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Phylogeny, ancestors, and anagenesis in the hominin fossil record

Published online by Cambridge University Press:  01 May 2019

Caroline Parins-Fukuchi Open the ORCID record for Caroline Parins-Fukuchi [Opens in a new window] ,
Elliot Greiner ,
Laura M. MacLatchy  and
Daniel C. Fisher
Caroline Parins-Fukuchi
Affiliation:
Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48109, U.S.A. Email: cfukuchi@umich.edu.
Elliot Greiner
Affiliation:
Department of Anthropology, University of Michigan, Ann Arbor, Michigan 48109, U.S.A.
Laura M. MacLatchy
Affiliation:
Department of Anthropology and Museum of Paleontology, University of Michigan, Ann Arbor, Michigan 48109, U.S.A.
Daniel C. Fisher
Affiliation:
Museum of Paleontology, Department of Earth and Environmental Sciences, and Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48109, U.S.A.
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Abstract

Probabilistic approaches to phylogenetic inference have recently gained traction in paleontological studies. Because they directly model processes of evolutionary change, probabilistic methods facilitate a deeper assessment of variability in evolutionary patterns by weighing evidence for competing models. Although phylogenetic methods used in paleontological studies have generally assumed that evolution proceeds by splitting cladogenesis, extensions to previous models help explore the potential for morphological and temporal data to provide differential support for contrasting modes of evolutionary divergence. Recent methodological developments have integrated ancestral relationships into probabilistic phylogenetic methods. These new approaches rely on parameter-rich models and sophisticated inferential methods, potentially obscuring the respective contributions of data and models. In this study, we describe a simple likelihoodist approach that combines probabilistic models of morphological evolution and fossil preservation to reconstruct both cladogenetic and anagenetic relationships. By applying this approach to a data set of fossil hominins, we demonstrate the capability of existing models to unveil evidence for anagenesis presented by morphological and temporal data. This evidence was previously recognized by qualitative assessments, but largely ignored by quantitative phylogenetic analyses. For example, we find support for directly ancestral relationships in multiple lineages: Sahelanthropus is ancestral to later hominins; Australopithecus anamensis is ancestral to Australopithecus afarensis; Australopithecus garhi is ancestral to Homo; Homo antecessor is ancestral to Homo heidelbergensis, which in turn is ancestral to both Homo sapiens and Homo neanderthalensis. By accommodating direct ancestry in phylogenetics, quantitative results align more closely with previous qualitative expectations.

Type
Articles
Information
Paleobiology , Volume 45 , Issue 2 , May 2019 , pp. 378 - 393
Copyright
Copyright © The Paleontological Society. All rights reserved 2019 

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Footnotes

Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.6d2h8bp; and the GitHub Digital Repository: https://github.com/carolinetomo/mandos and https://github.com/carolinetomo/hominin_anagenesis

References

Literature Cited

Asfaw, B., White, T., Lovejoy, O., Latimer, B., Simpson, S., and Suwa, G.. 1999. Australopithecus garhi: a new species of early hominid from Ethiopia. Science 284:629–635.Google Scholar
Aze, T., Ezard, T. H. G., Purvis, A., Coxall, H. K., Stewart, D. R. M., Wade, B. S., and Pearson, P. N.. 2011. A phylogeny of Cenozoic macroperforate planktonic foraminifera from fossil data. Biological Reviews 86:900–927.Google Scholar
Aze, T., Ezard, T. H. G., Purvis, A., Coxall, H. K., Stewart, D. R. M., Wade, B. S., and Pearson, P. N.. 2013. Identifying anagenesis and cladogenesis in the fossil record. Proceedings of the National Academy of Sciences USA 110:E2946–E2946.Google Scholar
Bapst, D. W. 2013. A stochastic rate-calibrated method for time-scaling phylogenies of fossil taxa. Methods in Ecology and Evolution 4:724–733.Google Scholar
Bapst, D. W., and Hopkins, M. J.. 2017. Comparing cal3 and other a posteriori time-scaling approaches in a case study with the pterocephaliid trilobites. Paleobiology 43:49–67.Google Scholar
Bermúdez de Castro, J. M., Arsuaga, J. L., Carbonell, E., Rosas, A., Martínez, I., and Mosquera, M.. 1997. A hominid from the lower Pleistocene of Atapuerca, Spain: possible ancestor to Neandertals and modern humans. Science 276:1392–1395.Google Scholar
Brown, J. W., Parins-Fukuchi, C., Stull, G. W., Vargas, O. M., and Smith, S. A.. 2017. Bayesian and likelihood phylogenetic reconstructions of morphological traits are not discordant when taking uncertainty into consideration: a comment on Puttick et al. Proceedings of the Royal Society of London B 284:20170986.Google Scholar
Brunet, M., Guy, F., Pilbeam, D., Mackaye, H. T., Likius, A., Ahounta, D., Beauvilain, A., Blondel, C., Bocherens, H., Boisserie, J.-R., De Bonis, L., Coppens, Y., Dejax, J., Denys, C., Duringer, P., Eisenmann, V., Fanone, G., Fronty, P., Geraads, D., Lehmann, T., Lihoreau, F., Louchart, A., Mahamat, A., Merceron, G., Mouchelin, G., Otero, O., Campomanes, P. P., De Leon, M. P., Rage, J.-C., Sapanet, M., Schuster, M., Sudre, J., Tassy, P., Valentin, X., Vignaud, P., Viriot, L., Zazzo, A., and Zollikofer, C.. 2002. A new hominid from the Upper Miocene of Chad, Central Africa. Nature 418:145–151.Google Scholar
Buck, L. T., and Stringer, C. B.. 2014. Homo heidelbergensis. Current Biology 24:R214–R215.Google Scholar
Chamberlain, A., and Wood, B.. 1987. Early hominid phylogeny. Journal of Human Evolution 16:119–133.Google Scholar
Collard, M., and Wood, B.. 2000. How reliable are human phylogenetic hypotheses? Proceedings of the National Academy of Sciences USA 97:5003–5006.Google Scholar
Darwin, C. 1871. The descent of man, and selection in relation to sex, 1st ed. John Murray, London.Google Scholar
Delson, E., Eldredge, N., and Tattersall, I.. 1977. Reconstruction of hominid phylogeny: a testable framework based on cladistic analysis. Journal of Human Evolution 6:263–278.Google Scholar
Dembo, M., Matzke, N. J., Mooers, A. Ø., and Collard, M.. 2015. Bayesian analysis of a morphological supermatrix sheds light on controversial fossil hominin relationships. Proceedings of the Royal Society of London B 282:20150943.Google Scholar
Dembo, M., Radovčić, D., Garvin, H. M., Laird, M. F., Schroeder, L., Scott, J. E., Brophy, J., Ackermann, R. R., Musiba, C. M., de Ruiter, D. J., Mooers, A. Ø., and Collard, M.. 2016. The evolutionary relationships and age of Homo naledi: an assessment using dated Bayesian phylogenetic methods. Journal of Human Evolution 97:17–26.Google Scholar
Felsenstein, J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution 17:368–376.Google Scholar
Felsenstein, J. 1988. Phylogenies and quantitative characters. Annual Review of Ecology and Systematics 19:445–471.Google Scholar
Fisher, D. C. 1994. Stratocladistics: morphological and temporal patterns and their relation to phylogenetic process. Pp. 133–171 in Grande, L. and Rieppel, O., eds. Interpreting the hierarchy of nature: from systematic patterns to evolutionary process theories. Academic Press, New York.Google Scholar
Fisher, D. C. 2008. Stratocladistics: integrating temporal data and character data in phylogenetic inference. Annual Review of Ecology, Evolution, and Systematics 39:365–385.Google Scholar
Foote, M. 1997. Estimating taxonomic durations and preservation probability. Paleobiology 23:278–300.Google Scholar
Foote, M. 1996. On the probability of ancestors in the fossil record. Paleobiology 22:141–151.Google Scholar
Foote, M. 2001. Inferring temporal patterns of preservation, origination, and extinction from taxonomic survivorship analysis. Paleobiology 27:602–630.Google Scholar
Fox, D. L., Fisher, D. C., and Leighton, L. R.. 1999. Reconstructing phylogeny with and without temporal data. Science 284:1816–1819.Google Scholar
Futuyma, D. J. 1987. On the role of species in anagenesis. American Naturalist 130:465–473.Google Scholar
Gavryushkina, A., Welch, D., Stadler, T., and Drummond, A. J.. 2014. Bayesian inference of sampled ancestor trees for epidemiology and fossil calibration. PLoS Computational Biology 10:e1003919.Google Scholar
Gavryushkina, A., Heath, T. A., Ksepka, D. T., Stadler, T., Welch, D., and Drummond, A. J.. 2017. Bayesian total-evidence dating reveals the recent crown radiation of penguins. Systematic Biology 66:57–73.Google Scholar
Gingerich, P. D. 1979. Stratophenetic approach to phylogeny reconstruction in vertebrate paleontology. Pp. 41–77 in Cracraft, J. and Eldredge, N., eds. Phylogenetic analysis and paleontology. Columbia University Press, New York.Google Scholar
Gingerich, P. D. 1985. Species in the fossil record: concepts, trends, and transitions. Paleobiology 11:27–41.Google Scholar
Goloboff, P. A., Mattoni, C. I., and Quinteros, A. S.. 2006. Continuous characters analyzed as such. Cladistics 22:589–601.Google Scholar
Goloboff, P. A., Torres, A., and Arias, J. S.. 2017. Weighted parsimony outperforms other methods of phylogenetic inference under models appropriate for morphology. Cladistics 281:20141278.Google Scholar
Gould, S. J. 1980. Is a new and general theory of evolution emerging? Paleobiology 6:119–130.Google Scholar
Gould, S. J., and Eldredge, N.. 1977. Punctuated equilibria: the tempo and mode of evolution reconsidered. Paleobiology 3:115–151.Google Scholar
Guy, F., Lieberman, D. E., Pilbeam, D., de Leon, M. P., Likius, A., Mackaye, H. T., Vignaud, P., Zollikofer, C., and Brunet, M.. 2005. Morphological affinities of the Sahelanthropus tchadensis (Late Miocene hominid from Chad) cranium. Proceedings of the National Academy of Sciences USA 102:18836–18841.Google Scholar
Heath, T. A., Huelsenbeck, J. P., and Stadler, T.. 2014. The fossilized birth-death process for coherent calibration of divergence-time estimates. Proceedings of the National Academy of Sciences USA 111:E2957–66.Google Scholar
Huelsenbeck, J. P., and Rannala, B.. 1997. Maximum likelihood estimation of phylogeny using stratigraphic data. Paleobiology 23:174–180.Google Scholar
Irish, J. D., Guatelli-Steinberg, D., Legge, S. S., de Ruiter, D. J., and Berger, L. R.. 2013. Dental morphology and the phylogenetic “place” of Australopithecus sediba. Science 340:1233062–1233062.Google Scholar
Jones, E., Oliphant, T., and Peterson, P.. 2001. SciPy: open source scientific tools for Python. http://www.scipy.org, accessed 23 September 2018.Google Scholar
Kimbel, W. H., Lockwood, C. A., Ward, C. V., Leakey, M. G., Rak, Y., and Johanson, D. C.. 2006. Was Australopithecus anamensis ancestral to A. afarensis? A case of anagenesis in the hominin fossil record. Journal of Human Evolution 51:134–152.Google Scholar
Leakey, M. G., Feibel, C. S., McDougall, I., and Walker, A.. 1995. New four-million-year-old hominid species from Kanapoi and Allia Bay, Kenya. Nature 376:565–571.Google Scholar
Levinton, J. S. 2001. Genetics, paleontology, and macroevolution. Cambridge University Press, Cambridge.Google Scholar
Levinton, J. S., and Chris, M. S.. 1980. A critique of the punctuated equilibria model and implications for the detection of speciation in the fossil record. Systematic Biology 29:130–142.Google Scholar
Lewis, P. O. 2001. A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology 50:913–925.Google Scholar
Lewis, P. O., Chen, M.-H., Kuo, L., Lewis, L. A., Fučíková, K., Neupane, S., Wang, Y.-B., and Shi, D.. 2016. Estimating Bayesian phylogenetic information content. Systematic Biology 65:1009–1023.Google Scholar
Luo, A., Duchene, D., Zhang, C., Zhu, C. D., and Ho, S.. 2018. A simulation-based evaluation of total-evidence dating under the fossilized birth-death process. BioRxiv. doi: 10.1101/436303.Google Scholar
MacLatchy, L. M., Desilva, J., Sanders, W. J., and Wood, B.. 2010. Hominini. Pp. 471–542 in Sanders, W. J. and Werdelin, L., eds. Cenozoic mammals of Africa. University of California Press, Oakland.Google Scholar
MacLeod, N. 1991. Punctuated anagenesis and the importance of stratigraphy to paleobiology. Paleobiology 17:167–188.Google Scholar
Mounier, A., Marchal, F., and Condemi, S.. 2009. Is Homo heidelbergensis a distinct species? New insight on the Mauer mandible. Journal of Human Evolution 56:219–246.Google Scholar
Parins-Fukuchi, C. 2017. Use of continuous traits can improve morphological phylogenetics. Systematic Biology 67:328–339.Google Scholar
Puttick, M. N., O'Reilly, J. E., Tanner, A. R., Fleming, J. F., Clark, J., Holloway, L., Lozano-Fernandez, J., Parry, L. A., Tarver, J. E., Pisani, D., and Donoghue, P. C. J.. 2017. Uncertain-tree: discriminating among competing approaches to the phylogenetic analysis of phenotype data. Proceedings of the Royal Society of London B 284:20162290.Google Scholar
Pyron, R. A. 2011. Divergence time estimation using fossils as terminal taxa and the origins of Lissamphibia. Systematic Biology 60:466–481.Google Scholar
Rightmire, G. P. 1998. Human evolution in the Middle Pleistocene: the role of Homo heidelbergensis. Evolutionary Anthropology 6:218–227.Google Scholar
Rosas, A., and Bermúdez De Castro, J. M.. 1998. The Mauer mandible and the evolutionary significance of Homo heidelbergensis. Geobios 31:687–697.Google Scholar
Simpson, G. G. 1944. Tempo and mode in evolution. Columbia University Press, New York.Google Scholar
Smith, A. B. 1994. Systematics and the fossil record. Blackwell Science, Oxford.Google Scholar
Smith, A. B. 2000. Stratigraphy in phylogeny reconstruction. Journal of Paleontology 74:763–766.Google Scholar
Soul, L. C., and Friedman, M.. 2017. Bias in phylogenetic measurements of extinction and a case study of end-Permian tetrapods. Palaeontology 60:169–185.Google Scholar
Stadler, T. 2010. Sampling-through-time in birth–death trees. Journal of Theoretical Biology 267:396–404.Google Scholar
Stadler, T., Gavryushkina, A., Warnock, R. C. M., Drummond, A. J., and Heath, T. A.. 2018. The fossilized birth-death model for the analysis of stratigraphic range data under different speciation concepts. Journal of Theoretical Biology 447:41–55.Google Scholar
Stanley, S. M. 1998. Macroevolution: pattern and process, 2nd ed. Johns Hopkins University Press, Baltimore, Md.Google Scholar
Strait, D. S. 1999. Cladistics and early hominid phylogeny. Science 285:1209.Google Scholar
Strait, D. S., Grine, F. E., and Moniz, M. A.. 1997. A reappraisal of early hominid phylogeny. Journal of Human Evolution 32:17–82.Google Scholar
Stringer, C. 2012. The status of Homo heidelbergensis (Schoetensack 1908). Evolutionary Anthropology 21:101–107.Google Scholar
Strotz, L. C., and Allen, A. P.. 2013. Assessing the role of cladogenesis in macroevolution by integrating fossil and molecular evidence. Proceedings of the National Academy of Sciences USA 110:2904–2909.Google Scholar
Wagner, P. J. 1998. A likelihood approach for evaluating estimates of phylogenetic relationships among fossil taxa. Paleobiology 24:430–449.Google Scholar
Ward, C. V., Leakey, M. G., and Walker, A.. 2001. Morphology of Australopithecus anamensis from Kanapoi and Allia Bay, Kenya. Journal of Human Evolution 41:255–368.Google Scholar
White, T. 2003. Paleoanthropology. Early hominids—diversity or distortion? Science 299:1994–1997.Google Scholar
Wright, A. M., and Hillis, D. M.. 2014. Bayesian analysis using a simple likelihood model outperforms parsimony for estimation of phylogeny from discrete morphological data. PLoS ONE 9:e109210.Google Scholar
Yang, Z., and Zhu, T.. 2018. Bayesian selection of misspecified models is overconfident and may cause spurious posterior probabilities for phylogenetic trees. Proceedings of the National Academy of Sciences USA 115:1854–1859.Google Scholar
Yang, Z., Kumar, S., and Nei, M.. 1995. A new method of inference of ancestral nucleotide and amino acid sequences. Genetics 141:1641–1650.Google Scholar
Zhang, C., Stadler, T., Klopfstein, S., Heath, T. A., and Ronquist, F.. 2016. Total-evidence dating under the fossilized birth-death process. Systematic Biology 65:228–249.Google Scholar
Zollikofer, C. P. E., Ponce de León, M. S., Lieberman, D. E., Guy, F., Pilbeam, D., Likius, A., Mackaye, H. T., Vignaud, P., and Brunet, M.. 2005. Virtual cranial reconstruction of Sahelanthropus tchadensis. Nature 434:755–759.Google Scholar