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Evolutionarily distinct “living fossils” require both lower speciation and lower extinction rates

Published online by Cambridge University Press:  24 November 2016

Dominic J. Bennett ,
Mark D. Sutton  and
Samuel T. Turvey
Dominic J. Bennett
Affiliation:
Department of Earth Sciences and Engineering, Imperial College London, London, U.K., and Institute of Zoology, Zoological Society of London, London, U.K. E-mail: dominic.john.bennett@gmail.com
Mark D. Sutton
Affiliation:
Department of Earth Sciences and Engineering, Imperial College London, London, U.K.
Samuel T. Turvey
Affiliation:
Institute of Zoology, Zoological Society of London, London, U.K.
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Abstract

As a label for a distinct category of life, “living fossil” is controversial. The term has multiple definitions, and it is unclear whether the label can be genuinely used to delimit biodiversity. Even taking a purely phylogenetic perspective in which a proxy for the living fossil is evolutionary distinctness (ED), an inconsistency arises: Does it refer to “dead-end” lineages doomed to extinction or “panchronic” lineages that survive through multiple epochs? Recent tree-growth model studies indicate that speciation rates must have been unequally distributed among species in the past to produce the shape of the tree of life. Although an uneven distribution of speciation rates may create the possibility for a distinct group of living fossil lineages, such a grouping could only be considered genuine if extinction rates also show a consistent pattern, be it indicative of dead-end or panchronic lineages. To determine whether extinction rates also show an unequal distribution, we developed a tree-growth model in which the probability of speciation and extinction is a function of a tip’s ED. We simulated thousands of trees in which the ED function for a tip is randomly and independently determined for speciation and extinction rates. We find that simulations in which the most evolutionarily distinct tips have lower rates of speciation and extinction produce phylogenetic trees closest in shape to empirical trees. This implies that a distinct set of lineages with reduced rates of diversification, indicative of a panchronic definition, is required to create the shape of the tree of life.

Type
Articles
Information
Paleobiology , Volume 43 , Issue 1 , February 2017 , pp. 34 - 48
Copyright
Copyright © 2016 The Paleontological Society. All rights reserved 

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References

Literature Cited

Alfaro, M. E., Santini, F., Brock, C., Alamillo, H., Dornburg, A., Rabosky, D. L., Giorgio, C., and Harmon, L. J.. 2009. Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proceedings of the National Academy of Sciences USA 106:13410–13414.CrossRefGoogle ScholarPubMed
Alroy, J. 1996. Constant extinction, constrained diversification, and uncoordinated stasis in North American mammals. Palaeogeography, Palaeoclimatology and Palaeoecology 127:285–311.Google Scholar
Alroy, J., et al. 2008. Phanerozoic trends in the global diversity of marine invertebrates. Science 321:97–100.Google Scholar
Amemiya, C. T., et al. 2013. The African coelacanth genome provides insights into tetrapod evolution. Nature 496:311–316.Google Scholar
Bennett, D. J. 2016. Project-EDBMM: testing the phylogenetic reality of the living fossil with an EDBMM. https://github.com/DomBennett/Project-EDBMM.Google Scholar
Blum, M., and François, O.. 2006. Which random processes describe the Tree of Life? A large-scale study of phylogenetic tree imbalance. Systematic Biology 55:685–691.Google Scholar
Boettiger, C., and Temple Lang, D.. 2012. treebase: an R package for discovery, access and manipulation of online phylogenies. Methods in Ecology and Evolution 3:1060–1066.Google Scholar
Bortolussi, N., Durand, E., Blum, M., and François, O.. 2006. apTreeshape: Statistical analysis of phylogenetic tree shape. Bioinformatics 22:363–364.Google Scholar
Boyajian, G. E. 1991. Taxon age and selectivity of extinction. Paleobiology 17:49–57.CrossRefGoogle Scholar
Brayard, A., Escarguel, G., Bucher, H., Monnet, C., Brühwiler, T., Goudemand, N., Galfetti, T., and Guex, J.. 2009. Good genes and good luck: ammonoid diversity and the end-Permian mass extinction. Science 325:1118–1121.Google Scholar
Britton, T., Oxelman, B., Vinnersten, A., and Bremer, K.. 2002. Phylogenetic dating with confidence intervals using mean path lengths. Molecular Phylogenetics and Evolution 24:58–65.Google Scholar
Britton, T., Anderson, C. L., Jacquet, D., Lundqvist, S., and Bremer, K.. 2007. Estimating divergence times in large phylogenetic trees. Systematic Biology 56:741–752.Google Scholar
Casane, D., and Laurenti, P.. 2013. Why coelacanths are not “living fossils”: a review of molecular and morphological data. BioEssays 35:332–338.Google Scholar
Cavin, L., and Kemp, A.. 2011. The impact of fossils on the evolutionary distinctiveness and conservation status of the Australian lungfish. Biological Conservation 144:3140–3142.Google Scholar
Colless, D. H. 1982. Review of phylogenetics: the theory and practice of phylogenetic systematics. Systematic Zoology 31:100–104.Google Scholar
Courtillot, V., and Gaudemer, Y.. 1996. Effects of mass extinctions on biodiversity. Nature 381:146–148.Google Scholar
Darwin, C. 1859. On the origin of species by means of natural selection. London: J. Murray.Google Scholar
Eldredge, N., and Stanley, S. M.. 1984. Living fossils. Casebooks in Earth Sciences. Springer, New York.Google Scholar
Ezard, T. H. G., Aze, T., Pearson, P. N., and Purvis, A.. 2011. Interplay between changing climate and species” ecology drives macroevolutionary dynamics. Science 332:349–351.Google Scholar
Ezard, T. H. G., Thomas, G. H., and Purvis, A.. 2013. Inclusion of a near-complete fossil record reveals speciation-related molecular evolution. Methods in Ecology and Evolution 4:745–753.Google Scholar
Forey, P. 1984. The coelacanth as a living fossil. Pp. 166–169 in N. Eldredge and S. M. Stanley, ed. Living fossils. Casebooks in Earth Sciences. Springer, New York.Google Scholar
Global Names Architecture. 2015. Global Names Resolver. http://resolver.globalnames.biodinfo.org, accessed 14 July 2015.Google Scholar
Gould, S. J., and Eldredge, N.. 1993. Punctuated equilibrium comes of age. Nature 366:223–227.Google Scholar
Gould, S. J., Gilinsky, N. L., and German, R. Z.. 1987. Asymmetry of lineages and the direction of evolutionary time. Science 236:1437–1441.Google Scholar
Hagen, O., Hartmann, K., Steel, M., and Stadler, T.. 2015. Age-dependent speciation can explain the shape of empirical phylogenies. Systematic Biology 64:432–440.Google Scholar
Hay, J. M., Subramanian, S., Millar, C. D., Mohandesan, E., and Lambert, D. M.. 2008. Rapid molecular evolution in a living fossil. Trends in Genetics 24:106–109.Google Scholar
Helmus, M. R., Bland, T. J., Williams, C. K., and Ives, A. R.. 2007. Phylogenetic measures of biodiversity. American Naturalist 169(3):E68–E83.Google Scholar
Isaac, N. J. B., Turvey, S. T., Collen, B., Waterman, C., and Baillie, J. E. M.. 2007. Mammals on the EDGE: conservation priorities based on threat and phylogeny. PLoS ONE 2:e296.Google Scholar
Liow, L. H. 2004. A test of Simpson’s “Rule of the Survival of the Relatively Unspecialized” using fossil crinoids. American Naturalist 164:431–443.Google Scholar
Liow, L. H. 2006. Do deviants live longer? Morphology and longevity in trachyleberidid ostracodes. Paleobiology 32:55–69.Google Scholar
Liow, L. H., and Finarelli, J. A.. 2014. A dynamic global equilibrium in carnivoran diversification over 20 million years. Proceedings of Royal Society of London B 281:20132312.Google Scholar
Manceau, M., Lambert, A., and Morlon, H.. 2015. Phylogenies support out-of-equilibrium models of biodiversity. Ecology Letters 18:347–356.Google Scholar
Miller, A. I., and Sepkoski, J. J.. 1988. Modeling bivalve diversification: the effect of interaction on a macroevolutionary system. Paleobiology 14:364–369.Google Scholar
Mooers, A., and Heard, S.. 1997. Inferring evolutionary process from phylogenetic tree shape. Quarterly Review of Biology 72:31–54.Google Scholar
Nagalingum, N. S., Marshall, C. R., Quental, T. B., Rai, H. S., Little, D. P., and Mathews, S.. 2011. Recent synchronous radiation of a living fossil. Science 334:796–799.Google Scholar
Paradis, E., Claude, J., and Strimmer, K.. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290.Google Scholar
Piel, W. H., Donoghue, M., and Sanderson, M.. 2002. TreeBASE: a database of phylogenetic information. Pp. 41–47 in To the Interoperable “Catalog of Life” with Partners, Species 2000 Asia Oceania. Tsukuba, Japan.Google Scholar
Purvis, A., Fritz, S. A., Rodríguez, J., Harvey, P. H., and Grenyer, R.. 2011. The shape of mammalian phylogeny: patterns, processes and scales. Philosophical Transactions of the Royal Society of London B 366:2462–2477.Google Scholar
Pybus, O. G., and Harvey, P. H.. 2000. Testing macro-evolutionary models using incomplete molecular phylogenies. Proceedings of the Royal Society of London B 267:2267–2272.Google Scholar
Quental, T. B., and Marshall, C. R.. 2013. How the Red Queen drives terrestrial mammals to extinction. Science 341:290–292.Google Scholar
Rabosky, D. L., and Goldberg, E. E.. 2015. Model inadequacy and mistaken inferences of trait-dependent speciation. Systematic Biology 64:340–355.CrossRefGoogle ScholarPubMed
Raup, D. M. 1985. Mathematical models of cladogenesis. Paleobiology 11:42–52.Google Scholar
Redding, D. W., DeWolff, C. V., and Mooers, A. Ø.. 2010. Evolutionary distinctiveness, threat status, and ecological oddity in primates. Conservation Biology 24:1052–1058.Google Scholar
Roy, K. 1996. The roles of mass extinction and biotic interaction in large-scale replacements: a reexamination using the fossil record of stromboidean gastropods. Paleobiology 22:436–452.Google Scholar
Royer, D. L., Hickey, L. J., and Wing, S. L.. 2003. Ecological conservatism in the “living fossil” Ginkgo. Paleobiology 29:84–104.Google Scholar
Rudkin, D. M., Young, G. A., and Nowlan, G. S.. 2008. The oldest horseshoe crab: a new xiphosurid from Late Ordovician Konservat-Lagerstätten deposits, Manitoba, Canada. Palaeontology 51:1–9.Google Scholar
Sackin, M. J. 1972. “Good” and “bad” phenograms. Systematic Zoology 21:225–226.Google Scholar
Sanderson, M. J. 2002. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Molecular Biology and Evolution 19:101–109.Google Scholar
Schluter, D. 2000. The ecology of adaptive radiation. Oxford University Press, Oxford.Google Scholar
Schopf, T. J. M. 1984. Rates of evolution and the notion of “living fossils.”. Annual Review of Earth Planetary Science 12:245–292.Google Scholar
Simpson, G.G. 1944. Tempo and mode in evolution. Columbia University Press, New York.Google Scholar
Sepkoski, J. J. Jr. 1978. A kinetic model of Phanerozoic taxonomic diversity I. Analysis of marine orders. Paleobiology 4:223–251.Google Scholar
Sepkoski, J. J. Jr. 1979. A kinetic model of Phanerozoic taxonomic diversity II. Early Phanerozoic families and multiple equilibria. Paleobiology 5:222–251.Google Scholar
Sepkoski, J. J. Jr. 1984. A kinetic model of Phanerozoic taxonomic diversity III. Post-Paleozoic families and mass extinctions. Paleobiology 10:246–267.Google Scholar
Sepkoski, J. J. Jr., McKinney, F. K., and Lidgard, S.. 2000. Competitive displacement among post-Paleozoic cyclostome and cheilostome bryozoans. Paleobiology 26:7–18.Google Scholar
Van Valen, L. 1973. A new evolutionary law. Evolutionary Theory 1:1–30.Google Scholar
Venditti, C., and Pagel, M.. 2010. Speciation as an active force in promoting genetic evolution. Trends in Ecology and Evolution 25:14–20.Google Scholar
Venkatesh, B., et al. 2014. Elephant shark genome provides unique insights into gnathostome evolution. Nature 505:174–179.Google Scholar
Voje, K. L., Holen, Ø. H., Liow, L. H., and Stenseth, N. C.. 2015. The role of biotic forces in driving macroevolution: beyond the Red Queen. Proceedings of the Royal Society of London B 282:1–9.Google Scholar
Wagner, P. J., and Estabrook, G. F.. 2014. Trait-based diversification shifts reflect differential extinction among fossil taxa. Proceedings of the National Academy of Sciences USA 111:16419–16424.Google Scholar
Wiltshire, J., Huffer, F. W., and Parker, W. C.. 2014. A general class of test statistics for Van Valen’s Red Queen hypothesis. Journal of Applied Statistics 41:2028–2043.Google Scholar
Yoshida, K. 2002. Long survival of “living fossils” with low taxonomic diversities in an evolving food web. Paleobiology 28:464–473.Google Scholar
Yule, G. U. 1925. A mathematical theory of evolution, based on the conclusions of Dr. J. C. Willis, F.R.S. Philosophical Transactions of the Royal Society of London B 213:21–87.Google Scholar