The Natural History of Class I Primate Alcohol Dehydrogenases Includes Gene Duplication, Gene Loss, and Gene Conversion
Open Access
- 31 July 2012
- journal article
- research article
- Published by Public Library of Science (PLoS) in PLOS ONE
- Vol. 7 (7), e41175
- https://doi.org/10.1371/journal.pone.0041175
Abstract
Gene duplication is a source of molecular innovation throughout evolution. However, even with massive amounts of genome sequence data, correlating gene duplication with speciation and other events in natural history can be difficult. This is especially true in its most interesting cases, where rapid and multiple duplications are likely to reflect adaptation to rapidly changing environments and life styles. This may be so for Class I of alcohol dehydrogenases (ADH1s), where multiple duplications occurred in primate lineages in Old and New World monkeys (OWMs and NWMs) and hominoids. To build a preferred model for the natural history of ADH1s, we determined the sequences of nine new ADH1 genes, finding for the first time multiple paralogs in various prosimians (lemurs, strepsirhines). Database mining then identified novel ADH1 paralogs in both macaque (an OWM) and marmoset (a NWM). These were used with the previously identified human paralogs to resolve controversies relating to dates of duplication and gene conversion in the ADH1 family. Central to these controversies are differences in the topologies of trees generated from exonic (coding) sequences and intronic sequences. We provide evidence that gene conversions are the primary source of difference, using molecular clock dating of duplications and analyses of microinsertions and deletions (micro-indels). The tree topology inferred from intron sequences appear to more correctly represent the natural history of ADH1s, with the ADH1 paralogs in platyrrhines (NWMs) and catarrhines (OWMs and hominoids) having arisen by duplications shortly predating the divergence of OWMs and NWMs. We also conclude that paralogs in lemurs arose independently. Finally, we identify errors in database interpretation as the source of controversies concerning gene conversion. These analyses provide a model for the natural history of ADH1s that posits four ADH1 paralogs in the ancestor of Catarrhine and Platyrrhine primates, followed by the loss of an ADH1 paralog in the human lineage.Keywords
This publication has 66 references indexed in Scilit:
- RDP3: a flexible and fast computer program for analyzing recombinationBioinformatics, 2010
- Evolution and Survival on Eutherian Sex ChromosomesPLoS Genetics, 2009
- Phylogenetic evidence for parallel adaptive origins of digestive RNases in Asian and African leaf monkeys: A response to Xu et al. (2009)Molecular Phylogenetics and Evolution, 2009
- Development and application of a phylogenomic toolkit: Resolving the evolutionary history of Madagascar’s lemursGenome Research, 2008
- Parallel adaptive origins of digestive RNases in Asian and African leaf monkeysNature Genetics, 2006
- BLAT—The BLAST-Like Alignment ToolGenome Research, 2002
- Human liver class III alcohol and glutathione dependent formaldehyde dehydrogenase are the same enzymeBiochemical and Biophysical Research Communications, 1991
- Evidence for three genes encoding class-I alcohol dehydrogenase subunits in baboon and analysis of the 5' region of the gene encoding the ADHβ subunitGene, 1991
- Chemical and biological evolution of a nucleotide-binding proteinNature, 1974
- Studies on the properties of the human alcohol dehydrogenase isozymes determined by the different loci ADH1, ADH2, ADH3Annals of Human Genetics, 1973