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Phenotypic variance inflation in fossil samples: an empirical assessment

Published online by Cambridge University Press:  08 April 2016

Gene Hunt*
Affiliation:
Committee on Evolutionary Biology, University of Chicago, Chicago, Illinois 60637

Abstract

Evolutionary change during the interval in which a fossil sample accumulates will inflate the variance of that sample relative to the population-level standing variation. If this effect is widespread and severe, paleontological samples will not provide reliable estimates of population variation. Although the few published studies conducted to test this possibility have found similar levels of variation in samples differing greatly in temporal acuity, the paucity of case studies prevents assessing the generality of this pattern. In this paper, two independent, literature-based approaches are used to greatly expand the data available to address this issue. The first approach compares morphometric variability in Quaternary mammal samples with samples from related modern populations. The second approach artificially lumps separate samples from evolving lineages and calculates the variance effects of this analytical time-averaging. Both approaches yield consistent results indicating that variance observed in time-averaged samples is typically only slightly inflated (approximately 5%) relative to population-level values. This finding suggests that rates of evolution are typically slow when scaled to within-population variation, providing support for relative stasis as the dominant mode of within-lineage evolution. An important practical consequence of these findings is that time-averaged fossil samples generally show trait variances and covariances that are similar to population-level parameters, which has been an important but implicit assumption in many paleontological studies of phenotypic variation.

Type
Research Article
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Arnold, S. J., and Phillips, P. C. 1999. Hierarchical comparison of genetic variance-covariance matrices. II. Coastal-inland divergence in the garter snake, Thamnophis elegans. Evolution 53:15161527.Google Scholar
Barnosky, A. D. 1993. Mosaic evolution at the population level in Microtus pennsylvanicus. Pp. 2459in Martin, R. A. and Barnosky, A. D., eds. Morphological change in Quaternary mammals of North America. Cambridge University Press, Cambridge.Google Scholar
Barton, D. G., and Wilson, M. V. H. 1999. Microstratigraphic study of meristic variation in an Eocene fish from a 10 000-year varved interval at Horsefly, British Columbia. Canadian Journal of Earth Science 36:20592072.CrossRefGoogle Scholar
Behrensmeyer, A. K. 1991. Terrestrial vertebrate accumulations. Pp. 291335in Allison, P. A. and Briggs, D. E. G., eds. Taphonomy: releasing the data locked in the fossil record. Plenum, New York.Google Scholar
Behrensmeyer, A. K., and Hook, R. W. 1992. Paleoenvironmental contexts and taphonomic modes. Pp. 15136in Behrensmeyer, A. K., Damuth, J. D., DiMichele, W. A., Potts, R., Sues, H.-D., and Wing, S. L., eds. Terrestrial ecosystems through time: evolutionary paleoecology of terrestrial plants and animals. University of Chicago Press, Chicago.Google Scholar
Bell, M. A., Baumgartner, J. V., and Olson, E. C. 1985. Patterns of temporal change in single morphological characters of a Miocene stickleback fish. Paleobiology 11:258271.Google Scholar
Bell, M. A., Sadagursky, M. S., and Baumgartner, J. V. 1987. Utility of lacustrine deposits for the study of variation within fossil samples. Palaios 2:455466.Google Scholar
Bird, J., Riska, B., and Sokal, R. R. 1981. Geographic variation in variability of Pemphigus populicaulis. Systematic Zoology 30:5870.Google Scholar
Bookstein, F. L., Gingerich, P. D., and Kluge, A. G. 1978. Hierarchical linear modeling of the tempo and mode of evolution. Paleobiology 4:120134.Google Scholar
Bush, A., Powell, M. G., Arnold, W. S., Bert, T. M., and Daley, G. M. 2002. Time-averaging, evolution, and morphological variation. Paleobiology 28:925.Google Scholar
Carleton, M. D., and Eshelman, R. E. 1979. A synopsis of fossil grasshopper mice, genus Onychomys, and their relationship to Recent species. University of Michigan Museum of Paleontology, Papers on Paleontology 21:163.Google Scholar
Charlesworth, B., Lande, R., and Slatkin, M. 1982. A Neo-Darwinian commentary on macroevolution. Evolution 36:474498.Google Scholar
Cleveland, W. S. 1979. Robust locally weighted regression and smoothing scatterplots. Journal of the American Statistical Association 74:829836.Google Scholar
Clyde, W. C., and Gingerich, P. D. 1994. Rates of evolution in the dentition of early Eocene Cantius: comparison of size and shape. Paleobiology 20:506522.Google Scholar
Corfield, R. M., and Granlund, A. H. 1988. Speciation and structural evolution in the Paleocene Morozovella lineage (planktic Foraminiferida). Journal of Micropalaeontology 7:5962.Google Scholar
Cronin, T. M. 1985. Speciation and stasis in marine Ostracoda: climatic modulation of evolution. Science 227:6063.Google Scholar
de Deckker, P. 1979. The Middle Pleistocene ostracod fauna of the West Runton Freshwater Bed, Norfolk. Palaeontology 22:293316.Google Scholar
Drooger, C. W., and De Klerk, J. C. 1985. The punctuation in the evolution of Orbitoides in the Campanian of south-west France. Utrecht Micropaleontological Bulletins 33:1132.Google Scholar
Erwin, D. H., and Anstey, R. L. 1995. Speciation in the fossil record. Pp. 1138in Erwin, D. H. and Anstey, R. L., eds. New approaches to speciation in the fossil record. Columbia University Press, New York.Google Scholar
Fermont, W. J. J. 1982. Discocyclinidae from Ein Avedat (Israel). Utrecht Micropaleontological Bulletins 27:1152.Google Scholar
Foote, M., and Cowie, R. H. 1988. Developmental buffering as a mechanism for stasis: evidence from the pulmonate Theba pisana. Evolution 42:369399.Google Scholar
Forsten, A. 1990. Dental size trends in an equid sample from the Sandalja II cave of northwestern Yugoslavia. Paläontologische Zeitschrift 64(1/2):153160.CrossRefGoogle Scholar
Gingerich, P. D. 1983. Rates of evolution: effects of time and temporal scaling. Science 222:159161.Google Scholar
Gingerich, P. D. 2001. Rates of evolution on the time scale of evolutionary process. Genetica 112–113:127144.CrossRefGoogle ScholarPubMed
Gingerich, P. D., and Gunnell, G. F. 1995. Rates of evolution in Paleocene-Eocene mammals of the Clarks Fork Basin, Wyoming, and a comparison with Neogene Siwalik lineages of Pakistan. Palaeogeography, Palaeoclimatology, Palaeoecology 115(1–4):227247.Google Scholar
Goodin, J. T., and Johnson, M. S. 1992. Patterns of morphological covariation in Partula. Systematic Biology 41:292304.Google Scholar
Guilday, J. E. 1982. Dental variation in Microtus xanthognathus, M. chrotorrhinus, and M. pennsylvanicus (Rodentia: Mammalia). Annals of the Carnegie Museum 51:211230.Google Scholar
Guilday, J. E., Martin, P. S., and McGrady, A. D. 1964. New Paris No. 4: a Late Pleistocene cave deposit in Bedford county, Pennsylvania. Bulletin of the National Speleological Society 26:121194.Google Scholar
Guilday, J. E., Parmalee, P. W., and Hamilton, H. W. 1977. The Clarke's Cave bone deposit and the Late Pleistocene paleoecology of the central Appalachian mountains of Virginia. Bulletin of the Carnegie Museum of Natural History 2:186.Google Scholar
Guilday, J. E., Hamilton, H. W., Anderson, E., and Parmalee, P. W. 1978. The Baker Bluff cave deposit, Tennessee, and the late Pleistocene faunal gradient. Bulletin of the Carnegie Museum of Natural History 11:167.Google Scholar
Harris, A. H. 1988. Late Pleistocene and Holocene Microtus (Pitymys) (Rodentia: Cricetidae) in New Mexico. Journal of Vertebrate Paleontology 8:307313.Google Scholar
Hunt, G. 2004. Phenotypic variation in fossil samples: modeling the consequences of time-averaging. Paleobiology 30:426443.Google Scholar
Kidwell, S. M. 1986. Models for fossil concentrations: paleobiological implications. Paleobiology 12:624.Google Scholar
Kidwell, S. M. 1998. Time-averaging in the marine fossil record: overview of strategies and uncertainties. Geobios 30:977995.Google Scholar
Kidwell, S. M. 2001. Preservation of species abundance in marine death assemblages. Science 294:10911094.Google Scholar
Kidwell, S. M. 2002. Time-averaged molluscan death assemblages: palimpsests of richness, snapshots of abundance. Geology 30:803806.Google Scholar
Kidwell, S. M., and Behrensmeyer, A. K. 1993 Summary: estimates of time-averaging. In Kidwell, S. M. and Behrensmeyer, A. K., eds. Taphonomic approaches to time resolution in fossil assemblages. Short Courses in Paleontology 6:301302. Paleontological Society, Knoxville, Tenn.Google Scholar
Kidwell, S. M., and Holland, S. M. 2002. The quality of the fossil record: implications for evolutionary analysis. Annual Review of Ecology and Systematics 33:561588.Google Scholar
Klippel, W. E., and Parmalee, P. W. 1982. Diachronic variation in insectivores from Cheek Bend Cave and environmental change in the Midsouth. Paleobiology 8:447458.Google Scholar
Kowalewski, M. 1996. Time-averaging, overcompleteness and the geological record. Journal of Geology 104:317326.Google Scholar
Kowalewski, M., and Bambach, R. K. 2003. The limits of paleontological resolution. In Harries, P. J., ed. High-resolution approaches in stratigraphic paleontology. Topics in Geobiology 21-1-48. Kluwer Academic, Dordrecht.Google Scholar
Kozlowski, J. K., ed. 1982. Excavation in the Bacho Kiro Cave (Bulgaria). Final Report. Panstwowe Wydawnictwo Naukowe, Warsaw.Google Scholar
Laaglund, H. 1990. Cycloclypeus in the Mediterranean Oligocene. Utrecht Micropaleontological Bulletins 39:1161.Google Scholar
Lazarus, D. 1986. Tempo and mode of morphologic evolution near the origin of the radiolarian lineage Pterocanium prismatium. Paleobiology 12:175189.Google Scholar
Lazarus, D., Scherer, R. P., and Prothero, D. R. 1985. Evolution of the radiolarian species-complex Pterocanium: a preliminary survey. Journal of Paleontology 59:183220.Google Scholar
Lewontin, R. C. 1966. On the measurement of relative variability. Systematic Zoology 15:141142.Google Scholar
Lich, D. K. 1990. Cosomys primus: a case for stasis. Paleobiology 16:384395.Google Scholar
Lieberman, B. S., and Dudgeon, S. 1996. An evaluation of stabilizing selection as a mechanism for stasis. Palaeogeography, Palaeoclimatology, Palaeoecology 127:229238.Google Scholar
MacFadden, B. J. 1986. Fossil horses from “Eohippus” (Hyracotherium) to Equus: scaling, Cope's Law, and the evolution of body size. Paleobiology 12:355369.Google Scholar
MacFadden, B. J. 1989. Dental character variation in paleopopulations and morphospecies of fossil horses and extant analogs. Pp. 128141in Prothero, D. R. and Schoch, R. M., eds. The evolution of perissodactyls. Oxford University Press, New York.Google Scholar
MacLeod, N. 1991. Punctuated anagenesis and the importance of stratigraphy to paleobiology. Paleobiology 17:167188.Google Scholar
Malmgren, B. A., and Kennett, J. A. 1981. Phyletic gradualism in a Late Cenozoic planktonic foraminiferal lineage; DSDP Site 284, southwest Pacific. Paleobiology 7:230240.Google Scholar
Malmgren, B. A., Berggren, W. A., and Lohmann, G. P. 1983. Evidence for puncuated gradualism in the Late Neogene Globorotalia tumida lineage of planktonic foraminifera. Paleobiology 9:377389.Google Scholar
Malmgren, B. A., Kucera, M., and Ekman, G. 1996. Evolutionary changes in supplementary apertural characteristics of the late Neogene Sphaeroidinella dehiscens lineage (planktonic foraminifera). Palaios 11:192206.Google Scholar
Martin, R. E. 1999. Taphonomy: a process approach. Cambridge University Press, Cambridge.Google Scholar
Smith, J. Maynard 1983. The genetics of stasis and punctuation. Annual Review of Genetics 17:1125.Google Scholar
Murphy, M. A., and Berry, W. B. N. 1983. Early Devonian conodont-graptolite collation and correlations with brachiopod and coral zones, central Nevada. American Association of Petroleum Geologists Bulletin 67:371379.Google Scholar
Murphy, M. A., and Springer, K. B. 1989. Morphometric study of the platform elements of Amydrotaxis praejohnsoni N. Sp. (Lower Devonian, conodonts, Nevada). Journal of Paleontology 63:349355.Google Scholar
Nadachowksi, A. 1982. Late Quaternary rodents of Poland with special reference to morphotype dentition analysis of voles. Polska Akademia Nauk, Warsaw.Google Scholar
Nadachowksi, A. 1984. Morphometric variability of dentition of the Late Pleistocene voles (Arvicolidae, Rodentia) from Bacho Kiro Cave (Bulgaria). Acta Zoologica Cracoviensia 27:149176.Google Scholar
Nadachowksi, A. 1985. Biharian voles (Arvicolidae, Rodentia, Mammalia) from Kozi Grzbiet (Central Poland). Acta Zoologica Cracoviensia 29:1328.Google Scholar
Nadachowksi, A. 1991. Systematics, geographic variation, and evolution of snow voles (Chionomys) based on dental characters. Acta Theriologica 36(1–2):145.Google Scholar
Olszewski, T. 1999. Taking advantage of time-averaging. Paleobiology 25:226238.Google Scholar
Palmer, A. R. 1999. Detecting publication bias in meta-analysis: a case study of fluctuating asymmetry and sexual selection. American Naturalist 154:220233.Google Scholar
Palmer, A. R. 2000. Quasireplication and the contract of error: lessons from sex ratios, heritabilities, and fluctuating asymmetry. Annual Review of Ecology and Systematics 31:441480.Google Scholar
Purdue, J. R. 1986. The size of white-tailed deer (Odocoileus virginianus) during the Archaic Period in central Illinois. Pp. 6595in Neusius, S. W., ed. Foraging, collecting, and harvesting: Archaic Period subsistence and settlement in the Eastern Woodlands. Center for Archaeological Investigations, Southern Illinois University at Carbondale, Carbondale.Google Scholar
Rekovets, L., and Nadachowski, A. 1995. Pleistocene voles (Arvicolidae) of the Ukraine. Paleontologia i Evolució 28–29:145245.Google Scholar
Rensberger, J. M., and Barnosky, A. D. 1993. Short-term fluctuations in small mammals of the late Pleistocene from eastern Washington. Pp. 299342in Martin, R. A. and Barnosky, A. D., eds. Morphological change in Quaternary mammals of North America. University of Cambridge Press, Cambridge.Google Scholar
Sokal, R. R., and Rohlf, F. J. 1995. Biometry, 3d ed.W. H. Freeman, New York.Google Scholar
Storch, G. 1975. Eine mittelpleistozäne Nager-Fauna von der Insel Chios, Ägäis (Mammalia: Rodentia). Senckenbergiana Biologica 56:165189.Google Scholar
Travis, J. 1989. The role of optimizing selection in natural populations. Annual Review of Ecology and Systematics 20:279296.Google Scholar
Walker, K. R., and Bambach, R. K. 1971. The significance of fossil assemblages from fine-grained sediments: time-averaged communities. Geological Society of America Abstracts with Programs 3:783784.Google Scholar
Wildenborg, A. F. B. 1991. Evolutionary aspects of the Miogypsinids in the Oligo-Miocene carbonates near Mineo (Sicily). Utrecht Micropaleontological Bulletins 41:5133.Google Scholar
Williamson, P. G. 1981. Palaeontological documentation of speciation in Cenozoic molluscs from Turkana Basin. Nature 293:437443.Google Scholar
Wilson, M. V. H. 1988. Taphonomic processes: information loss and information gain. Geoscience Canada 15:131148.Google Scholar