Loss of Olfactory Receptor Function in Hominin Evolution

The mammalian sense of smell is governed by the largest gene family, which encodes the olfactory receptors (ORs). The gain and loss of OR genes is typically correlated with adaptations to various ecological niches. Modern humans have 853 OR genes but 55% of these have lost their function. Here we show evidence of additional OR loss of function in the Neanderthal and Denisovan hominin genomes using comparative genomic methodologies. Ten Neanderthal and 8 Denisovan ORs show evidence of loss of function that differ from the reference modern human OR genome. Some of these losses are also present in a subset of modern humans, while some are unique to each lineage. Morphological changes in the cranium of Neanderthals suggest different sensory arrangements to that of modern humans. We identify differences in functional olfactory receptor genes among modern humans, Neanderthals and Denisovans, suggesting varied loss of function across all three taxa and we highlight the utility of using genomic information to elucidate the sensory niches of extinct species.

[1]  S. Pääbo,et al.  Loss of Olfactory Receptor Genes Coincides with the Acquisition of Full Trichromatic Vision in Primates , 2004, PLoS biology.

[2]  Cole Trapnell,et al.  Ultrafast and memory-efficient alignment of short DNA sequences to the human genome , 2009, Genome Biology.

[3]  Qiaomei Fu,et al.  The complete mitochondrial DNA genome of an unknown hominin from southern Siberia , 2010, Nature.

[4]  John Ngai,et al.  The cell biology of smell , 2010, The Journal of cell biology.

[5]  Yasuhiro Go,et al.  Similar numbers but different repertoires of olfactory receptor genes in humans and chimpanzees. , 2008, Molecular biology and evolution.

[6]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[7]  D. Higgins,et al.  Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega , 2011, Molecular systems biology.

[8]  T. Hummel,et al.  Olfactory bulb volume in smokers , 2012, Experimental Brain Research.

[9]  Philip L. F. Johnson,et al.  Patterns of damage in genomic DNA sequences from a Neandertal , 2007, Proceedings of the National Academy of Sciences.

[10]  M. DePristo,et al.  The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. , 2010, Genome research.

[11]  Adrian W. Briggs,et al.  A High-Coverage Genome Sequence from an Archaic Denisovan Individual , 2012, Science.

[12]  Philip L. F. Johnson,et al.  Genetic history of an archaic hominin group from Denisova Cave in Siberia , 2010, Nature.

[13]  B. Hardy Climatic variability and plant food distribution in Pleistocene Europe: Implications for Neanderthal diet and subsistence , 2010 .

[14]  C. Crasto Olfactory Receptors , 2013, Methods in Molecular Biology.

[15]  Tsviya Olender,et al.  Personal receptor repertoires: olfaction as a model , 2012, BMC Genomics.

[16]  Giorgio Manzi,et al.  Evolution of the base of the brain in highly encephalized human species. , 2011, Nature communications.

[17]  Philip L. F. Johnson,et al.  A Draft Sequence of the Neandertal Genome , 2010, Science.

[18]  M. DePristo,et al.  A framework for variation discovery and genotyping using next-generation DNA sequencing data , 2011, Nature Genetics.

[19]  Stefano Mariani,et al.  Ecological adaptation determines functional mammalian olfactory subgenomes. , 2010, Genome research.

[20]  Fernando Martín,et al.  Environmental temperature modulates olfactory reception in Drosophila melanogaster. , 2011, Journal of insect physiology.

[21]  Gustavo Glusman,et al.  The complete human olfactory subgenome. , 2001, Genome research.