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151. Primate phylogenomics uncovers multiple rapid radiations and ancient interspecific introgression

Author

Vanderpool, Dan, Minh, Bui Quang, Lanfear, Robert, Hughes, Daniel, Murali, Shwetha, Harris, R. Alan, Raveendran, Muthuswamy, Muzny, Donna M., Hibbins, Mark S., Williamson, Robert J., Gibbs, Richard A., Worley, Kim C., Rogers, Jeffrey, Hahn, Matthew W., Vanderpool, Dan, Minh, Bui Quang, Lanfear, Robert, Hughes, Daniel, Murali, Shwetha, Harris, R. Alan, Raveendran, Muthuswamy, Muzny, Donna M., Hibbins, Mark S., Williamson, Robert J., Gibbs, Richard A., Worley, Kim C., Rogers, Jeffrey, and Hahn, Matthew W.

Abstract

Our understanding of the evolutionary history of primates is undergoing continual revision due to ongoing genome sequencing efforts. Bolstered by growing fossil evidence, these data have led to increased acceptance of once controversial hypotheses regarding phylogenetic relationships, hybridization and introgression, and the biogeographical history of primate groups. Among these findings is a pattern of recent introgression between species within all major primate groups examined to date, though little is known about introgression deeper in time. To address this and other phylogenetic questions, here, we present new reference genome assemblies for 3 Old World monkey (OWM) species: Colobus angolensis ssp. palliatus (the black and white colobus), Macaca nemestrina (southern pig-tailed macaque), and Mandrillus leucophaeus (the drill). We combine these data with 23 additional primate genomes to estimate both the species tree and individual gene trees using thousands of loci. While our species tree is largely consistent with previous phylogenetic hypotheses, the gene trees reveal high levels of genealogical discordance associated with multiple primate radiations. We use strongly asymmetric patterns of gene tree discordance around specific branches to identify multiple instances of introgression between ancestral primate lineages. In addition, we exploit recent fossil evidence to perform fossil-calibrated molecular dating analyses across the tree. Taken together, our genome-wide data help to resolve multiple contentious sets of relationships among primates, while also providing insight into the biological processes and technical artifacts that led to the disagreements in the first place. Combining three newly sequenced primate genomes with other published genomes, this study adapts a little-known method for detecting ancient introgression to genome-scale data, revealing multiple previously unknown examples of hybridization between primate species.

Published
2020

152. Gene content evolution in the arthropods

Author

Thomas, Gregg W. C., Dohmen, Elias, Hughes, Daniel S. T., Murali, Shwetha C., Poelchau, Monica, Glastad, Karl, Anstead, Clare A., Ayoub, Nadia A., Batterham, Phillip, Bellair, Michelle, Binford, Greta J., Chao, Hsu, Chen, Yolanda H., Childers, Christopher, Dinh, Huyen, Doddapaneni, Harsha Vardhan, Duan, Jian J., Dugan, Shannon, Esposito, Lauren A., Friedrich, Markus, Garb, Jessica, Gasser, Robin B., Goodisman, Michael A. D., Gundersen-Rindal, Dawn E., Han, Yi, Handler, Alfred M., Hatakeyama, Masatsugu, Hering, Lars, Hunter, Wayne B., Ioannidis, Panagiotis, Jayaseelan, Joy C., Kalra, Divya, Khila, Abderrahman, Korhonen, Pasi K., Lee, Carol Eunmi, Lee, Sandra L., Li, Yiyuan, Lindsey, Amelia R. I., Mayer, Georg, McGregor, Alistair P., McKenna, Duane D., Misof, Bernhard, Munidasa, Mala, Munoz-Torres, Monica, Muzny, Donna M., Niehuis, Oliver, Osuji-Lacy, Nkechinyere, Palli, Subba R., Panfilio, Kristen A., Pechmann, Matthias, Perry, Trent, Peters, Ralph S., Poynton, Helen C., Prpic, Nikola-Michael, Qu, Jiaxin, Rotenberg, Dorith, Schal, Coby, Schoville, Sean D., Scully, Erin D., Skinner, Evette, Sloan, Daniel B., Stouthamer, Richard, Strand, Michael R., Szucsich, Nikolaus U., Wijeratne, Asela, Young, Neil D., Zattara, Eduardo E., Benoit, Joshua B., Zdobnov, Evgeny M., Pfrender, Michael E., Hackett, Kevin J., Werren, John H., Worley, Kim C., Gibbs, Richard A., Chipman, Ariel D., Waterhouse, Robert M., Bornberg-Bauer, Erich, Hahn, Matthew W., Richards, Stephen, Thomas, Gregg W. C., Dohmen, Elias, Hughes, Daniel S. T., Murali, Shwetha C., Poelchau, Monica, Glastad, Karl, Anstead, Clare A., Ayoub, Nadia A., Batterham, Phillip, Bellair, Michelle, Binford, Greta J., Chao, Hsu, Chen, Yolanda H., Childers, Christopher, Dinh, Huyen, Doddapaneni, Harsha Vardhan, Duan, Jian J., Dugan, Shannon, Esposito, Lauren A., Friedrich, Markus, Garb, Jessica, Gasser, Robin B., Goodisman, Michael A. D., Gundersen-Rindal, Dawn E., Han, Yi, Handler, Alfred M., Hatakeyama, Masatsugu, Hering, Lars, Hunter, Wayne B., Ioannidis, Panagiotis, Jayaseelan, Joy C., Kalra, Divya, Khila, Abderrahman, Korhonen, Pasi K., Lee, Carol Eunmi, Lee, Sandra L., Li, Yiyuan, Lindsey, Amelia R. I., Mayer, Georg, McGregor, Alistair P., McKenna, Duane D., Misof, Bernhard, Munidasa, Mala, Munoz-Torres, Monica, Muzny, Donna M., Niehuis, Oliver, Osuji-Lacy, Nkechinyere, Palli, Subba R., Panfilio, Kristen A., Pechmann, Matthias, Perry, Trent, Peters, Ralph S., Poynton, Helen C., Prpic, Nikola-Michael, Qu, Jiaxin, Rotenberg, Dorith, Schal, Coby, Schoville, Sean D., Scully, Erin D., Skinner, Evette, Sloan, Daniel B., Stouthamer, Richard, Strand, Michael R., Szucsich, Nikolaus U., Wijeratne, Asela, Young, Neil D., Zattara, Eduardo E., Benoit, Joshua B., Zdobnov, Evgeny M., Pfrender, Michael E., Hackett, Kevin J., Werren, John H., Worley, Kim C., Gibbs, Richard A., Chipman, Ariel D., Waterhouse, Robert M., Bornberg-Bauer, Erich, Hahn, Matthew W., and Richards, Stephen

Abstract

Background Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods. Results Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality, and chemoperception. Conclusions These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.

Published
2020

153. Evolutionary superscaffolding and chromosome anchoring to improve Anopheles genome assemblies

Author

Entomology, Waterhouse, Robert M., Aganezov, Sergey, Anselmetti, Yoann, Lee, Jiyoung, Ruzzante, Livio, Reijnders, Maarten J. M. F., Feron, Romain, Bérard, Sèverine, George, Phillip, Hahn, Matthew W., Howell, Paul I., Kamali, Maryam, Koren, Sergey, Lawson, Daniel, Maslen, Gareth, Peery, Ashley, Phillippy, Adam M., Sharakhova, Maria V., Tannier, Eric, Unger, Maria F., Zhang, Simo V., Alekseyev, Max A., Besansky, Nora J., Chauve, Cedric, Emrich, Scott J., Sharakhov, Igor V., Entomology, Waterhouse, Robert M., Aganezov, Sergey, Anselmetti, Yoann, Lee, Jiyoung, Ruzzante, Livio, Reijnders, Maarten J. M. F., Feron, Romain, Bérard, Sèverine, George, Phillip, Hahn, Matthew W., Howell, Paul I., Kamali, Maryam, Koren, Sergey, Lawson, Daniel, Maslen, Gareth, Peery, Ashley, Phillippy, Adam M., Sharakhova, Maria V., Tannier, Eric, Unger, Maria F., Zhang, Simo V., Alekseyev, Max A., Besansky, Nora J., Chauve, Cedric, Emrich, Scott J., and Sharakhov, Igor V.

Abstract

Background New sequencing technologies have lowered financial barriers to whole genome sequencing, but resulting assemblies are often fragmented and far from ‘finished’. Updating multi-scaffold drafts to chromosome-level status can be achieved through experimental mapping or re-sequencing efforts. Avoiding the costs associated with such approaches, comparative genomic analysis of gene order conservation (synteny) to predict scaffold neighbours (adjacencies) offers a potentially useful complementary method for improving draft assemblies. Results We evaluated and employed 3 gene synteny-based methods applied to 21 Anopheles mosquito assemblies to produce consensus sets of scaffold adjacencies. For subsets of the assemblies, we integrated these with additional supporting data to confirm and complement the synteny-based adjacencies: 6 with physical mapping data that anchor scaffolds to chromosome locations, 13 with paired-end RNA sequencing (RNAseq) data, and 3 with new assemblies based on re-scaffolding or long-read data. Our combined analyses produced 20 new superscaffolded assemblies with improved contiguities: 7 for which assignments of non-anchored scaffolds to chromosome arms span more than 75% of the assemblies, and a further 7 with chromosome anchoring including an 88% anchored Anopheles arabiensis assembly and, respectively, 73% and 84% anchored assemblies with comprehensively updated cytogenetic photomaps for Anopheles funestus and Anopheles stephensi. Conclusions Experimental data from probe mapping, RNAseq, or long-read technologies, where available, all contribute to successful upgrading of draft assemblies. Our evaluations show that gene synteny-based computational methods represent a valuable alternative or complementary approach. Our improved Anopheles reference assemblies highlight the utility of applying comparative genomics approaches to improve community genomic resources.

Published
2020

158. Species Tree Inference Methods Intended to Deal with Incomplete Lineage Sorting Are Robust to the Presence of Paralogs.

Author

Yan, Zhi, Smith, Megan L, Du, Peng, Hahn, Matthew W, and Nakhleh, Luay

Subjects
SPECIES, CHROMOSOME duplication
Abstract

Many recent phylogenetic methods have focused on accurately inferring species trees when there is gene tree discordance due to incomplete lineage sorting (ILS). For almost all of these methods, and for phylogenetic methods in general, the data for each locus are assumed to consist of orthologous, single-copy sequences. Loci that are present in more than a single copy in any of the studied genomes are excluded from the data. These steps greatly reduce the number of loci available for analysis. The question we seek to answer in this study is: what happens if one runs such species tree inference methods on data where paralogy is present, in addition to or without ILS being present? Through simulation studies and analyses of two large biological data sets, we show that running such methods on data with paralogs can still provide accurate results. We use multiple different methods, some of which are based directly on the multispecies coalescent model, and some of which have been proven to be statistically consistent under it. We also treat the paralogous loci in multiple ways: from explicitly denoting them as paralogs, to randomly selecting one copy per species. In all cases, the inferred species trees are as accurate as equivalent analyses using single-copy orthologs. Our results have significant implications for the use of ILS-aware phylogenomic analyses, demonstrating that they do not have to be restricted to single-copy loci. This will greatly increase the amount of data that can be used for phylogenetic inference.[Gene duplication and loss; incomplete lineage sorting; multispecies coalescent; orthology; paralogy.] [ABSTRACT FROM AUTHOR]

Published
2022
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159. Phylogenomic approaches to detecting and characterizing introgression.

Author

Hibbins, Mark S. and Hahn, Matthew W.

Subjects
*PHYLOGENY, *SEQUENCE analysis, *CELLULAR signal transduction, *HUMAN reproductive technology, *GENOMICS
Abstract

Phylogenomics has revealed the remarkable frequency with which introgression occurs across the tree of life. These discoveries have been enabled by the rapid growth of methods designed to detect and characterize introgression from whole-genome sequencing data. A large class of phylogenomic methods makes use of data across species to infer and characterize introgression based on expectations from the multispecies coalescent. These methods range from simple tests, such as the D-statistic, to model-based approaches for inferring phylogenetic networks. Here, we provide a detailed overview of the various signals that different modes of introgression are expected leave in the genome, and how current methods are designed to detect them. We discuss the strengths and pitfalls of these approaches and identify areas for future development, highlighting the different signals of introgression, and the power of each method to detect them. We conclude with a discussion of current challenges in inferring introgression and how they could potentially be addressed. [ABSTRACT FROM AUTHOR]

Published
2022
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162. Reproductive Longevity Predicts Mutation Rates in Primates

Author

Thomas, Gregg W.C., Wang, Richard J., Puri, Arthi, Harris, R. Alan, Raveendran, Muthuswamy, Hughes, Daniel S.T., Murali, Shwetha C., Williams, Lawrence E., Doddapaneni, Harsha, Muzny, Donna M., Gibbs, Richard A., Abee, Christian R., Galinski, Mary R., Worley, Kim C., Rogers, Jeffrey, Radivojac, Predrag, and Hahn, Matthew W.

Published
2018
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164. Species Tree Inference under the Multispecies Coalescent on Data with Paralogs is Accurate

Author

Du, Peng, Hahn, Matthew W., and Nakhleh, Luay

Abstract

The multispecies coalescent (MSC) has emerged as a powerful and desirable framework for species tree inference in phylogenomic studies. Under this framework, the data for each locus is assumed to consist of orthologous, single-copy genes, and heterogeneity across loci is assumed to be due to incomplete lineage sorting (ILS). These assumptions have led biologists who use ILS-aware inference methods, whether based directly on the MSC or proven to be statistically consistent under it (collectively referred to here as MSC-based methods), to exclude all loci that are present in more than a single copy in any of the studied genomes. Furthermore, such analyses entail orthology assignment to avoid the potential of hidden paralogy in the data. The question we seek to answer in this study is: What happens if one runs such species tree inference methods on data where paralogy is present, in addition to or without ILS being present? Through simulation studies and analyses of two biological data sets, we show that running such methods on data with paralogs, while treating all gene copies within a family as alleles from multiple individuals or by randomly selecting one copy per species, provide very accurate results. Our results have two significant implications. First, MSC-based phylogenomic analyses do not have to be restricted to single-copy loci, thus maximizing the amount of data to be used. Second, when an MSC-based inference Eļl method infers an accurate species tree, this does not necessarily imply that ILS was the main factor in the heterogeneity across loci.

Published
2018
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166. The potential for a released autosomal X-shredder becoming a driving-Y chromosome and invasively suppressing wild populations of malaria mosquitoes

Author

Alcalay, Yehonatan, primary, Fuchs, Silke, additional, Galizi, Roberto, additional, Bernardini, Federica, additional, Haghighat-Khah, Roya Elaine, additional, Rusch, Douglas B., additional, Adrion, Jeffrey R., additional, Hahn, Matthew W., additional, Tortosa, Pablo, additional, and Papathanos, Philippos Aris, additional

Published
2019
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170. Paternal age in rhesus macaques is positively associated with germline mutation accumulation but not with measures of offspring sociability

Author

Wang, Richard J., primary, Thomas, Gregg W.C., additional, Raveendran, Muthuswamy, additional, Harris, R. Alan, additional, Doddapaneni, Harshavardhan, additional, Muzny, Donna M., additional, Capitanio, John P., additional, Radivojac, Predrag, additional, Rogers, Jeffrey, additional, and Hahn, Matthew W., additional

Published
2019
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172. Evolutionary superscaffolding and chromosome anchoring to improve Anopheles genome assemblies.

Author

Waterhouse, Robert M., Aganezov, Sergey, Anselmetti, Yoann, Lee, Jiyoung, Ruzzante, Livio, Reijnders, Maarten J.M.F., Feron, Romain, Bérard, Sèverine, George, Phillip, Hahn, Matthew W., Howell, Paul I., Kamali, Maryam, Koren, Sergey, Lawson, Daniel, Maslen, Gareth, Peery, Ashley, Phillippy, Adam M., Sharakhova, Maria V., Tannier, Eric, Unger, Maria F., Zhang, Simo V., Alekseyev, Max A., Besansky, Nora J., Chauve, Cedric, Emrich, Scott J., Sharakhov, Igor V., Waterhouse, Robert M., Aganezov, Sergey, Anselmetti, Yoann, Lee, Jiyoung, Ruzzante, Livio, Reijnders, Maarten J.M.F., Feron, Romain, Bérard, Sèverine, George, Phillip, Hahn, Matthew W., Howell, Paul I., Kamali, Maryam, Koren, Sergey, Lawson, Daniel, Maslen, Gareth, Peery, Ashley, Phillippy, Adam M., Sharakhova, Maria V., Tannier, Eric, Unger, Maria F., Zhang, Simo V., Alekseyev, Max A., Besansky, Nora J., Chauve, Cedric, Emrich, Scott J., and Sharakhov, Igor V.

Published
2019

173. Origins and Long-Term Patterns of Copy-Number Variation in Rhesus Macaques.

Author

Thomas, Gregg W C, Wang, Richard J, Nguyen, Jelena, Harris, R Alan, Raveendran, Muthuswamy, Rogers, Jeffrey, and Hahn, Matthew W

Subjects
DNA copy number variations, GENETIC mutation, SPERMATOGENESIS, GENOMES, DELETION mutation
Abstract

Mutations play a key role in the development of disease in an individual and the evolution of traits within species. Recent work in humans and other primates has clarified the origins and patterns of single-nucleotide variants, showing that most arise in the father's germline during spermatogenesis. It remains unknown whether larger mutations, such as deletions and duplications of hundreds or thousands of nucleotides, follow similar patterns. Such mutations lead to copy-number variation (CNV) within and between species, and can have profound effects by deleting or duplicating genes. Here, we analyze patterns of CNV mutations in 32 rhesus macaque individuals from 14 parent–offspring trios. We find the rate of CNV mutations per generation is low (less than one per genome) and we observe no correlation between parental age and the number of CNVs that are passed on to offspring. We also examine segregating CNVs within the rhesus macaque sample and compare them to a similar data set from humans, finding that both species have far more segregating deletions than duplications. We contrast this with long-term patterns of gene copy-number evolution between 17 mammals, where the proportion of deletions that become fixed along the macaque lineage is much smaller than the proportion of segregating deletions. These results suggest purifying selection acting on deletions, such that the majority of them are removed from the population over time. Rhesus macaques are an important biomedical model organism, so these results will aid in our understanding of this species and the disease models it supports. [ABSTRACT FROM AUTHOR]

Published
2021
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174. The sequencing and interpretation of the genome obtained from a Serbian individual

Author

Robinson-Rechavi, Marc, Mohammed Ismail, Wazim, Pagel, Kymberleigh A., Pejaver, Vikas, Zhang, Simo V., Casasa, Sofia, Mort, Matthew, Cooper, David, Hahn, Matthew W., and Radivojac, Predrag

Subjects
0301 basic medicine, Proband, Male, European People, Hominids, Ethnic group, Social Sciences, Genome, Geographical Locations, Serbian People, Ethnicity, Ethnicities, Neanderthals, Multidisciplinary, Paleogenetics, Genomics, Eastern european, Europe, language, Medicine, Female, Physical Anthropology, Serbian, Serbia, Research Article, Science, Context (language use), Biology, 03 medical and health sciences, Archaic Humans, Genomic Medicine, Paleoanthropology, Genetics, Hominins, Animals, Humans, Quantitative Biology - Genomics, Genetic Predisposition to Disease, Genomics (q-bio.GN), Genome, Human, Biology and Life Sciences, Paleontology, Computational Biology, Genetic Variation, Genome Analysis, language.human_language, 030104 developmental biology, Evolutionary biology, Anthropology, FOS: Biological sciences, People and Places, Earth Sciences, Population Groupings, Slavic People, Genome-Wide Association Study
Abstract

Recent genetic studies and whole-genome sequencing projects have greatly improved our understanding of human variation and clinically actionable genetic information. Smaller ethnic populations, however, remain underrepresented in both individual and large-scale sequencing efforts and hence present an opportunity to discover new variants of biomedical and demographic significance. This report describes the sequencing and analysis of a genome obtained from an individual of Serbian origin, introducing tens of thousands of previously unknown variants to the currently available pool. Ancestry analysis places this individual in close proximity of the Central and Eastern European populations; i.e., closest to Croatian, Bulgarian and Hungarian individuals and, in terms of other Europeans, furthest from Ashkenazi Jewish, Spanish, Sicilian, and Baltic individuals. Our analysis confirmed gene flow between Neanderthal and ancestral pan-European populations, with similar contributions to the Serbian genome as those observed in other European groups. Finally, to assess the burden of potentially disease-causing/clinically relevant variation in the sequenced genome, we utilized manually curated genotype-phenotype association databases and variant-effect predictors. We identified several variants that have previously been associated with severe early-onset disease that is not evident in the proband, as well as variants that could yet prove to be clinically relevant to the proband over the next decades. The presence of numerous private and low-frequency variants along with the observed and predicted disease-causing mutations in this genome exemplify some of the global challenges of genome interpretation, especially in the context of understudied ethnic groups., Comment: 18 pages, 2 figures

Published
2018
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182. Evolutionary superscaffolding and chromosome anchoring to improve Anopheles genome assemblies

Author

Waterhouse, Robert M., primary, Aganezov, Sergey, additional, Anselmetti, Yoann, additional, Lee, Jiyoung, additional, Ruzzante, Livio, additional, Reijnders, Maarten J.M.F., additional, Feron, Romain, additional, Bérard, Sèverine, additional, George, Phillip, additional, Hahn, Matthew W., additional, Howell, Paul I., additional, Kamali, Maryam, additional, Koren, Sergey, additional, Lawson, Daniel, additional, Maslen, Gareth, additional, Peery, Ashley, additional, Phillippy, Adam M., additional, Sharakhova, Maria V., additional, Tannier, Eric, additional, Unger, Maria F., additional, Zhang, Simo V., additional, Alekseyev, Max A., additional, Besansky, Nora J., additional, Chauve, Cedric, additional, Emrich, Scott J., additional, and Sharakhov, Igor V., additional

Published
2018
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186. Gene Content Evolution in the Arthropods

Author

Thomas, Gregg W.C., primary, Dohmen, Elias, additional, Hughes, Daniel S.T., additional, Murali, Shwetha C., additional, Poelchau, Monica, additional, Glastad, Karl, additional, Anstead, Clare A., additional, Ayoub, Nadia A., additional, Batterham, Phillip, additional, Bellair, Michelle, additional, Binford, Gretta J., additional, Chao, Hsu, additional, Chen, Yolanda H., additional, Childers, Christopher, additional, Dinh, Huyen, additional, Doddapaneni, HarshaVardhan, additional, Duan, Jian J., additional, Dugan, Shannon, additional, Esposito, Lauren A., additional, Friedrich, Markus, additional, Garb, Jessica, additional, Gasser, Robin B., additional, Goodisman, Michael A.D., additional, Gundersen-Rindal, Dawn E., additional, Han, Yi, additional, Handler, Alfred M., additional, Hatakeyama, Masatsugu, additional, Hering, Lars, additional, Hunter, Wayne B., additional, Ioannidis, Panagiotis, additional, Jayaseelan, Joy C., additional, Kalra, Divya, additional, Khila, Abderrahman, additional, Korhonen, Pasi K., additional, Lee, Carol Eunmi, additional, Lee, Sandra L., additional, Li, Yiyuan, additional, Lindsey, Amelia R.I., additional, Mayer, Georg, additional, McGregor, Alistair P., additional, McKenna, Duane D., additional, Misof, Bernhard, additional, Munidasa, Mala, additional, Munoz-Torres, Monica, additional, Muzny, Donna M., additional, Niehuis, Oliver, additional, Osuji-Lacy, Nkechinyere, additional, Palli, Subba R., additional, Panfilio, Kristen A., additional, Pechmann, Matthias, additional, Perry, Trent, additional, Peters, Ralph S., additional, Poynton, Helen C., additional, Prpic, Nikola-Michael, additional, Qu, Jiaxin, additional, Rotenberg, Dorith, additional, Schal, Coby, additional, Schoville, Sean D., additional, Scully, Erin D., additional, Skinner, Evette, additional, Sloan, Daniel B., additional, Stouthamer, Richard, additional, Strand, Michael R., additional, Szucsich, Nikolaus U., additional, Wijeratne, Asela, additional, Young, Neil D., additional, Zattara, Eduardo E., additional, Benoit, Joshua B., additional, Zdobnov, Evgeny M., additional, Pfrender, Michael E., additional, Hackett, Kevin J., additional, Werren, John H., additional, Worley, Kim C., additional, Gibbs, Richard A., additional, Chipman, Ariel D., additional, Waterhouse, Robert M., additional, Bornberg-Bauer, Erich, additional, Hahn, Matthew W., additional, and Richards, Stephen, additional

Published
2018
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192. Reproductive longevity predicts mutation rates in primates

Author

Thomas, Gregg W.C., primary, Wang, Richard J., additional, Puri, Arthi, additional, Harris, R. Alan, additional, Raveendran, Muthuswamy, additional, Hughes, Daniel, additional, Murali, Shwetha, additional, Williams, Lawrence, additional, Doddapaneni, Harsha, additional, Muzny, Donna, additional, Gibbs, Richard, additional, Abee, Christian, additional, Galinski, Mary R., additional, Worley, Kim C., additional, Rogers, Jeffrey, additional, Radivojac, Predrag, additional, and Hahn, Matthew W., additional

Published
2018
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