skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Homoplasy in genome-wide analysis of rare amino acid replacements: the molecular-evolutionary basis for Vavilov's law of homologous series

Journal Article · · Biology Direct
 [1];  [2];  [3];  [4];  [1]
  1. National Institutes of Health (NIH), Bethesda, MD (United States)
  2. University of New Orleans, New Orleans, LA (United States)
  3. University of Montreal, QC (Canada)
  4. National Institutes of Health (NIH), Bethesda, MD (United States)n

Rare genomic changes (RGCs) that are thought to comprise derived shared characters of individual clades are becoming an increasingly important class of markers in genome-wide phylogenetic studies. Recently, we proposed a new type of RGCs designated RGC_CAMs (after Conserved Amino acids-Multiple substitutions) that were inferred using genome-wide identification of amino acid replacements that were: i) located in unambiguously aligned regions of orthologous genes, ii) shared by two or more taxa in positions that contain a different, conserved amino acid in a much broader range of taxa, and iii) require two or three nucleotide substitutions. When applied to animal phylogeny, the RGC_CAM approach supported the coelomate clade that unites deuterostomes with arthropods as opposed to the ecdysozoan (molting animals) clade. However, a nonnegligible level of homoplasy was detected. We provide a direct estimate of the level of homoplasy caused by parallel changes and reversals among the RGC_CAMs using 462 alignments of orthologous genes from 19 eukaryotic species. It is shown that the impact of parallel changes and reversals on the results of phylogenetic inference using RGC_CAMs cannot explain the observed support for the Coelomata clade. In contrast, the evidence in support of the Ecdysozoa clade, in large part, can be attributed to parallel changes. It is demonstrated that parallel changes are significantly more common in internal branches of different subtrees that are separated from the respective common ancestor by relatively short times than in terminal branches separated by longer time intervals. A similar but much weaker trend was detected for reversals. The observed evolutionary trend of parallel changes is explained in terms of the covarion model of molecular evolution. As the overlap between the covarion sets in orthologous genes from different lineages decreases with time after divergence, the likelihood of parallel changes decreases as well. The level of homoplasy observed here appears to be low enough to justify the utility of RGC_CAMs and other types of RGCs for resolution of hard problems in phylogeny. Parallel changes, one of the major classes of events leading to homoplasy, occur much more often in relatively recently diverged lineages than in those separated from their last common ancestor by longer time intervals of time. This pattern seems to provide the molecular-evolutionary underpinning of Vavilov's law of homologous series and is readily interpreted within the framework of the covarion model of molecular evolution.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); National Institutes of Health (NIH), Bethesda, MD (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Institutes of Health (NIH); National Sciences and Engineering Research Council (NSERC)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1626627
Journal Information:
Biology Direct, Vol. 3, Issue 1; ISSN 1745-6150
Publisher:
BioMed CentralCopyright Statement
Country of Publication:
United States
Language:
English

References (62)

Evidence for a clade of nematodes, arthropods and other moulting animals journal May 1997
Phylogenomics and the reconstruction of the tree of life journal May 2005
Large-Scale Taxonomic Profiling of Eukaryotic Model Organisms: A Comparison of Orthologous Proteins Encoded by the Human, Fly, Nematode, and Yeast Genomes journal June 1998
Combinatorial RNA interference in Caenorhabditis elegans reveals that redundancy between gene duplicates can be maintained for more than 80 million years of evolution journal January 2006
Systematic searches for molecular synapomorphies in model metazoan genomes give some support for Ecdysozoa after accounting for the idiosyncrasies of Caenorhabditis elegans journal May 2004
Relaxed Phylogenetics and Dating with Confidence journal March 2006
The root of the eukaryote tree pinpointed journal September 2003
Phylogenetic relationships among cetartiodactyls based on insertions of short and long interpersed elements: Hippopotamuses are the closest extant relatives of whales journal August 1999
Maximum-Likelihood Phylogenetic Analysis Under a Covarion-like Model journal May 2001
The use of genome-level characters for phylogenetic reconstruction journal August 2006
The colonization of land by animals: molecular phylogeny and divergence times among arthropods journal January 2004
Analysis of Rare Amino Acid Replacements Supports the Coelomata Clade journal June 2007
Late changes in spliceosomal introns define clades in vertebrate evolution journal August 1999
Genome Trees and the Nature of Genome Evolution journal October 2005
Comparative Genome Analysis of the Yellow Fever Mosquito Aedes aegypti with Drosophila melanogaster and the Malaria Vector Mosquito Anopheles gambiae journal March 2004
The evolutionary position of nematodes journal January 2002
Origin of the metazoan phyla: Molecular clocks confirm paleontological estimates journal January 1998
Rooting the Eukaryote Tree by Using a Derived Gene Fusion journal July 2002
The origin and evolution of model organisms journal November 2002
Testing a Covariotide Model of DNA Substitution journal May 2002
Coelomata and Not Ecdysozoa: Evidence From Genome-Wide Phylogenetic Analysis journal December 2003
The Opisthokonta and the Ecdysozoa May Not Be Clades: Stronger Support for the Grouping of Plant and Animal than for Animal and Fungi and Stronger Support for the Coelomata than Ecdysozoa journal February 2005
SINEs of speciation: tracking lineages with retroposons journal October 2004
Precision of molecular time estimates journal May 2004
Rare Coding Sequence Changes are Consistent with Ecdysozoa, not Coelomata journal April 2007
Genome trees and the tree of life journal September 2002
Ecdysozoan Clade Rejected by Genome-Wide Analysis of Rare Amino Acid Replacements journal January 2007
Genome-scale evidence of the nematode-arthropod clade journal January 2005
Detecting groups of co-evolving positions in a molecule: a clustering approach journal January 2007
Mathematical Elegance with Biochemical Realism: The Covarion Model of Molecular Evolution journal December 2001
Similarity of the Domain Structure of Proteins as a Basis for the Conservation of Meiosis book January 2007
Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision journal February 2004
Evidence for a High Frequency of Simultaneous Double-Nucleotide Substitutions journal February 2000
Are Vavilov's law of homologous series and synteny related? journal January 1994
Molecular dating: ape bones agree with chicken entrails journal February 2005
The nematode?arthropod clade revisited: phylogenomic analyses from ribosomal protein genes misled by shared evolutionary biases journal April 2007
Multigene Analyses of Bilaterian Animals Corroborate the Monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia journal February 2005
Evolution of bacterial RNA polymerase: implications for large-scale bacterial phylogeny, domain accretion, and horizontal gene transfer journal June 2004
The new animal phylogeny: Reliability and implications journal April 2000
Extensive parallelism in protein evolution journal August 2007
The COG database: an updated version includes eukaryotes journal January 2003
MUSCLE: multiple sequence alignment with high accuracy and high throughput journal March 2004
Topological Estimation Biases with Covarion Evolution journal December 2007
A Genomic Perspective on Protein Families journal October 1997
Testing for Covarion-like Evolution in Protein Sequences journal October 2006
Animal Phylogeny: Fatal Attraction journal April 2005
An SVD-based comparison of nine whole eukaryotic genomes supports a coelomate rather than ecdysozoan lineage journal January 2004
Heterotachy and long-branch attraction in phylogenetics journal October 2005
An improved method for determining codon variability in a gene and its application to the rate of fixation of mutations in evolution journal October 1970
The molecular evolution of cytochrome c in eukaryotes journal March 1976
Nikolai I Vavilov (1887–1943) journal June 2005
The law of homologous series in variation journal April 1922
Molecular Clock Calibrations and Metazoan Divergence Dates journal September 1999
Modeling the covarion hypothesis of nucleotide substitution journal January 1998
Patterns in spontaneous mutation revealed by human–baboon sequence comparison journal November 2002
Rare genomic changes as a tool for phylogenetics journal November 2000
Long-branch attraction phenomenon and the impact of among-site rate variation on rodent phylogeny journal December 2000
Liquid-liquid phase separation and extracellular multivalent interactions in the tale of galectin-3 journal March 2020
Comparative in-silico proteomic analysis discerns potential granuloma proteins of Yersinia pseudotuberculosis journal February 2020
SINEs of the perfect character journal August 1999
Systematic searches for molecular synapomorphies in model metazoan genomes give some support for Ecdysozoa after accounting for the idiosyncrasies of Caenorhabditis elegans journal May 2004
Two brilliant generalizations of Nikolai Ivanovich Vavilov (for the 120th anniversary) journal November 2007

Cited By (18)

Senescence and entrenchment in evolution of amino acid sites journal September 2020
Are Convergent and Parallel Amino Acid Substitutions in Protein Evolution More Prevalent Than Neutral Expectations? journal April 2015
A new deep-sea genus of the family Polyceridae (Nudibranchia) possesses a gill cavity, with implications for the cryptobranch condition and a ‘Periodic Table’ approach to taxonomy journal March 2015
Embracing heterogeneity: coalescing the Tree of Life and the future of phylogenomics journal January 2019
Senescence and entrenchment in evolution of amino acid sites posted_content January 2019
Epistasis and the dynamics of reversion in molecular evolution posted_content March 2016
A late origin of the extant eukaryotic diversity: divergence time estimates using rare genomic changes journal January 2011
Epistasis and the Dynamics of Reversion in Molecular Evolution journal July 2016
Causes of molecular convergence and parallelism in protein evolution journal March 2016
Mendelian-Mutationism: The Forgotten Evolutionary Synthesis journal May 2014
Analysis of Rare Genomic Changes Does Not Support the Unikont–Bikont Phylogeny and Suggests Cyanobacterial Symbiosis as the Point of Primary Radiation of Eukaryotes journal January 2009
Deep Genomic-Scale Analyses of the Metazoa Reject Coelomata: Evidence from Single- and Multigene Families Analyzed Under a Supertree and Supermatrix Paradigm journal January 2010
Parallel evolution of metazoan mitochondrial proteins posted_content March 2017
Gene tree discordance generates patterns of diminishing convergence over time journal June 2016
Homoplastic microinversions and the avian tree of life journal May 2011
Phylogenomics: Gene Duplication, Unrecognized Paralogy and Outgroup Choice journal February 2009
Evaluating Rare Amino Acid Substitutions (RGC_CAMs) in a Yeast Model Clade journal March 2014
Substitutions into amino acids that are pathogenic in human mitochondrial proteins are more frequent in lineages closely related to human than in distant lineages journal December 2017