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Mol. Biol. Evol. 21(1):36-44. 2004
DOI: 10.1093/molbev/msg236
© 2004 by the Society for Molecular Biology and Evolution. ISSN: 0737-4038

Temporal Patterns of Fruit Fly (Drosophila) Evolution Revealed by Mutation Clocks

Koichiro Tamura*,{dagger}, Sankar Subramanian* and Sudhir Kumar*

* Center for Evolutionary Functional Genomics, Arizona Biodesign Institute, and School of Life Sciences, Arizona State University
{dagger} Department of Biological Sciences, Tokyo Metropolitan University, Tokyo, Japan

E-mail: s.kumar{at}asu.edu.

Drosophila melanogaster has been a canonical model organism to study genetics, development, behavior, physiology, evolution, and population genetics for nearly a century. Despite this emphasis and the completion of its nuclear genome sequence, the timing of major speciation events leading to the origin of this fruit fly remain elusive because of the paucity of extensive fossil records and biogeographic data. Use of molecular clocks as an alternative has been fraught with non-clock-like accumulation of nucleotide and amino-acid substitutions. Here we present a novel methodology in which genomic mutation distances are used to overcome these limitations and to make use of all available gene sequence data for constructing a fruit fly molecular time scale. Our analysis of 2977 pairwise sequence comparisons from 176 nuclear genes reveals a long-term fruit fly mutation clock ticking at a rate of 11.1 mutations per kilobase pair per Myr. Genomic mutation clock–based timings of the landmark speciation events leading to the evolution of D. melanogaster show that it shared most recent common ancestry 5.4 MYA with D. simulans, 12.6 MYA with D. erecta+D. orena, 12.8 MYA with D. yakuba+D. teisseri, 35.6 MYA with the takahashii subgroup, 41.3 MYA with the montium subgroup, 44.2 MYA with the ananassae subgroup, 54.9 MYA with the obscura group, 62.2 MYA with the willistoni group, and 62.9 MYA with the subgenus Drosophila. These and other estimates are compatible with those known from limited biogeographic and fossil records. The inferred temporal pattern of fruit fly evolution shows correspondence with the cooling patterns of paleoclimate changes and habitat fragmentation in the Cenozoic.

Key Words: mutation rate • Drosophila • speciation • molecular evolution • molecular clock • evolutionary distance estimation


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