journal article Open Access Nov 16, 2022

Modeling the Evolution of Rates of Continuous Trait Evolution

View at Publisher Save 10.1093/sysbio/syac068
Abstract
Abstract
Rates of phenotypic evolution vary markedly across the tree of life, from the accelerated evolution apparent in adaptive radiations to the remarkable evolutionary stasis exhibited by so-called “living fossils.” Such rate variation has important consequences for large-scale evolutionary dynamics, generating vast disparities in phenotypic diversity across space, time, and taxa. Despite this, most methods for estimating trait evolution rates assume rates vary deterministically with respect to some variable of interest or change infrequently during a clade’s history. These assumptions may cause underfitting of trait evolution models and mislead hypothesis testing. Here, we develop a new trait evolution model that allows rates to vary gradually and stochastically across a clade. Further, we extend this model to accommodate generally decreasing or increasing rates over time, allowing for flexible modeling of “early/late bursts” of trait evolution. We implement a Bayesian method, termed “evolving rates” (evorates for short), to efficiently fit this model to comparative data. Through simulation, we demonstrate that evorates can reliably infer both how and in which lineages trait evolution rates varied during a clade’s history. We apply this method to body size evolution in cetaceans, recovering substantial support for an overall slowdown in body size evolution over time with recent bursts among some oceanic dolphins and relative stasis among beaked whales of the genus Mesoplodon. These results unify and expand on previous research, demonstrating the empirical utility of evorates. [cetacea; macroevolution; comparative methods; phenotypic diversity; disparity; early burst; late burst]
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References
90
[1]
Arnold "Understanding the evolution and stability of the G-matrix" Evolution (2008) 10.1111/j.1558-5646.2008.00472.x
[2]
Beaulieu "Detecting hidden diversification shifts in models of trait-dependent speciation and extinction" Syst. Biol (2016) 10.1093/sysbio/syw022
[3]
Benson "Rates of dinosaur body mass evolution indicate 170 million years of sustained ecological innovation on the avian stem lineage" PLoS Biol (2014) 10.1371/journal.pbio.1001853
[4]
Betancourt "Hamiltonian Monte Carlo for hierarchical models" arXiv (2013)
[5]
Blomberg "Testing for phylogenetic signal in comparative data: behavioral traits are more labile" Evolution (2003)
[6]
Borstein "Reef fish functional traits evolve fastest at trophic extremes" Nat. Ecol. Evol (2019) 10.1038/s41559-018-0725-x
[7]
Browne "A comparison of Bayesian and likelihood-based methods for fitting multilevel models" Bayesian Anal (2006) 10.1214/06-ba117
[8]
Brusatte "Dinosaur morphological diversity and the end-Cretaceous extinction" Nat. Commun (2012) 10.1038/ncomms1815
[9]
Caetano "Estimating correlated rates of trait evolution with uncertainty" Syst. Biol (2019) 10.1093/sysbio/syy067
[10]
Caron "The phylogenetic signal of diversification rates" J. Zool. Syst. Evol. Res (2020) 10.1111/jzs.12379
[11]
Stan: A Probabilistic Programming Language

Bob Carpenter, Andrew Gelman, Matthew D. Hoffman et al.

Journal of Statistical Software 2017 10.18637/jss.v076.i01
[12]
Chartier "Global patterns and a latitudinal gradient of flower disparity: perspectives from the angiosperm order ericales" New Phytol (2021) 10.1111/nph.17195
[13]
Chira "Correlates of rate heterogeneity in avian ecomorphological traits" Ecol. Lett (2018) 10.1111/ele.13131
[14]
Chira "The impact of rate heterogeneity on inference of phylogenetic models of trait evolution" J. Evol. Biol (2016) 10.1111/jeb.12979
[15]
Clavel "Accelerated body size evolution during cold climatic periods in the cenozoic" Proc. Natl. Acad. Sci. U.S.A (2017) 10.1073/pnas.1606868114
[16]
Constantine "Future directions in research on Bryde’s whales" Front. Mar. Sci (2018) 10.3389/fmars.2018.00333
[17]
Cooper "What factors shape rates of phenotypic evolution? a comparative study of cranial morphology of four mammalian clades" J. Evol. Biol (2009) 10.1111/j.1420-9101.2009.01714.x
[18]
Cooper "A cautionary note on the use of Ornstein Uhlenbeck models in macroevolutionary studies" Biol. J. Linn. Soc. Lond (2016) 10.1111/bij.12701
[19]
Devreese "Path integral approach to Asian options in the Black-Scholes model" Phys. A: Stat. Mech. Appl (2010) 10.1016/j.physa.2009.10.020
[20]
Donoghue "Confluence, synnovation, and depauperons in plant diversification" New Phytol (2015) 10.1111/nph.13367
[21]
Drury "Tempo and mode of morphological evolution are decoupled from latitude in birds" PLoS Biol (2021) 10.1371/journal.pbio.3001270
[22]
Dufresne "The log-normal approximation in financial and other computations" Adv. Appl. Probab (2004) 10.1239/aap/1093962232
[23]
Eastman "A novel comparative method for identifying shifts in the rate of character evolution on trees" Evolution (2011) 10.1111/j.1558-5646.2011.01401.x
[24]
Fabre "Metamorphosis shapes cranial diversity and rate of evolution in salamanders" Nat. Ecol. Evol (2020) 10.1038/s41559-020-1225-3
[25]
Felsenstein "Maximum-likelihood estimation of evolutionary trees from continuous characters" Am. J. Hum. Genet (1973)
[26]
Felsenstein "Comparative methods with sampling error and within-species variation: contrasts revisited and revised" Am. Nat (2008) 10.1086/587525
[27]
Fisher "Relaxed random walks at scale" Syst. Biol (2021) 10.1093/sysbio/syaa056
[28]
Freckleton "Fast likelihood calculations for comparative analyses" Methods Ecol. Evol (2012) 10.1111/j.2041-210x.2012.00220.x
[29]
Gingerich "Rates of evolution" Annu. Rev. Ecol. Evol. Syst (2009) 10.1146/annurev.ecolsys.39.110707.173457
[30]
Goolsby "Rapid maximum likelihood ancestral state reconstruction of continuous characters: a rerooting-free algorithm" Ecol. Evol (2017) 10.1002/ece3.2837
[31]
Hansen "Analyzing disparity and rates of morphological evolution with model-based phylogenetic comparative methods" Syst. Biol (2022) 10.1093/sysbio/syab079
[32]
Harmon "Early bursts of body size and shape evolution are rare in comparative data" Evolution (2010)
[33]
Hassler "Inferring phenotypic trait evolution on large trees with many incomplete measurements" J. Am. Stat. Assoc (2020) 10.1080/01621459.2020.1799812
[34]
Held "On p-values and Bayes factors" Annu. Rev. Stat. Appl (2018) 10.1146/annurev-statistics-031017-100307
[35]
Hoffman "The No-U-Turn sampler: adaptively setting path lengths in Hamiltonian Monte Carlo" J. Mach. Learn. Res (2014)
[36]
Hopkins "Dynamic evolutionary change in post-Paleozoic echinoids and the importance of scale when interpreting changes in rates of evolution" Proc. Natl. Acad. Sci. U.S.A (2015) 10.1073/pnas.1418153112
[37]
Bayes Factors

Robert E. Kass, Adrian E. Raftery

Journal of the American Statistical Association 1995 10.1080/01621459.1995.10476572
[38]
Landis "Pulsed evolution shaped modern vertebrate body sizes" Proc. Natl. Acad. Sci. U.S.A (2017) 10.1073/pnas.1710920114
[39]
Landis "Phylogenetic analysis using lévy processes: finding jumps in the evolution of continuous traits" Syst. Biol (2013) 10.1093/sysbio/sys086
[40]
Lartillot "A mixed relaxed clock model" Philos. Trans. R. Soc. Lond. B Biol. Sci (2016) 10.1098/rstb.2015.0132
[41]
Lartillot "A phylogenetic model for investigating correlated evolution of substitution rates and continuous phenotypic characters" Mol. Biol. Evol (2011) 10.1093/molbev/msq244
[42]
Lemoine "Moving beyond noninformative priors: why and how to choose weakly informative priors in bayesian analyses" Oikos (2019) 10.1111/oik.05985
[43]
Lepage "A general comparison of relaxed molecular clock models" Mol. Biol. Evol (2007) 10.1093/molbev/msm193
[44]
Lepage "Continuous and tractable models for the variation of evolutionary rates" Math. Biosci (2006) 10.1016/j.mbs.2005.11.002
[45]
Log-normal Distributions across the Sciences: Keys and Clues

ECKHARD LIMPERT, WERNER A. STAHEL, MARKUS ABBT

BioScience 2001 10.1641/0006-3568(2001)051[0341:lndats]2.0.co;2
[46]
Lloyd "A total-group phylogenetic metatree for cetacea and the importance of fossil data in diversification analyses" Syst. Biol (2021) 10.1093/sysbio/syab002
[47]
Lloyd "Identifying heterogeneity in rates of morphological evolution: discrete character change in the evolution of lungfish (sarcopterygii; dipnoi)" Evolution (2012) 10.1111/j.1558-5646.2011.01460.x
[48]
May "A Bayesian approach for inferring the impact of a discrete character on rates of continuous-character evolution in the presence of background-rate variation" Syst. Biol (2020) 10.1093/sysbio/syz069
[49]
Mihalitsis "Morphological and functional diversity of piscivorous fishes on coral reefs" Coral Reefs (2019) 10.1007/s00338-019-01820-w
[50]
Montgomery "The evolutionary history of cetacean brain and body size" Evolution (2013) 10.1111/evo.12197

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23
Citations
90
References
Details
Published
Nov 16, 2022
Vol/Issue
72(3)
Pages
590-605
License
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Funding
National Science Foundation Award: DEB-1831164
Cite This Article
Bruce S Martin, Gideon S Bradburd, Luke J Harmon, et al. (2022). Modeling the Evolution of Rates of Continuous Trait Evolution. Systematic Biology, 72(3), 590-605. https://doi.org/10.1093/sysbio/syac068
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