HISTORICAL POPULATION SIZE CHANGE OF BOWHEAD WHALES INFERRED FROM DNA SEQUENCE POLYMORPHISM DATA
Alejandro P. Rooney
Mississippi State University, Department of Biological Sciences, Mississippi State, Mississippi 39762 E-mail: [email protected]
The Pennsylvania State University, Institute of Molecular Evolutionary Genetics, Department of Biology, 328 Mueller Laboratory, University Park, Pennsylvania 16802
Texas A&M University, College of Veterinary Medicine, Department of Veterinary Pathobiology, College Station, Texas 77843-4467
Search for more papers by this authorRodney L. Honeycutt
Texas A&M University, College of Veterinary Medicine, Department of Veterinary Pathobiology, College Station, Texas 77843-4467
Texas A&M University, Department of Wildlife & Fisheries Sciences, College Station, Texas 77843-2258
Search for more papers by this authorJames N. Derr
Texas A&M University, College of Veterinary Medicine, Department of Veterinary Pathobiology, College Station, Texas 77843-4467
Search for more papers by this authorAlejandro P. Rooney
Mississippi State University, Department of Biological Sciences, Mississippi State, Mississippi 39762 E-mail: [email protected]
The Pennsylvania State University, Institute of Molecular Evolutionary Genetics, Department of Biology, 328 Mueller Laboratory, University Park, Pennsylvania 16802
Texas A&M University, College of Veterinary Medicine, Department of Veterinary Pathobiology, College Station, Texas 77843-4467
Search for more papers by this authorRodney L. Honeycutt
Texas A&M University, College of Veterinary Medicine, Department of Veterinary Pathobiology, College Station, Texas 77843-4467
Texas A&M University, Department of Wildlife & Fisheries Sciences, College Station, Texas 77843-2258
Search for more papers by this authorJames N. Derr
Texas A&M University, College of Veterinary Medicine, Department of Veterinary Pathobiology, College Station, Texas 77843-4467
Search for more papers by this authorAbstract
Abstract.— Nucleotide sequence data from the mitochondrial control region were used from a phylogenetic context to investigate the long-term history of a population of bowhead whales (Balaena mysticetus). In addition, the coalescence time of these sequences was used to estimate the age of the inferred patterns of population size change. The results indicate that mitochondrial genetic polymorphism was not affected by a recent bottleneck that occurred near the turn of the 20th century, thereby preserving the signature of historical population size change in the mitochondrial genome. Further analysis showed that this population underwent an expansion initiated in the Middle to Late Pleistocene. As such, early Holocene changes in Arctic sea ice distribution appear to have had little influence on patterns of genetic variability in this population.
Literature Cited
- Arnason, U., A. Gullberg, and B. Widegren. 1993. Cetacean mitochondrial DNA control region: sequences of all extant baleen whales and two sperm whale species. Mol. Biol. Evol. 10: 960–970.
- Avise, J. C., J. E. Neigel, and J. Arnold. 1984. Demographic influences on mitochondrial DNA lineage survivorship in animal populations. J. Mol. Evol. 20: 99–105.
- Baker, C. S., A. Perry, J. L. Bannister, M. Weinrich, R. Abernethy, J. Calambokidis, J. Lien, R. Lambertsen, J. Urbán-Ramírez, O. Vasquez, P. Clapham, A. Alling, S. J. O'Brien, and S. R. Palumbi. 1993. Abundant mitochondrial DNA variation and world-wide population structure in humpback whales. Proc. Natl. Acad. Sci. USA 90: 8239–8243.
- Bakke, I., S. Johansen, O. Bakke, and M. R. El-Gewely. 1996. Lack of population subdivision among the minke whales (Balaenoptera acutorostrata) from Icelandic and Norwegian waters based on mitochondrial DNA sequences. Mar. Biol. 125: 1–9.
- Dyke, A. S., J. Hooper, and J. M. Savelle. 1996. A history of sea ice in the Canadian arctic archipelago based on postglacial remains of the bowhead whale (Balaena mysticetus). Arctic 49: 235–255.
- Felsenstein, J. 1992. Estimating effective population size from samples of sequences: inefficiency of pairwise and segregating sites as compared to phylogenetic estimates. Genet. Res. 59: 139–147.
- George, J. C., J. Bada, J. Zeh, L. Scott, S. E. Brown, T. O'Hara, and R. Suydam. 1999. Age and growth estimates of bowhead whales (Balaena mysticetus) via aspartic acid racemization. Can. J. Zool. 77: 1–10.
- Givens, G. H., J. E. Zeh, and A. E. Raftery. 1995. Assessment of the Bering-Chukchi Beaufort Seas stockof bowhead whales using the Baleen II model in a Bayesian synthesis framework. Rep. Int. Whal. Comm. 45: 345–364.
- Harpending, H. C., S. T. Sherry, A. R. Rogers, and M. Stoneking. 1993. The genetic structure of ancient human populations. Curr. Anthropol. 34: 483–496.
- Hillis, D. M., C. Moritz, and B. K. Maple. 1996. Molecular systematics. Sinauer, Sunderland , MA .
- Hoelzel, A. R., and G. A. Dover. 1991. Evolution of the cetacean mitochondrial D-loop region. Mol. Biol. Evol. 8: 475–493.
- Huelsenbeck, J. P., and B. Rannala. 1997. Phylogenetic methods come of age: testing hypotheses in an evolutionary context. Science 276: 227–232.
- International Whaling Commisssion. 1997. Report of the scientific committee. Rep. Int. Whal. Comm. 47: 55–112.
- Kocher, T. D., and A. C. Wilson. 1991. Sequence evolution of mitochondrial DNA in humans and chimpanzees: control region and a protein coding region. Pp. 391–413 in S. Osawa and T. Honjo, eds. Evolution of life: fossils molecules and culture. Springer, Tokyo .
- Koski, W. R., R. A. Davis, G. W. Miller, and D. E. Withrow. 1993. Reproduction. Pp. 239–274 in J. J. Burns, J. J. Montague, and C. J. Cowles, eds. The bowhead whale. Allen Press, Lawrence , KS .
- Kumar, S., K. Tamura, I. B. Jakobsen, and M. Nei. 2001. MEGA2. Institute for Molecular Evolutionary Genetics, The Pennsylvania State University, University Park , PA . Available at http://www.megasoftware.net.
- Luikart, G., F. W. Allendorf, J. M. Cornuet, and W. B. Sherwin. 1998. Distortion of allele frequency distributions provides a test for recent population bottlenecks. J. Hered. 89: 238–247.
- Lyrholm, T., O. Leimar, and U. Gyllensten. 1996. Low diversity and biased substitution patterns in the mitochondrial DNA control region of sperm whales: implications for estimates of time since common ancestry. Mol. Biol. Evol. 13(10): 1318–1326.
- Marjoram, P., and P. Donnelly. 1994. Pairwise comparisons of mitochondrial DNA sequences in subdivided populations and implications for early human evolution. Genetics 136: 673–683.
- McLeod, S. A., F. C. Whitmore Jr., and L. G. Barnes. 1993. Evolutionary relationships and classification. Pp. 45–70 in J. J. Burns, J. J. Montague, and C. J. Cowles, eds. The bowhead whale. Allen Press, Lawrence , KS .
- Moore, S. E., and R. R. Reeves. 1993. Distribution and movement. Pp. 313–507 in J. J. Burns, J. J. Montague, and C. J. Cowles, eds. The bowhead whale. Allen Press, Lawrence , KS .
- Nee, S., E. C. Holmes, A. Rambaut, and P. H. Harvey. 1995. Inferring population history from molecular phylogenies. Phil. Trans. R. Soc. Lond. B 349: 25–31.
-
Nei, M.
1987. Molecular evolutionary genetics. Columbia Univ. Press,
New York
.
10.1111/j.1365-294X.2006.02908.x Google Scholar
- Nei, M. 1992. Age of the common ancestor of human mitochondrial DNA. Mol. Biol. Evol. 9: 1176–1178.
- Nei, M. 1996. Phylogenetic analysis in molecular evolutionary genetics. Annu. Rev. Genet. 30: 371–403.
- Nei, M., and W.-H. Li. 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natl. Acad. Sci. USA 76: 5269–5273.
- Nei, M., T. Maruyama, and R. Chakraborty. 1975. The bottleneck effect and genetic variability in populations. Evolution 29: 1–10.
- Ong, C.-K., S. Nee, A. Rambaut, and P. H. Harvey. 1996. Inferring the population history of an epidemic from a phylogenetic tree. J. Theor. Biol. 182: 173–178.
- Pesole, G., C. Gissi, A. DeChirico, and C. Saccone. 1999. Nucleotide substitution rate of mammalian mitochondrial genomes. J. Mol. Evol. 48: 427–434.
- Raftery, A., and J. E. Zeh. 1998. Estimating bowhead whale population size and rate of increase from the 1993 census. J. Am. Stat. Assoc. 93: 451–463.
- Rambaut, A., P. H. Harvey, and S. Nee. 1997. End-Epi: an application for reconstructing phylogenetic and population processes from molecular sequence data. Comput. Appl. Biosci. 13: 303–306.
- Rogers, A. R. 1995. Genetic evidence for a Pleistocene population explosion. Evolution. 49: 608–615.
- Rogers, A. R., and H. C. Harpending. 1992. Population growth makes waves in the distribution of pairwise genetic differences. Mol. Biol. Evol. 9: 552–569.
- Rooney, A. P. 1998. Aseesment of recent bottlenecks: a case study of the Bering-Chukchi-Beaufort Seas stock of bowhead whales. Ph.D. diss., Texas A&M University, College Station, TX.
- Rooney, A. P., R. L. Honeycutt, S. K. Davis, and J. N. Derr. 1999. Evaluating a putative bottleneck in a population of bowhead whales from patterns of microsatellite diversity and genetic disequilibria. J. Mol. Evol. 49: 682–690.
- Rosel, P. E., A. E. Dizon, and J. E. Heyning. 1994. Genetic analysis of sympatric morphotypes of common dolphins (genus Delphinus). Mar. Biol. 119: 159–167.
- Rozas, J., and R. Rozas. 1999. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15: 174–175.
- Rugh, D. J., G. W. Miller, D. E. Withrow, and W. R. Koski. 1992. Calving intervals of bowhead whales established through photographic identifications. J. Mammal. 73: 487–490.
- Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425.
- Schell, D. M., and S. M. Saupe. 1993. Feeding and growth as indicated by stable isotopes. Pp. 491–509 in J. J. Burns, J. J. Montague, and C. J. Cowles, eds. The bowhead whale. Allen Press, Lawrence , KS .
- Slatkin, M., and R. R. Hudson. 1991. Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129: 552–562.
- Sonntag, R. M., and G. C. Broadhead. 1989. Documentation for the revised bowhead whale catch (1848–1987). Appendix 4 of Annex G, Report of the Subcommittee on Protected Species and Aboriginal Subsistence Whaling. Rep. Int. Whal. Comm. 39: 114–115.
- Sullivan, J., K. E. Holsinger, and C. Simon. 1995. Among-site rate variation and phylogenetic analysis of 12S rRNA in sigmodontine rodents. Mol. Biol. Evol. 12: 988–1001.
- Tamura, K., and M. Nei. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10: 512–526.
- Tarpley, R. J., and D. J. Hillman. 1998. Observations on ovary morphology, fetal size, and functional correlates in the bowhead whale, Balaena mysticetus. Final report to the Department of Wildlife Management, North Slope Borough, AK.
- Vigilant, L., M. Stoneking, H. Harpending, K. Hawkes, and A. C. Wilson. 1991. African populations and the evolution of human mitochondrial DNA. Science 253: 1503–1507.
- Wilson, A. C., R. L. Cann, S. M. Carr, M. L. George, U. B. Gyllensten, K. M. Helm Bychowski, R. G. Higuchi, S. R. Palumbi, E. M. Prager, R. D. Sage, and M. Stoneking. 1985. Mitochondrial DNA and two perspectives on evolutionary genetics. Biol. J. Linn. Soc. 26: 375–400.
- Woodby, D. A., and D. B. Botkin. 1993. Stock sizes prior to commercial whaling. Pp. 387–407 in J. J. Burns, J. J. Montague, and C. J. Cowles, eds. The bowhead whale. Allen Press, Lawrence , KS .