Three divergent rDNA clusters predate the species divergence in Quercus petraea (Matt.) Liebl. and Quercus robur L.

    abstract::Quercus petraea and Quercus robur are two closely related oak species that frequently hybridize. We sequenced 70 clones containing the 5.8S and ITS2 regions of ribosomal DNA (rDNA) from these two species and did not detect a species-specific difference. Surprisingly, three divergent (up to 12.6%) rDNA families were id...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a003785

    authors: Muir G,Fleming CC,Schlötterer C

    更新日期:2001-02-01 00:00:00

  • Ancestral sequence reconstruction in primate mitochondrial DNA: compositional bias and effect on functional inference.

    abstract::Reconstruction of ancestral DNA and amino acid sequences is an important means of inferring information about past evolutionary events. Such reconstructions suggest changes in molecular function and evolutionary processes over the course of evolution and are used to infer adaptation and convergence. Maximum likelihood...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msh198

    authors: Krishnan NM,Seligmann H,Stewart CB,De Koning AP,Pollock DD

    更新日期:2004-10-01 00:00:00

  • IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies.

    abstract::Large phylogenomics data sets require fast tree inference methods, especially for maximum-likelihood (ML) phylogenies. Fast programs exist, but due to inherent heuristics to find optimal trees, it is not clear whether the best tree is found. Thus, there is need for additional approaches that employ different search st...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msu300

    authors: Nguyen LT,Schmidt HA,von Haeseler A,Minh BQ

    更新日期:2015-01-01 00:00:00

  • Distribution of chromosome length variation in natural isolates of Escherichia coli.

    abstract::Large-scale variation in chromosome size was analyzed in 35 natural isolates of Escherichia coli by physical mapping with a restriction enzyme whose sites are restricted to rDNA operons. Although the genetic maps and chromosome lengths of the laboratory strains E. coli K12 and Salmonella enterica sv. Typhimurium LT2 a...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a025847

    authors: Bergthorsson U,Ochman H

    更新日期:1998-01-01 00:00:00

  • Horizontal transfer and selection in the evolution of P elements.

    abstract::The roles of selection and horizontal transfer in the evolution of the canonical subfamily of P: elements were studied in the saltans and willistoni species groups of the genus Drosophila (subgenus Sophophora). We estimate that the common ancestor of the canonical P: subfamily dates back 2-3 Myr at the most, despite t...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a026253

    authors: Silva JC,Kidwell MG

    更新日期:2000-10-01 00:00:00

  • Population structure in the American oyster as inferred by nuclear gene genealogies.

    abstract::Multiple haplotypes from each of three nuclear loci were isolated and sequenced from geographic populations of the American oyster, Crassostrea virginica. In tests of alternative phylogeographic hypotheses for this species, nuclear gene genealogies constructed for these haplotypes were compared to one another, to a mi...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a025908

    authors: Hare MP,Avise JC

    更新日期:1998-02-01 00:00:00

  • Functional conservation of the fruitless male sex-determination gene across 250 Myr of insect evolution.

    abstract::Male sexual behavior in the fruit fly Drosophila melanogaster is regulated by fruitless (fru), a sex-determination gene specifying the synthesis of BTB-Zn finger proteins that likely function as male-specific transcriptional regulators. Expression of fru in the nervous system specifies male sexual behavior and the mus...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msj070

    authors: Gailey DA,Billeter JC,Liu JH,Bauzon F,Allendorfer JB,Goodwin SF

    更新日期:2006-03-01 00:00:00