Understanding the effect of competition during evolutionary radiations: an integrated model of phenotypic and species diversification
Corresponding Author
Leandro Aristide
École Normale Supérieure, Paris Sciences et Lettres (PSL) Research University, Institut de Biologie de l’École Normale Supérieure (IBENS), CNRS, UMR 8197, INSERM U1024, 46 rue d’Ulm, F-75005 Paris, France
Correspondence: E-mail: [email protected]
Search for more papers by this authorHélène Morlon
École Normale Supérieure, Paris Sciences et Lettres (PSL) Research University, Institut de Biologie de l’École Normale Supérieure (IBENS), CNRS, UMR 8197, INSERM U1024, 46 rue d’Ulm, F-75005 Paris, France
Search for more papers by this authorCorresponding Author
Leandro Aristide
École Normale Supérieure, Paris Sciences et Lettres (PSL) Research University, Institut de Biologie de l’École Normale Supérieure (IBENS), CNRS, UMR 8197, INSERM U1024, 46 rue d’Ulm, F-75005 Paris, France
Correspondence: E-mail: [email protected]
Search for more papers by this authorHélène Morlon
École Normale Supérieure, Paris Sciences et Lettres (PSL) Research University, Institut de Biologie de l’École Normale Supérieure (IBENS), CNRS, UMR 8197, INSERM U1024, 46 rue d’Ulm, F-75005 Paris, France
Search for more papers by this authorAbstract
Competition can drive macroevolutionary change, for example during adaptive radiations. However, we still lack a clear understanding of how it shapes diversification processes and patterns. To better understand the macroevolutionary consequences of competition, as well as the signal left on phylogenetic data, we developed a model linking trait evolution and species diversification in an ecological context. We find four main results: first, competition spurs trait diversity but not necessarily species richness; second, competition produces slowdowns in species diversification even in the absence of explicit ecological limits, but not in phenotypic diversification even in the presence of such limits; third, early burst patterns do not provide a reliable way of testing for adaptive radiations; and fourth, looking for phylogenetic signal in trait data and support for phenotypic models incorporating competition is a better alternative. Our results clarify the macroevolutionary consequences of competition and could help design more powerful tests of adaptive radiations in nature.
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References
- Aguilée, R., Gascuel, F., Lambert, A. & Ferriere, R. (2018). Clade diversification dynamics and the biotic and abiotic controls of speciation and extinction rates. Nat. Commun., 9, 1–13.
- Bailey, S.F., Dettman, J.R., Rainey, P.B. & Kassen, R. (2013). Competition both drives and impedes diversification in a model adaptive radiation. Proc. R. Soc. B Biol. Sci., 280, 20131253.
- Blomberg, S.P., Garland, T. Jr & Ives, A.R. (2003). Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution, 57, 717–745.
- Burnham, K.P. & Anderson, D.R. (2004). Multimodel inference: understanding AIC and BIC in model selection. Sociol. Methods Res., 33, 261–304.
- Clarke, M., Thomas, G.H. & Freckleton, R.P. (2017). Trait evolution in adaptive radiations: modeling and measuring interspecific competition on phylogenies. Am. Nat., 189, 121–137.
- Condamine, F., Rolland, J. & Morlon, H. (in press). Assessing the causes of diversification slowdowns: temperature-dependent and diversitydependent models receive equivalent support. Ecol. Lett. http://doi.org/10.1111/ele.13382
- Cooper, N. & Purvis, A. (2009). What factors shape rates of phenotypic evolution? A comparative study of cranial morphology of four mammalian clades. J. Evol. Biol., 22, 1024–1035.
- Cornell, H.V. (2013). Is regional species diversity bounded or unbounded? Biol. Rev., 88, 140–165.
- Dieckmann, U. & Doebeli, M.O. (1999). On the origin of species by sympatric speciation. Nature, 400, 354–357.
- Doebeli, M. & Dieckmann, U. (2000). Evolutionary branching and sympatric speciation caused by different types of ecological interactions. Am. Nat., 156, S77–S101.
- Doebeli, M. & Ispolatov, I. (2017). Diversity and coevolutionary dynamics in high-dimensional phenotype spaces. Am. Nat., 189, 105–120.
- Drury, J., Clavel, J., Manceau, M. & Morlon, H. (2016). Estimating the effect of competition on trait evolution using maximum likelihood inference. Syst. Biol., 65, 700–710.
- Drury, J.P., Grether, G.F., Garland, T. Jr & Morlon, H. (2018). An assessment of phylogenetic tools for analyzing the interplay between interspecific interactions and phenotypic evolution. Syst. Biol., 67, 413–427.
- Dynesius, M. & Jansson, R. (2014). Persistence of within-species lineages: a neglected control of speciation rates. Evolution, 68, 923–934.
- Etienne, R.S. & Rosindell, J. (2012). Prolonging the past counteracts the pull of the present: protracted speciation can explain observed slowdowns in diversification. Syst. Biol., 61, 204–213.
- 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. Proc. R. Soc. B Biol. Sci., 279, 1300–1309.
- Felice, R.N., Randau, M. & Goswami, A. (2018). A fly in a tube: macroevolutionary expectations for integrated phenotypes. Evolution, 72, 2580–2594.
- Felsenstein, J. (1985). Phylogenies and the comparative method. Am. Nat., 125, 1–15.
- Foote, M. (1996). Models of Morphological Diversification. Evolutionary Paleobiology. University Chicago Press, Chicago, 62–86.
- Frankham, R. (2005). Genetics and extinction. Biol. Cons., 126, 131–140.
- Futuyma, D.J. (1998). Evolutionary Biology. Sinauer Associates, Sunderland, MA.
- Futuyma, D.J. (2010). Evolutionary constraint and ecological consequences. Evolution, 64, 1865–1884.
- Gavrilets, S. (1999). Dynamics of clade diversification on the morphological hypercube. Proc. R. Soc. B Biol. Sci., 266, 817–824.
- Gavrilets, S. & Losos, J.B. (2009). Adaptive radiation: contrasting theory with data. Science, 323, 732–737.
- Hansen, T.F. (1997). Stabilizing selection and the comparative analysis of adaptation. Evolution, 51, 1341–1351.
- Harmon, L.J. & Harrison, S. (2015). Species diversity is dynamic and unbounded at local and continental scales. Am. Nat., 185, 584–593.
- Harmon, L.J., Schulte, J.A. II, Larson, A. & Losos, J.B. (2003). Tempo and mode of evotutionary radiation in Iguanian lizards. Science, 301, 961–964.
- Harmon, L.J., Losos, J.B., Davies, J.T., Gillespie, R.G., Gittleman, J.L., Jennings, B.W. et al. (2010). Early bursts of body size and shape evolution are rare in comparative data. Evolution, 64, 2385–2396.
- Harvey, P.H. & Rambaut, A. (2000). Comparative analyses for adaptive radiations. Philos. Trans. Royal Soc. B, 355, 1599–1605.
- Hopkins, M.J. & Smith, A.B. (2015). Dynamic evolutionary change in post-Paleozoic echinoids and the importance of scale when interpreting changes in rates of evolution. Proc. Natl Acad. Sci., 201418153
- Hughes, M., Gerber, S. & Wills, M.A. (2013). Clades reach highest morphological disparity early in their evolution. Proc. Natl. Acad. Sci., 110, 13875–13879.
- Lande, R. (1993). Risks of population extinction from demographic and environmental stochasticity and random catastrophes. Am. Nat., 142, 911–927.
- Lewitus, E., Aristide, L. & Morlon, H. (in press). Characterizing and comparing phylogenetic trait data from their normalized Laplacian spectrum. Syst. Biol. https://doi.org/10.1101/654087
- Liow, L.H., Quental, T.B. & Marshall, C.R. (2010). When can decreasing diversification rates be detected with molecular phylogenies and the fossil record? Syst. Biol., 59, 646–659.
- Liow, L.H., Reitan, T. & Harnik, P.G. (2015). Ecological interactions on macroevolutionary time scales: clams and brachiopods are more than ships that pass in the night. Ecol. Lett., 18, 1030–1039.
- Losos, J.B. (2008). Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol. Lett., 11, 995–1003.
- MacArthur, R. & Levins, R. (1967). The limiting similarity, convergence, and divergence of coexisting species. Am. Nat., 101, 377–385.
- Mahler, D.L., Revell, L.J., Glor, R.E. & Losos, J.B. (2010). Ecological opportunity and the rate of morphological evolution in the diversification of greater Antillean anoles. Evolution, 64, 2731–2745.
- Maliet, O., Hartig, F. & Morlon, H. (2019). A model with many small shifts for estimating species-specific diversification rates. Nature Ecol. Evol., 3, 1086–1092.
- Manceau, M., Lambert, A. & Morlon, H. (2017). A unifying comparative phylogenetic framework including traits coevolving across interacting lineages. Syst. Biol., 66, 551–568.
- McPeek, M.A. (2008). The ecological dynamics of clade diversification and community assembly. Am. Nat., 172, E270–E284.
- Meyer, J.R. & Kassen, R. (2007). The effects of competition and predation on diversification in a model adaptive radiation. Nature, 446, 432–435.
- Moen, D. & Morlon, H. (2014). Why does diversification slow down? Trends Ecol. Evol., 29, 190–197.
- Morlon, H., Potts, M.D. & Plotkin, J.B. (2010). Inferring the dynamics of diversification: a coalescent approach. PLoS Biol., 8, e1000493.
- Morlon, H., Lewitus, E., Condamine, F.L., Manceau, M., Clavel, J. & Drury, J. (2016). RPANDA: An R package for macroevolutionary analyses on phylogenetic trees. Methods Ecol. Evol., 7, 589–597.
- Nee, S., May, R.M. & Harvey, P.H. (1994). The reconstructed evolutionary process. Phil. Trans. R. Soc. Lond. B, 344, 305–311.
- Nuismer, S.L. & Harmon, L.J. (2015). Predicting rates of interspecific interaction from phylogenetic trees. Ecol. Lett., 18, 17–27.
- Pennell, M.W. & Harmon, L.J. (2013). An integrative view of phylogenetic comparative methods: connections to population genetics, community ecology, and paleobiology. Ann. N. Y. Acad. Sci., 1289, 90–105.
- Pennell, M.W., Eastman, J.M., Slater, G.J., Brown, J.W., Uyeda, J.C., FitzJohn, R.G. et al. (2014). geiger v2. 0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees. Bioinformatics, 30, 2216–2218.
- Pfennig, K.S. & Pfennig, D.W. (2005). Character displacement as the “best of a bad situation”: fitness trade-offs resulting from selection to minimize resource and mate competition. Evolution, 59, 2200–2208.
- Pfennig, K. & Pfennig, D. (2009). Character displacement: ecological and reproductive responses to a common evolutionary problem. Q. Rev. Biol., 84, 253–276.
- Phillimore, A.B. & Price, T.D. (2008). Density-dependent cladogenesis in birds. PLoS Biol., 6, e71.
- Pybus, O.G. & Harvey, P.H. (2000). Testing macro–evolutionary models using incomplete molecular phylogenies. Proc. R. Soc. London B Biol. Sci., 267, 2267–2272.
- Rabosky, D.L. (2009). Ecological limits and diversification rate: alternative paradigms to explain the variation in species richness among clades and regions. Ecol. Lett., 12, 735–743.
- Rabosky, D.L. (2013). Diversity-dependence, ecological speciation, and the role of competition in macroevolution. Annu. Rev. Ecol. Evol. Syst., 44, 481–502.
- Rabosky, D.L. (2014). Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS ONE, 9, e89543.
- Rabosky, D.L. & Lovette, I.J. (2008a). Density-dependent diversification in North American wood warblers. Proc. R. Soc. B Biol. Sci., 275, 2363–2371.
- Rabosky, D.L. & Lovette, I.J. (2008b). Explosive evolutionary radiations: decreasing speciation or increasing extinction through time? Evolution, 62, 1866–1875.
- Revell, L.J. (2012). phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol., 3, 217–223.
- Revell, L.J., Harmon, L.J. & Collar, D.C. (2008). Phylogenetic signal, evolutionary process, and rate. Syst. Biol., 57, 591–601.
- Rosenblum, E.B., Sarver, B.A.J., Brown, J.W., Des Roches, S., Hardwick, K.M., Hether, T.D. et al. (2012). Goldilocks meets Santa Rosalia: an ephemeral speciation model explains patterns of diversification across time scales. Evol. Biol., 39, 255–261.
- Rundle, H.D. & Nosil, P. (2005). Ecological speciation. Ecol. Lett., 8, 336–352.
- Schluter, D. (1996). Adaptive radiation along genetic lines of least resistance. Evolution, 50, 1766–1774.
- Schluter, D. (2000). The Ecology of Adaptive Radiation. Oxford Univeristy Press, Oxford.
- Schluter, D. (2001). Ecology and the origin of species. Trends Ecol. Evol., 16, 372–380.
- Sepkoski, J.J. Jr (1978). A kinetic model of Phanerozoic taxonomic diversity I. Analysis of marine orders. Paleobiology, 4, 223–251.
- Sepkoski, J.J. Jr (1996). Competition in macroevolution: the double wedge revisited. In: Evolutionary Paleobiology (eds D. Jablonski, D.H. Erwin & J.H. Lipps). University of Chicago Press, Chicago, IL, pp. 211–255.
- Silvestro, D., Antonelli, A., Salamin, N. & Quental, T.B. (2015). The role of clade competition in the diversification of North American canids. Proc. Natl. Acad. Sci., 112, 8684–8689.
- Simpson, G.G. (1953). The Majors Features of Evolution. Columbia University Press, New York.
10.7312/simp93764 Google Scholar
- Slatkin, M. (1980). Ecological character displacement. Ecology, 61, 163–177.
- Soulebeau, A., Aubriot, X., Gaudeul, M., Rouhan, G., Hennequin, S., Haevermans, T. et al. (2015). The hypothesis of adaptive radiation in evolutionary biology: hard facts about a hazy concept. Org. Divers. Evol., 15, 747–761.
- Stanley, S.M. (1979). Macroevolution, Pattern and Process. Johns Hopkins University Press, Baltimore, MD.
- Stroud, J.T. & Losos, J.B. (2016). Ecological opportunity and adaptive radiation. Annu. Rev. Ecol. Evol. Syst., 47, 507–532.
- Uyeda, J.C., Caetano, D.S. & Pennell, M.W. (2015). Comparative analysis of principal components can be misleading. Syst. Biol., 64, 677–689.
- Venditti, C., Meade, A. & Pagel, M. (2011). Multiple routes to mammalian diversity. Nature, 479, 393–396.
- Vermeij, G.J. (2013). On escalation. Annu. Rev. Earth Planet. Sci., 41, 1–19.
- Webb, C. (2003). A complete classification of Darwinian extinction in ecological interactions. Am. Nat., 161, 181–205.
- Weber, M.G., Wagner, C.E., Best, R.J., Harmon, L.J. & Matthews, B. (2017). Evolution in a community context: on integrating ecological interactions and macroevolution. Trends Ecol. Evol., 32, 291–304.
- Weir, J.T. & Mursleen, S. (2013). Diversity-dependent cladogenesis and trait evolution in the adaptive radiation of the auks (Aves: Alcidae). Evolution, 67, 403–416.
- Wright, S. (1931). Evolution in Mendelian populations. Genetics, 16, 97.