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Detecting Trait-Dependent Diversification Under Diversification Slowdowns

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Abstract

Testing whether a certain biological trait significantly affects clade diversification is central to macroevolutionary research. To this end, many scientists use constant-rate estimators (CR estimators) of diversification. However, it has never been examined whether these estimators report meaningful relationships between traits and diversification even when the diversification itself decelerates over time. In this study, I simulate trait-driven diversification concurrently with diversification slowdowns. Then, I test whether CR estimators manage to uncover the simulated relationships. Results suggest that CR estimators are robust against violation of rate constancy and successfully detect trait-dependent diversification in spite of diversification declines. Interestingly, correct results were recovered whether clade age correlated with clade diversity or not. Further comparison of CR estimators with QuaSSE suggested that QuaSSE performs better under constant diversification, but tends to report spuriously significant outcomes when diversification decelerates (=elevated Type I error). Given that diversification slowdowns have been recently reported for a wide range of taxa, these findings may be of particular relevance for future diversification studies.

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References

  • Alfaro, M. E., Santini, F., Brock, C., Alamillo, H., Dornburg, A., Rabosky, D. L., et al. (2009). Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proceedings of the National Academy of Sciences of the United States of America, 106, 13410–13414.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Alroy, J. (2000). New methods for quantifying macroevolutionary patterns and processes. Paleobiology, 26, 707–733.

    Article  Google Scholar 

  • Blomberg, S. P., Garland, T., & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution, 57, 717–745.

    Article  PubMed  Google Scholar 

  • Blum, M. G. B., & Francois, O. (2006). Which random processes describe the tree of life? A large-scale study of phylogenetic tree imbalance. Systematic Biology, 55, 685–691.

    Article  PubMed  Google Scholar 

  • Bokma, F. (2008a). Bayesian estimation of speciation and extinction probabilities from (in)complete phylogenies. Evolution, 62, 2441–2445.

    Article  PubMed  Google Scholar 

  • Bokma, F. (2008b). Detection of punctuated equilibrium by Bayesian estimation of speciation and extinction rates, ancestral character states, and rates of anagenetic and cladogenetic evolution on a molecular phylogeny. Evolution, 62, 2718–2726.

    Article  PubMed  Google Scholar 

  • Bortolussi, N., Durand, E., Blum, M., & Francois, O. (2006). apTreeshape: Statistical analysis of phylogenetic tree shape. Bioinformatics, 22, 363–364.

    Article  CAS  PubMed  Google Scholar 

  • Butler, M. A., & King, A. A. (2004). Phylogenetic comparative analysis: A modeling approach for adaptive evolution. American Naturalist, 164, 683–695.

    Article  Google Scholar 

  • Davies, T. J., Barraclough, T. G., Chase, M. W., Soltis, P. S., Soltis, D. E., & Savolainen, V. (2004). Darwin’s abominable mystery: Insights from a supertree of the angiosperms. Proceedings of the National Academy of Sciences of the United States of America, 101, 1904–1909.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Etienne, R. S., Haegeman, B., Stadler, T., Aze, T., Pearson, P. N., Purvis, A., et al. (2012). Diversity-dependence brings molecular phylogenies closer to agreement with the fossil record. Proceedings of the Royal Society B Biological Sciences, 279, 1300–1309.

    Article  PubMed Central  Google Scholar 

  • Felsenstein, J. (1985). Phylogenies and the comparative method. American Naturalist, 125, 1–15.

    Article  Google Scholar 

  • FitzJohn, R. G. (2010). Quantitative traits and diversification. Systematic Biology, 59, 619–633.

    Article  PubMed  Google Scholar 

  • FitzJohn, R. G. (2012). Diversitree: Comparative phylogenetic analyses of diversification in R. Methods in Ecology and Evolution, 3, 1084–1092.

    Article  Google Scholar 

  • Foote, M. (2000). Origination and extinction components of taxonomic diversity: General problems. Paleobiology, 26, 74–102.

    Article  Google Scholar 

  • Freckleton, R. P., Harvey, P. H., & Pagel, M. (2002). Phylogenetic analysis and comparative data: A test and review of evidence. American Naturalist, 160, 712–726.

    Article  CAS  PubMed  Google Scholar 

  • Gittleman, J. L., & Kot, M. (1990). Adaptation—statistics and a null model for estimating phylogenetic effects. Systematic Zoology, 39, 227–241.

    Article  Google Scholar 

  • Glor, R. E. (2010). Phylogenetic insights on adaptive radiation. Annual Review of Ecology Evolution and Systematics, 41, 251–270.

    Article  Google Scholar 

  • Good-Avila, S. V., Souza, V., Gaut, B. S., & Eguiarte, L. E. (2006). Timing and rate of speciation in Agave (Agavaceae). Proceedings of the National Academy of Sciences of the United States of America, 103, 9124–9129.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E., & Challenger, W. (2008). GEIGER: Investigating evolutionary radiations. Bioinformatics, 24, 129–131.

    Article  CAS  PubMed  Google Scholar 

  • Hohna, S., Stadler, T., Ronquist, F., & Britton, T. (2011). Inferring speciation and extinction rates under different sampling schemes. Molecular Biology and Evolution, 28, 2577–2589.

    Article  PubMed  Google Scholar 

  • Hunt, T., Bergsten, J., Levkanicova, Z., Papadopoulou, A., John, O. S., Wild, R., et al. (2007). A comprehensive phylogeny of beetles reveals the evolutionary origins of a superradiation. Science, 318, 1913–1916.

    Article  CAS  PubMed  Google Scholar 

  • Hutchinson, G. E. (1959). Homage to Santa Rosalia or why are there so many kinds of animals. American Naturalist, 93, 145–159.

    Article  Google Scholar 

  • Ingram, T. (2011). Speciation along a depth gradient in a marine adaptive radiation. Proceedings of the Royal Society B Biological Sciences, 278, 613–618.

    Article  PubMed Central  Google Scholar 

  • Jablonski, D. (2008). Species selection: Theory and data. Annual Review of Ecology Evolution and Systematics, 39, 501–524.

    Article  Google Scholar 

  • Jansson, R., & Davies, T. J. (2008). Global variation in diversification rates of flowering plants: Energy vs. climate change. Ecology Letters, 11, 173–183.

    Article  PubMed  Google Scholar 

  • Klak, C., Reeves, G., & Hedderson, T. (2004). Unmatched tempo of evolution in Southern African semi-desert ice plants. Nature, 427, 63–65.

    Article  CAS  PubMed  Google Scholar 

  • Maddison, W. P. (2006). Confounding asymmetries in evolutionary diversification and character change. Evolution, 60, 1743–1746.

    Article  PubMed  Google Scholar 

  • Maddison, W. P., Midford, P. E., & Otto, S. P. (2007). Estimating a binary character’s effect on speciation and extinction. Systematic Biology, 56, 701–710.

    Article  PubMed  Google Scholar 

  • Magallon, S., & Sanderson, M. J. (2001). Absolute diversification rates in angiosperm clades. Evolution, 55, 1762–1780.

    Article  CAS  PubMed  Google Scholar 

  • McPeek, M. A. (2008). The ecological dynamics of clade diversification and community assembly. American Naturalist, 172, 270–284.

    Article  Google Scholar 

  • Mittelbach, G. G., Schemske, D. W., Cornell, H. V., Allen, A. P., Brown, J. M., Bush, M. B., et al. (2007). Evolution and the latitudinal diversity gradient: Speciation, extinction and biogeography. Ecology Letters, 10, 315–331.

    Article  PubMed  Google Scholar 

  • Moore, B. R., & Donoghue, M. J. (2009). A Bayesian approach for evaluating the impact of historical events on rates of diversification. Proceedings of the National Academy of Sciences of the United States of America, 106, 4307–4312.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Morlon, H., Potts, M. D., & Plotkin, J. B. (2010). Inferring the dynamics of diversification: A coalescent approach. PLoS Biology, 89, e1000493.

    Article  Google Scholar 

  • Nee, S. (2006). Birth-death models in macroevolution. Annual Review of Ecology Evolution and Systematics, 2006(37), 1–17.

    Article  Google Scholar 

  • Nee, S., May, R. M., & Harvey, P. H. (1994). The reconstructed evolutionary process. Philosophical Transactions of the Royal Society B Biological Sciences, 344, 305–311.

    Article  CAS  Google Scholar 

  • Nylin, S., & Wahlberg, N. (2008). Does plasticity drive speciation? Host-plant shifts and diversification in nymphaline butterflies (Lepidoptera: Nymphalidae) during the tertiary. Biological Journal of the Linnean Society, 94, 115–130.

    Article  Google Scholar 

  • Paradis, E. (2004). Can extinction rates be estimated without fossils? Journal of Theoretical Biology, 229, 19–30.

    Article  PubMed  Google Scholar 

  • Paradis, E. (2005). Statistical analysis of diversification with species traits. Evolution, 59, 1–12.

    Article  PubMed  Google Scholar 

  • Paradis, E. (2008). Asymmetries in phylogenetic diversification and character change can be untangled. Evolution, 62, 241–247.

    PubMed  Google Scholar 

  • Paradis, E., Claude, J., & Strimmer, K. (2004). APE: Analyses of phylogenetics and evolution in R language. Bioinformatics, 20, 289–290.

    Article  CAS  PubMed  Google Scholar 

  • Pennell, M. W., Sarver, B. A. J., & Harmon, L. J. (2012). Trees of unusual size: Biased inference of early bursts from large molecular phylogenies. PLoS ONE, 7, e43348.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Phillimore, A. B., & Price, T. D. (2008). Density-dependent cladogenesis in birds. PLoS Biology, 6, e0071.

    Article  Google Scholar 

  • Pybus, O. G., & Harvey, P. H. (2000). Testing macro-evolutionary models using incomplete molecular phylogenies. Proceedings of the Royal Society B Biological Sciences, 267, 2267–2272.

    Article  CAS  PubMed Central  Google Scholar 

  • R Development Core Team. (2012). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

    Google Scholar 

  • Rabosky, D. L. (2006). Likelihood methods for detecting temporal shifts in diversification rates. Evolution, 60, 1152–1164.

    Article  PubMed  Google Scholar 

  • Rabosky, D. L. (2009a). Ecological limits and diversification rate: Alternative paradigms to explain the variation in species richness among clades and regions. Ecology Letters, 12, 735–743.

    Article  PubMed  Google Scholar 

  • Rabosky, D. L. (2009b). Ecological limits on clade diversification in higher taxa. American Naturalist, 173, 662–674.

    Article  PubMed  Google Scholar 

  • Rabosky, D. L. (2010a). Extinction rates should not be estimated from molecular phylogenies. Evolution, 64, 1816–1824.

    Article  PubMed  Google Scholar 

  • Rabosky, D. L. (2010b). Primary controls on species richness in higher taxa. Systematic Biology, 59, 634–645.

    Article  PubMed  Google Scholar 

  • Rabosky, D. L., & Adams, D. C. (2012). Rates of morphological evolution are correlated with species richness in salamanders. Evolution, 66, 1807–1818.

    Article  PubMed  Google Scholar 

  • Rabosky, D. L., & Lovette, I. J. (2008). Density-dependent diversification in North American wood warblers. Proceedings of the Royal Society B Biological Sciences, 275, 2363–2371.

    Article  PubMed Central  Google Scholar 

  • Rabosky, D. L., Slater, G. J., & Alfaro, M. E. (2012). Clade age and species richness are decoupled across the eukaryotic tree of life. PLoS Biology, 10, e1001381.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Raup, D. M. (1985). Mathematical models of cladogenesis. Paleobiology, 11, 42–52.

    Google Scholar 

  • Ricklefs, R. E. (2006). Global variation in the diversification rate of passerine birds. Ecology, 87, 2468–2478.

    Article  PubMed  Google Scholar 

  • Ricklefs, R. E. (2007). Estimating diversification rates from phylogenetic information. Trends in Ecology & Evolution, 22, 601–610.

    Article  Google Scholar 

  • Sanderson, M. J., & Donoghue, M. J. (1996). Reconstructing shifts in diversification rates on phylogenetic trees. Trends in Ecology & Evolution, 11, 15–20.

    Article  CAS  Google Scholar 

  • Schluter, D., Price, T., Mooers, A. O., & Ludwig, D. (1997). Likelihood of ancestor states in adaptive radiation. Evolution, 51, 1699–1711.

    Article  Google Scholar 

  • Schnitzler, J., Barraclough, T. G., Boatwright, J. S., Goldblatt, P., Manning, J. C., Powell, M. P., et al. (2011). Causes of plant diversification in the cape biodiversity hotspot of South Africa. Systematic Biology, 60, 343–357.

    Article  PubMed  Google Scholar 

  • Sepkoski, J. J. (1998). Rates of speciation in the fossil record. Philosophical Transactions of the Royal Society B Biological Sciences, 353, 315–326.

    Article  PubMed Central  Google Scholar 

  • Silvestro, D., Schnitzler, J., & Zizka, G. (2011). A Bayesian framework to estimate diversification rates and their variation through time and space. BMC Evolutionary Biology, 11, 311.

    Article  PubMed Central  PubMed  Google Scholar 

  • Stadler, T. (2009). On incomplete sampling under birth-death models and connections to the sampling-based coalescent. Journal of Theoretical Biology, 261, 58–66.

    Article  PubMed  Google Scholar 

  • Stadler, T. (2011). Mammalian phylogeny reveals recent diversification rate shifts. Proceedings of the National Academy of Sciences of the United States of America, 108, 6187–6192.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vamosi, J. C., & Vamosi, S. M. (2010). Key innovations within a geographical context in flowering plants: Towards resolving Darwin’s abominable mystery. Ecology Letters, 13, 1270–1279.

    Article  PubMed  Google Scholar 

  • Wertheim, J. O., & Sanderson, M. J. (2011). Estimating diversification rates: How useful are divergence times? Evolution, 65, 309–320.

    Article  PubMed Central  PubMed  Google Scholar 

  • Weston, S. J. (2013). FOREACH: R package for parallel computing. Palo Alto, USA: Revolutionary Analytics.

    Google Scholar 

  • Wiens, J. J. (2011). The causes of species richness patterns across space, time, and clades and the role of ecological limits. The Quarterly Review of Biology, 86, 75–96.

    Article  PubMed  Google Scholar 

  • Wiens, J. J., Graham, C. H., Moen, D. S., Smith, S. A., & Reeder, T. W. (2006). Evolutionary and ecological causes of the latitudinal diversity gradient in hylid frogs: Treefrog trees unearth the roots of high tropical diversity. American Naturalist, 168, 579–596.

    Article  PubMed  Google Scholar 

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Acknowledgments

I am thankful to Luke Harmon, Dan Rabosky, John Wiens and members of his lab for insightful comments on earlier versions of the manuscript. They may not necessarily endorse everything I have written. Computational capacity was lent by the NGI MetaCentrum, provided under the program “Projects of large infrastructure for research, development, and innovations” (LM2010005). This work was supported by the Grant Agency of the Czech Republic (P505/11/2387) and the J. W. Fulbright Commission.

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  1. Department of Ecology and Evolution, Stony Brook University, 650 Life Sciences Bldg., Stony Brook, NY, 11794, USA

    Antonin Machac

  2. Department of Ecology, Charles University, Vinicna 7, 128 44, Praha 2, Czech Republic

    Antonin Machac

  3. Center for Theoretical Study, Charles University and Academy of Sciences of the Czech Republic, Jilska 1, 110 00, Praha 1, Czech Republic

    Antonin Machac

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Machac, A. Detecting Trait-Dependent Diversification Under Diversification Slowdowns. Evol Biol 41, 201–211 (2014). https://doi.org/10.1007/s11692-013-9258-z

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