A Genome Sequence Resource for the Aye-Aye (Daubentonia madagascariensis), a Nocturnal Lemur from Madagascar

We present a high-coverage draft genome assembly of the aye-aye (Daubentonia madagascariensis), a highly unusual nocturnal primate from Madagascar. Our assembly totals ∼3.0 billion bp (3.0 Gb), roughly the size of the human genome, comprised of ∼2.6 million scaffolds (N50 scaffold size = 13,597 bp) based on short paired-end sequencing reads. We compared the aye-aye genome sequence data with four other published primate genomes (human, chimpanzee, orangutan, and rhesus macaque) as well as with the mouse and dog genomes as nonprimate outgroups. Unexpectedly, we observed strong evidence for a relatively slow substitution rate in the aye-aye lineage compared with these and other primates. In fact, the aye-aye branch length is estimated to be ∼10% shorter than that of the human lineage, which is known for its low substitution rate. This finding may be explained, in part, by the protracted aye-aye life-history pattern, including late weaning and age of first reproduction relative to other lemurs. Additionally, the availability of this draft lemur genome sequence allowed us to polarize nucleotide and protein sequence changes to the ancestral primate lineage—a critical period in primate evolution, for which the relevant fossil record is sparse. Finally, we identified 293,800 high-confidence single nucleotide polymorphisms in the donor individual for our aye-aye genome sequence, a captive-born individual from two wild-born parents. The resulting heterozygosity estimate of 0.051% is the lowest of any primate studied to date, which is understandable considering the aye-aye's extensive home-range size and relatively low population densities. Yet this level of genetic diversity also suggests that conservation efforts benefiting this unusual species should be prioritized, especially in the face of the accelerating degradation and fragmentation of Madagascar's forests.

[1]  Páll Melsted,et al.  Comparative RNA sequencing reveals substantial genetic variation in endangered primates. , 2012, Genome research.

[2]  Steven J. Plimpton,et al.  MapReduce in MPI for Large-scale graph algorithms , 2011, Parallel Comput..

[3]  S. Pääbo,et al.  Bonobos Fall within the Genomic Variation of Chimpanzees , 2011, PloS one.

[4]  S. O’Brien,et al.  A Molecular Phylogeny of Living Primates , 2011, PLoS genetics.

[5]  Walter Pirovano,et al.  BIOINFORMATICS APPLICATIONS , 2022 .

[6]  Albert J. Vilella,et al.  Comparative and demographic analysis of orang-utan genomes , 2011, Nature.

[7]  A. Gnirke,et al.  High-quality draft assemblies of mammalian genomes from massively parallel sequence data , 2010, Proceedings of the National Academy of Sciences.

[8]  G. Perry,et al.  Genomic-scale capture and sequencing of endogenous DNA from feces. , 2010, Molecular ecology.

[9]  David R. Kelley,et al.  Quake: quality-aware detection and correction of sequencing errors , 2010, Genome Biology.

[10]  W. Jungers,et al.  "Life history space": a multivariate analysis of life history variation in extant and extinct Malagasy lemurs. , 2010, American journal of physical anthropology.

[11]  T. Okamoto,et al.  A-kinase-interacting Protein 1 (AKIP1) Acts as a Molecular Determinant of PKA in NF-κB Signaling , 2010, The Journal of Biological Chemistry.

[12]  L. Quintana-Murci,et al.  From evolutionary genetics to human immunology: how selection shapes host defence genes , 2010, Nature Reviews Genetics.

[13]  M. Steiper,et al.  Age at first reproduction explains rate variation in the strepsirrhine molecular clock , 2009, Proceedings of the National Academy of Sciences.

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

[15]  Richard Durbin,et al.  Sequence analysis Fast and accurate short read alignment with Burrows – Wheeler transform , 2009 .

[16]  Lior Pachter,et al.  Fast Statistical Alignment , 2009, PLoS Comput. Biol..

[17]  Hans-Peter Lenhof,et al.  GeneTrailExpress: a web-based pipeline for the statistical evaluation of microarray experiments , 2008, BMC Bioinformatics.

[18]  F. Palstra,et al.  Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? , 2008, Molecular ecology.

[19]  August E. Woerner,et al.  A novel DNA sequence database for analyzing human demographic history. , 2008, Genome research.

[20]  H. Willard,et al.  Development and application of a phylogenomic toolkit: resolving the evolutionary history of Madagascar's lemurs. , 2008, Genome research.

[21]  B. Demes,et al.  How Big Were the "Giant" Extinct Lemurs of Madagascar? , 2008 .

[22]  N. Stevens,et al.  Paleontological Exploration in Africa A View from the Rukwa Rift Basin of Tanzania , 2008 .

[23]  G. Perry,et al.  Signatures of functional constraint at aye-aye opsin genes: the potential of adaptive color vision in a nocturnal primate. , 2007, Molecular biology and evolution.

[24]  M. Nei,et al.  MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. , 2007, Molecular biology and evolution.

[25]  Ziheng Yang PAML 4: phylogenetic analysis by maximum likelihood. , 2007, Molecular biology and evolution.

[26]  Ryan D. Hernandez,et al.  Demographic Histories and Patterns of Linkage Disequilibrium in Chinese and Indian Rhesus Macaques , 2007, Science.

[27]  David N. Messina,et al.  Evolutionary and Biomedical Insights from the Rhesus Macaque Genome , 2007, Science.

[28]  S. Cachel Primate adaptation and evolution , 1989, International Journal of Primatology.

[29]  Eric Vigoda,et al.  Heterogeneous Genomic Molecular Clocks in Primates , 2006, PLoS genetics.

[30]  B. Nickel,et al.  Demographic History and Genetic Differentiation in Apes , 2006, Current Biology.

[31]  G. Perry,et al.  Molecular evolution of the primate developmental genes MSX1 and PAX9. , 2006, Molecular biology and evolution.

[32]  M. Dagosto,et al.  Primate Origins and Evolution. A phylogenetic reconstruction , 1991, International Journal of Primatology.

[33]  W. Jungers,et al.  Ecology and Extinction of Madagascar's Subfossil Lemurs , 2006 .

[34]  L. Gould,et al.  Lemurs : ecology and adaptation , 2006 .

[35]  R. Hudson,et al.  Interrogating multiple aspects of variation in a full resequencing data set to infer human population size changes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[36]  R. Frankham Genetics and extinction , 2005 .

[37]  Jean L. Chang,et al.  Initial sequence of the chimpanzee genome and comparison with the human genome , 2005, Nature.

[38]  Nathan M. Young,et al.  Genomic data support the hominoid slowdown and an Early Oligocene estimate for the hominoid-cercopithecoid divergence. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[39]  E. Lander,et al.  Finishing the euchromatic sequence of the human genome , 2004 .

[40]  J. Bonfield,et al.  Finishing the euchromatic sequence of the human genome , 2004, Nature.

[41]  M. Nei,et al.  Prospects for inferring very large phylogenies by using the neighbor-joining method. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[42]  S. Pääbo,et al.  Evidence for a complex demographic history of chimpanzees. , 2004, Molecular biology and evolution.

[43]  Wen-Hsiung Li,et al.  Nucleotide Diversity in Gorillas , 2004, Genetics.

[44]  International Human Genome Sequencing Consortium Finishing the euchromatic sequence of the human genome , 2004 .

[45]  Ziheng Yang,et al.  Comparison of likelihood and Bayesian methods for estimating divergence times using multiple gene Loci and calibration points, with application to a radiation of cute-looking mouse lemur species. , 2003, Systematic biology.

[46]  K. Kidd,et al.  Low nucleotide diversity in chimpanzees and bonobos. , 2003, Genetics.

[47]  Michael E. Pereira,et al.  Primate life histories and socioecology , 2003 .

[48]  Wen-Hsiung Li,et al.  Slow molecular clocks in Old World monkeys, apes, and humans. , 2002, Molecular biology and evolution.

[49]  M. Ashburner,et al.  Gene Ontology: tool for the unification of biology , 2000, Nature Genetics.

[50]  E. Sterling,et al.  Tool Use, Aye-Ayes, and Sensorimotor Intelligence , 1999, Folia Primatologica.

[51]  Gapped BLAST and PSI-BLAST: A new , 1997 .

[52]  G. A. Doyle,et al.  Creatures of the dark : the nocturnal prosimians , 1995 .

[53]  E. Simons History, Anatomy, Subfossil Record and Management of Daubentonia Madagascariensis , 1995 .

[54]  R. M. Winn Preliminary study of the sexual behaviour of three aye-ayes (Daubentonia madagascariensis) in captivity. , 1994, Folia primatologica; international journal of primatology.

[55]  R. Mittermeier,et al.  Lemurs of Madagascar , 1994 .

[56]  E. Simons The giant aye-aye Daubentonia robusta. , 1994, Folia primatologica; international journal of primatology.

[57]  F. Tajima,et al.  Simple methods for testing the molecular evolutionary clock hypothesis. , 1993, Genetics.

[58]  C. J. Erickson Percussive foraging in the aye-aye, Daubentonia madagascariensis , 1991, Animal Behaviour.

[59]  Taizo Iwano,et al.  Feeding Behaviour of the Aye-Aye (Daubentonia madagascariensis) on Nuts of Ramy (Canarium madagascariensis) , 1988 .

[60]  R. MacPhee,et al.  Modified subfossil aye-aye incisors from southwestern Madagascar: species allocation and paleoecological significance. , 1988, Folia primatologica; international journal of primatology.

[61]  Phyllis C. Lee,et al.  Primate Ontogeny, Cognition and Social Behaviour , 1986 .