Serotonin Receptor 1A Variation Is Associated with Anxiety and Agonistic Behavior in Chimpanzees.

Abstract:

:Serotonin is a neurotransmitter that plays an important role in regulating behavior and personality in humans and other mammals. Polymorphisms in genes coding for the serotonin receptor subtype 1A (HTR1A), the serotonin transporter (SLC6A4), and the serotonin degrading enzyme monoamine oxidase A (MAOA) are associated with anxiety, impulsivity, and neurotic personality in humans. In primates, previous research has largely focused on SLC6A4 and MAOA, with few studies investigating the role of HTR1A polymorphic variation on behavior. Here, we examined variation in the coding region of HTR1A across apes, and genotyped polymorphic coding variation in a sample of 214 chimpanzees with matched measures of personality and behavior. We found evidence for positive selection at three amino acid substitution sites, one in chimpanzees-bonobos (Thr26Ser), one in humans (Phe33Val), and one in orangutans (Ala274Gly). Investigation of the HTR1A coding region in chimpanzees revealed a polymorphic site, where a C/A single nucleotide polymorphism changes a proline to a glutamine in the amino acid sequence (Pro248Gln). The substitution is located in the third intracellular loop of the receptor, a region important for serotonin signal transduction. The derived variant is the major allele in this population (frequency 0.67), and is associated with a reduction in anxiety, decreased rates of male agonistic behavior, and an increase in socio-positive behavior. These results are the first evidence that the HTR1A gene may be involved in regulating social behavior in chimpanzees and encourage further systematic investigation of polymorphic variation in other primate populations with corresponding data on behavior.

journal_name

Mol Biol Evol

authors

Staes N,Sherwood CC,Freeman H,Brosnan SF,Schapiro SJ,Hopkins WD,Bradley BJ

doi

10.1093/molbev/msz061

subject

Has Abstract

pub_date

2019-07-01 00:00:00

pages

1418-1429

issue

7

eissn

0737-4038

issn

1537-1719

pii

5380437

journal_volume

36

pub_type

杂志文章
  • Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution.

    abstract::The selective pressure at the protein level is usually measured by the nonsynonymous/synonymous rate ratio (omega = dN/dS), with omega < 1, omega = 1, and omega > 1 indicating purifying (or negative) selection, neutral evolution, and diversifying (or positive) selection, respectively. The omega ratio is commonly calcu...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a003945

    authors: Anisimova M,Bielawski JP,Yang Z

    更新日期:2001-08-01 00:00:00

  • Sequencing errors and molecular evolutionary analysis.

    abstract::Heuristic approaches were used to quantify the influence that sequencing errors have on estimates of nucleotide diversity, substitution rate, and the construction of genealogies. Error rates of less than 1 nucleotide/kb probably have little affect on conclusions about the evolutionary history of highly polymorphic org...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a040756

    authors: Clark AG,Whittam TS

    更新日期:1992-07-01 00:00:00

  • Molecular phylogeny of the springhare, Pedetes capensis, based on mitochondrial DNA sequences.

    abstract::The phylogenetic position of the Pedetidae, represented by a single species Pedetes capensis, is controversial, reflecting in part the retention of both Hystricomorphous and Sciurognathous characteristics in this rodent. In an attempt to clarify the species evolutionary relationships, mtDNA gene sequences from 10 rode...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a025698

    authors: Matthee CA,Robinson TJ

    更新日期:1997-01-01 00:00:00

  • Low nucleotide diversity for the expanded organelle and nuclear genomes of Volvox carteri supports the mutational-hazard hypothesis.

    abstract::The noncoding-DNA content of organelle and nuclear genomes can vary immensely. Both adaptive and nonadaptive explanations for this variation have been proposed. This study addresses a nonadaptive explanation called the mutational-hazard hypothesis and applies it to the mitochondrial, plastid, and nuclear genomes of th...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msq110

    authors: Smith DR,Lee RW

    更新日期:2010-10-01 00:00:00

  • Transcriptional diversification and functional conservation between DELLA proteins in Arabidopsis.

    abstract::Plasticity and robustness of signaling pathways partly rely on genetic redundancy, although the precise mechanism that provides functional specificity to the different redundant elements in a given process is often unknown. In Arabidopsis, functional redundancy in gibberellin signaling has been largely attributed to t...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msq012

    authors: Gallego-Bartolomé J,Minguet EG,Marín JA,Prat S,Blázquez MA,Alabadí D

    更新日期:2010-06-01 00:00:00

  • Parallel evolution of opsin gene expression in African cichlid fishes.

    abstract::Phenotypic evolution may occur either through alterations to the structure of protein-coding genes or their expression. Evidence for which of these two mechanisms more commonly contribute to the evolution of a phenotype can be garnered from examples of parallel and convergent evolution. The visual system of East Afric...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msq171

    authors: O'Quin KE,Hofmann CM,Hofmann HA,Carleton KL

    更新日期:2010-12-01 00:00:00

  • Genomic Analyses Reveal Potential Independent Adaptation to High Altitude in Tibetan Chickens.

    abstract::Much like other indigenous domesticated animals, Tibetan chickens living at high altitudes (2,200-4,100 m) show specific physiological adaptations to the extreme environmental conditions of the Tibetan Plateau, but the genetic bases of these adaptations are not well characterized. Here, we assembled a de novo genome o...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msv071

    authors: Wang MS,Li Y,Peng MS,Zhong L,Wang ZJ,Li QY,Tu XL,Dong Y,Zhu CL,Wang L,Yang MM,Wu SF,Miao YW,Liu JP,Irwin DM,Wang W,Wu DD,Zhang YP

    更新日期:2015-07-01 00:00:00

  • A Working Model of the Deep Relationships of Diverse Modern Human Genetic Lineages Outside of Africa.

    abstract::A major topic of interest in human prehistory is how the large-scale genetic structure of modern populations outside of Africa was established. Demographic models have been developed that capture the relationships among small numbers of populations or within particular geographical regions, but constructing a phylogen...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msw293

    authors: Lipson M,Reich D

    更新日期:2017-04-01 00:00:00

  • Evolutionary Modeling in SLiM 3 for Beginners.

    abstract::The SLiM forward genetic simulation framework has proved to be a powerful and flexible tool for population genetic modeling. However, as a complex piece of software with many features that allow simulating a diverse assortment of evolutionary models, its initial learning curve can be difficult. Here we provide a step-...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msy237

    authors: Haller BC,Messer PW

    更新日期:2019-05-01 00:00:00

  • Protein structure, neighbor effect, and a new index of amino acid dissimilarities.

    abstract::Amino acids interact with each other, especially with neighboring amino acids, to generate protein structures. We studied the pattern of association and repulsion of amino acids based on 24,748 protein-coding genes from human, 11,321 from mouse, and 15,028 from Escherichia coli, and documented the pattern of neighbor ...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a003982

    authors: Xia X,Xie Z

    更新日期:2002-01-01 00:00:00

  • Adjusting for selection on synonymous sites in estimates of evolutionary distance.

    abstract::Evolution at silent sites is often used to estimate the pace of selectively neutral processes or to infer differences in divergence times of genes. However, silent sites are subject to selection in favor of preferred codons, and the strength of such selection varies dramatically across genes. Here, we use the relation...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msh265

    authors: Hirsh AE,Fraser HB,Wall DP

    更新日期:2005-01-01 00:00:00

  • Structural Patching Fosters Divergence of Mitochondrial Ribosomes.

    abstract::Mitochondrial ribosomes (mitoribosomes) are essential components of all mitochondria that synthesize proteins encoded by the mitochondrial genome. Unlike other ribosomes, mitoribosomes are highly variable across species. The basis for this diversity is not known. Here, we examine the composition and evolutionary histo...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msy221

    authors: Petrov AS,Wood EC,Bernier CR,Norris AM,Brown A,Amunts A

    更新日期:2019-02-01 00:00:00

  • The variability of the hepatitis B virus genome: statistical analysis and biological implications.

    abstract::A statistical analysis of the nucleotide sequence variability in 14 published hepatitis B virus (HBV) genomes was carried out using parametric and nonparametric methods. A parametric statistical model revealed that the different regions of the genome differed significantly in their variability. The conclusion was supp...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a040013

    authors: Lauder IJ,Lin HJ,Lau JY,Siu TS,Lai CL

    更新日期:1993-03-01 00:00:00

  • Combining multiple data sets in a likelihood analysis: which models are the best?

    abstract::Until recently, phylogenetic analyses have been routinely based on homologous sequences of a single gene. Given the vast number of gene sequences now available, phylogenetic studies are now based on the analysis of multiple genes. Thus, it has become necessary to devise statistical methods to combine multiple molecula...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a004053

    authors: Pupko T,Huchon D,Cao Y,Okada N,Hasegawa M

    更新日期:2002-12-01 00:00:00

  • Chromosome size in diploid eukaryotic species centers on the average length with a conserved boundary.

    abstract::Understanding genome and chromosome evolution is important for understanding genetic inheritance and evolution. Universal events comprising DNA replication, transcription, repair, mobile genetic element transposition, chromosome rearrangements, mitosis, and meiosis underlie inheritance and variation of living organism...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msr011

    authors: Li X,Zhu C,Lin Z,Wu Y,Zhang D,Bai G,Song W,Ma J,Muehlbauer GJ,Scanlon MJ,Zhang M,Yu J

    更新日期:2011-06-01 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

  • Comparison of regulatory and structural regions of genes of tryptophan metabolism.

    abstract::The genes of tryptophan biosynthesis are arranged and regulated differently in many microorganisms. Comparison of the transcription regulatory regions of the trp operons of several species of enterobacteria reveals that those sequences and structures believed to be essential for repression and attenuation control are ...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a040307

    authors: Yanofsky C

    更新日期:1984-02-01 00:00:00

  • Divergence time of porcine reproductive and respiratory syndrome virus subtypes.

    abstract::Porcine reproductive and respiratory syndrome virus (PRRSV) recently emerged in domestic pigs of Western Europe and North America. Although time of emergence was identical on the two continents, genetic composition was markedly different with a clear geographical subtype structure, indicating that subtypes diverged in...

    journal_title:Molecular biology and evolution

    pub_type: 评论,信件

    doi:10.1093/molbev/msi208

    authors: Forsberg R

    更新日期:2005-11-01 00:00:00

  • Overdispersion of the molecular clock: temporal variation of gene-specific substitution rates in Drosophila.

    abstract::Simple models of molecular evolution assume that sequences evolve by a Poisson process in which nucleotide or amino acid substitutions occur as rare independent events. In these models, the expected ratio of the variance to the mean of substitution counts equals 1, and substitution processes with a ratio greater than ...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msn112

    authors: Bedford T,Hartl DL

    更新日期:2008-08-01 00:00:00

  • The increase in the number of subunits in eukaryotic RNA polymerase III relative to RNA polymerase II is due to the permanent recruitment of general transcription factors.

    abstract::The number of subunits of RNA polymerases (RNAPs) increases during evolution from 5 in eubacteria to 12 in archaea. In eukaryotes, which have at least three RNAPs, the number of subunits has expanded from 12 in RNA polymerase II (RNAPII) to 14 in RNA polymerase I (RNAPI) and to 17 in RNA polymerase III (RNAPIII). It w...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msp316

    authors: Carter R,Drouin G

    更新日期:2010-05-01 00:00:00

  • Evolution of Hox post-transcriptional regulation by alternative polyadenylation and microRNA modulation within 12 Drosophila genomes.

    abstract::Hox genes encode a family of transcriptional regulators that operate differential developmental programs along the anteroposterior axis of bilateral animals. Regulatory changes affecting Hox gene expression are believed to have been crucial for the evolution of animal body plans. In Drosophila melanogaster, Hox expres...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msr073

    authors: Patraquim P,Warnefors M,Alonso CR

    更新日期:2011-09-01 00:00:00

  • mtDNA tandem repeats in domestic dogs and wolves: mutation mechanism studied by analysis of the sequence of imperfect repeats.

    abstract::The mitochondrial (mt) DNA control region (CR) of dogs and wolves contains an array of imperfect 10 bp tandem repeats. This region was studied for 14 domestic dogs representing the four major phylogenetic groups of nonrepetitive CR and for 5 wolves. Three repeat types were found among these individuals, distributed so...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a026328

    authors: Savolainen P,Arvestad L,Lundeberg J

    更新日期:2000-04-01 00:00:00

  • Gene turnover in the avian globin gene families and evolutionary changes in hemoglobin isoform expression.

    abstract::The apparent stasis in the evolution of avian chromosomes suggests that birds may have experienced relatively low rates of gene gain and loss in multigene families. To investigate this possibility and to explore the phenotypic consequences of variation in gene copy number, we examined evolutionary changes in the famil...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msu341

    authors: Opazo JC,Hoffmann FG,Natarajan C,Witt CC,Berenbrink M,Storz JF

    更新日期:2015-04-01 00:00:00

  • Evolution and phylogenetic utility of alignment gaps within intron sequences of three nuclear genes in bumble bees (Bombus).

    abstract::To test whether gaps resulting from sequence alignment contain phylogenetic signal concordant with those of base substitutions, we analyzed the occurrence of indel mutations upon a well-resolved, substitution-based tree for three nuclear genes in bumble bees (Bombus, Apidae: Bombini). The regions analyzed were exon an...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msg007

    authors: Kawakita A,Sota T,Ascher JS,Ito M,Tanaka H,Kato M

    更新日期:2003-01-01 00:00:00

  • Divergent evolution and evolution by the birth-and-death process in the immunoglobulin VH gene family.

    abstract::Immunoglobulin diversity is generated primarily by the heavy- and light-chain variable-region gene families. To understand the pattern of long-term evolution of the heavy-chain variable-region (VH) gene family, which is composed of a large number of member genes, the evolutionary relationships of representative VH gen...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a040127

    authors: Ota T,Nei M

    更新日期:1994-05-01 00:00:00

  • Conditional gene genealogies under strong purifying selection.

    abstract::The ancestral selection graph, conditioned on the allelic types in the sample, is used to obtain a limiting gene genealogical process under strong selection. In an equilibrium, two-allele system with strong selection, neutral gene genealogies are predicted for random samples and for samples containing at most one unfa...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msn209

    authors: Wakeley J

    更新日期:2008-12-01 00:00:00

  • Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae).

    abstract::Polymerase chain reaction (PCR) products corresponding to 803 bp of the cytochrome oxidase subunits I and II region of mitochondrial DNA (mtDNA COI-II) were deduced to consist of multiple haplotypes in three Sitobion species. We investigated the molecular basis of these observations. PCR products were cloned, and six ...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a025612

    authors: Sunnucks P,Hales DF

    更新日期:1996-03-01 00:00:00

  • A codon-based model of host-specific selection in parasites, with an application to the influenza A virus.

    abstract::Parasites sometimes expand their host range by acquiring a new host species. After a host change event, the selective regime acting on a given parasite gene may change as a result of host-specific adaptive alterations of protein functionality or host-specific immune-mediated selection. We present a codon-based model t...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/molbev/msg149

    authors: Forsberg R,Christiansen FB

    更新日期:2003-08-01 00:00:00

  • A graphical method for detecting recombination in phylogenetic data sets.

    abstract::Current phylogenetic tree reconstruction methods assume that there is a single underlying tree topology for all sites along the sequence. The presence of mosaic sequences due to recombination violates this assumption and will cause phylogenetic methods to give misleading results due to the imposition of a single tree ...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a025722

    authors: McGuire G,Wright F,Prentice MJ

    更新日期:1997-11-01 00:00:00

  • Evolution at the tip and base of the X chromosome in an African population of Drosophila melanogaster.

    abstract::Hitchhiking effects of advantageous mutations have been invoked to explain reduced polymorphism in regions of low crossing-over in Drosophila. Besides reducing DNA heterozygosity, hitchhiking effects should produce strong linkage disequilibrium and a frequency spectrum skewed toward an excess of rare polymorphisms (co...

    journal_title:Molecular biology and evolution

    pub_type: 杂志文章

    doi:10.1093/oxfordjournals.molbev.a040213

    authors: Begun DJ,Aquadro CF

    更新日期:1995-05-01 00:00:00