DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Estimating rates and patterns of diversification with incomplete sampling: a case study in the rosids

Abstract

Premise Recent advances in generating large‐scale phylogenies enable broad‐scale estimation of species diversification. These now common approaches typically are characterized by (1) incomplete species coverage without explicit sampling methodologies and/or (2) sparse backbone representation, and usually rely on presumed phylogenetic placements to account for species without molecular data. We used empirical examples to examine the effects of incomplete sampling on diversification estimation and provide constructive suggestions to ecologists and evolutionary biologists based on those results. Methods We used a supermatrix for rosids and one well‐sampled subclade (Cucurbitaceae) as empirical case studies. We compared results using these large phylogenies with those based on a previously inferred, smaller supermatrix and on a synthetic tree resource with complete taxonomic coverage. Finally, we simulated random and representative taxon sampling and explored the impact of sampling on three commonly used methods, both parametric (RPANDA and BAMM) and semiparametric (DR). Results We found that the impact of sampling on diversification estimates was idiosyncratic and often strong. Compared to full empirical sampling, representative and random sampling schemes either depressed or inflated speciation rates, depending on methods and sampling schemes. No method was entirely robust to poor sampling, but BAMM was least sensitive to moderate levels of missingmore » taxa. Conclusions We suggest caution against uncritical modeling of missing taxa using taxonomic data for poorly sampled trees and in the use of summary backbone trees and other data sets with high representative bias, and we stress the importance of explicit sampling methodologies in macroevolutionary studies.« less

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [5]; ORCiD logo [6]; ORCiD logo [7]
  1. Florida Museum of Natural History University of Florida Gainesville Florida 32611 USA, State Key Laboratory of Systematic and Evolutionary Botany Institute of Botany Chinese Academy of Sciences Beijing 100093 China, Department of Bioscience Aarhus University Aarhus 8000 Denmark
  2. Department of Biological Sciences Mississippi State University Mississippi State Mississippi 39762 USA
  3. Department of Biology University of Florida Gainesville Florida 32611 USA, Biodiversity Institute University of Florida Gainesville Florida 32611 USA
  4. Florida Museum of Natural History University of Florida Gainesville Florida 32611 USA, Biodiversity Institute University of Florida Gainesville Florida 32611 USA, Genetics Institute University of Florida Gainesville Florida 32608 USA
  5. State Key Laboratory of Systematic and Evolutionary Botany Institute of Botany Chinese Academy of Sciences Beijing 100093 China
  6. Florida Museum of Natural History University of Florida Gainesville Florida 32611 USA, Department of Biology University of Florida Gainesville Florida 32611 USA, Biodiversity Institute University of Florida Gainesville Florida 32611 USA, Genetics Institute University of Florida Gainesville Florida 32608 USA
  7. Florida Museum of Natural History University of Florida Gainesville Florida 32611 USA, Biodiversity Institute University of Florida Gainesville Florida 32611 USA
Publication Date:
Research Org.:
Univ. of Florida, Gainesville, FL (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Science Foundation (NSF); Chinese Academy of Sciences; National Natural Science Foundation of China (NSFC)
OSTI Identifier:
1632777
Alternate Identifier(s):
OSTI ID: 1632778; OSTI ID: 1803330
Grant/Contract Number:  
DE‐SC0018247; SC0018247; DEB-1208809; DEB-1442280; DBI-1523667; DEB-1916632; XDA19050103; XDB31000000; 31590822
Resource Type:
Published Article
Journal Name:
American Journal of Botany
Additional Journal Information:
Journal Name: American Journal of Botany Journal Volume: 107 Journal Issue: 6; Journal ID: ISSN 0002-9122
Publisher:
Wiley Blackwell (John Wiley & Sons)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; plant sciences; diversification; mega-phylogeny; modeling; rosids; sampling bias

Citation Formats

Sun, Miao, Folk, Ryan A., Gitzendanner, Matthew A., Soltis, Pamela S., Chen, Zhiduan, Soltis, Douglas E., and Guralnick, Robert P. Estimating rates and patterns of diversification with incomplete sampling: a case study in the rosids. United States: N. p., 2020. Web. doi:10.1002/ajb2.1479.
Sun, Miao, Folk, Ryan A., Gitzendanner, Matthew A., Soltis, Pamela S., Chen, Zhiduan, Soltis, Douglas E., & Guralnick, Robert P. Estimating rates and patterns of diversification with incomplete sampling: a case study in the rosids. United States. https://doi.org/10.1002/ajb2.1479
Sun, Miao, Folk, Ryan A., Gitzendanner, Matthew A., Soltis, Pamela S., Chen, Zhiduan, Soltis, Douglas E., and Guralnick, Robert P. Tue . "Estimating rates and patterns of diversification with incomplete sampling: a case study in the rosids". United States. https://doi.org/10.1002/ajb2.1479.
@article{osti_1632777,
title = {Estimating rates and patterns of diversification with incomplete sampling: a case study in the rosids},
author = {Sun, Miao and Folk, Ryan A. and Gitzendanner, Matthew A. and Soltis, Pamela S. and Chen, Zhiduan and Soltis, Douglas E. and Guralnick, Robert P.},
abstractNote = {Premise Recent advances in generating large‐scale phylogenies enable broad‐scale estimation of species diversification. These now common approaches typically are characterized by (1) incomplete species coverage without explicit sampling methodologies and/or (2) sparse backbone representation, and usually rely on presumed phylogenetic placements to account for species without molecular data. We used empirical examples to examine the effects of incomplete sampling on diversification estimation and provide constructive suggestions to ecologists and evolutionary biologists based on those results. Methods We used a supermatrix for rosids and one well‐sampled subclade (Cucurbitaceae) as empirical case studies. We compared results using these large phylogenies with those based on a previously inferred, smaller supermatrix and on a synthetic tree resource with complete taxonomic coverage. Finally, we simulated random and representative taxon sampling and explored the impact of sampling on three commonly used methods, both parametric (RPANDA and BAMM) and semiparametric (DR). Results We found that the impact of sampling on diversification estimates was idiosyncratic and often strong. Compared to full empirical sampling, representative and random sampling schemes either depressed or inflated speciation rates, depending on methods and sampling schemes. No method was entirely robust to poor sampling, but BAMM was least sensitive to moderate levels of missing taxa. Conclusions We suggest caution against uncritical modeling of missing taxa using taxonomic data for poorly sampled trees and in the use of summary backbone trees and other data sets with high representative bias, and we stress the importance of explicit sampling methodologies in macroevolutionary studies.},
doi = {10.1002/ajb2.1479},
journal = {American Journal of Botany},
number = 6,
volume = 107,
place = {United States},
year = {Tue Jun 09 00:00:00 EDT 2020},
month = {Tue Jun 09 00:00:00 EDT 2020}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1002/ajb2.1479

Citation Metrics:
Cited by: 11 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Angiosperm phylogeny: 17 genes, 640 taxa
journal, April 2011

  • Soltis, Douglas E.; Smith, Stephen A.; Cellinese, Nico
  • American Journal of Botany, Vol. 98, Issue 4
  • DOI: 10.3732/ajb.1000404

PASTIS: an R package to facilitate phylogenetic assembly with soft taxonomic inferences
journal, November 2013

  • Thomas, Gavin H.; Hartmann, Klaas; Jetz, Walter
  • Methods in Ecology and Evolution, Vol. 4, Issue 11
  • DOI: 10.1111/2041-210X.12117

Extant timetrees are consistent with a myriad of diversification histories
journal, April 2020


A New Method for Handling Missing Species in Diversification Analysis Applicable to Randomly or Nonrandomly Sampled Phylogenies
journal, February 2012

  • Cusimano, Natalie; Stadler, Tanja; Renner, Susanne S.
  • Systematic Biology, Vol. 61, Issue 5
  • DOI: 10.1093/sysbio/sys031

Non-equilibrium dynamics and floral trait interactions shape extant angiosperm diversity
journal, May 2016

  • O'Meara, Brian C.; Smith, Stacey D.; Armbruster, W. Scott
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 283, Issue 1830
  • DOI: 10.1098/rspb.2015.2304

BAMM gives misleading rate estimates in simulated and empirical datasets
journal, August 2018

  • Meyer, Andreas L. S.; Román‐Palacios, Cristian; Wiens, John J.
  • Evolution, Vol. 72, Issue 10
  • DOI: 10.1111/evo.13574

Key questions and challenges in angiosperm macroevolution
journal, March 2018

  • Sauquet, Hervé; Magallón, Susana
  • New Phytologist, Vol. 219, Issue 4
  • DOI: 10.1111/nph.15104

Three keys to the radiation of angiosperms into freezing environments
journal, December 2013

  • Zanne, Amy E.; Tank, David C.; Cornwell, William K.
  • Nature, Vol. 506, Issue 7486
  • DOI: 10.1038/nature12872

Global patterns of diversification in the history of modern amphibians
journal, January 2007

  • Roelants, Kim; Gower, David J.; Wilkinson, Mark
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 3
  • DOI: 10.1073/pnas.0608378104

Towards a phylogenetic nomenclature of Tracheophyta
journal, August 2007

  • Cantino, Philip D.; Doyle, James A.; Graham, Sean W.
  • TAXON, Vol. 56, Issue 3
  • DOI: 10.2307/25065864

Critically evaluating the theory and performance of Bayesian analysis of macroevolutionary mixtures
journal, August 2016

  • Moore, Brian R.; Höhna, Sebastian; May, Michael R.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 34
  • DOI: 10.1073/pnas.1518659113

Mammalian phylogeny reveals recent diversification rate shifts
journal, March 2011


An inverse latitudinal gradient in speciation rate for marine fishes
journal, July 2018


Synthesis of phylogeny and taxonomy into a comprehensive tree of life
journal, September 2015

  • Hinchliff, Cody E.; Smith, Stephen A.; Allman, James F.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 41
  • DOI: 10.1073/pnas.1423041112

Ferns diversified in the shadow of angiosperms
journal, April 2004

  • Schneider, Harald; Schuettpelz, Eric; Pryer, Kathleen M.
  • Nature, Vol. 428, Issue 6982
  • DOI: 10.1038/nature02361

Diversification rates and species richness across the Tree of Life
journal, September 2016

  • Scholl, Joshua P.; Wiens, John J.
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 283, Issue 1838
  • DOI: 10.1098/rspb.2016.1334

Taxon sampling effects in molecular clock dating: An example from the African Restionaceae
journal, June 2005

  • Linder, H. Peter; Hardy, Christopher R.; Rutschmann, Frank
  • Molecular Phylogenetics and Evolution, Vol. 35, Issue 3
  • DOI: 10.1016/j.ympev.2004.12.006

On incomplete sampling under birth–death models and connections to the sampling-based coalescent
journal, November 2009


The delayed rise of present-day mammals
journal, March 2007

  • Bininda-Emonds, Olaf R. P.; Cardillo, Marcel; Jones, Kate E.
  • Nature, Vol. 446, Issue 7135
  • DOI: 10.1038/nature05634

Impact of whole-genome duplication events on diversification rates in angiosperms
journal, March 2018

  • Landis, Jacob B.; Soltis, Douglas E.; Li, Zheng
  • American Journal of Botany, Vol. 105, Issue 3
  • DOI: 10.1002/ajb2.1060

Thirty clues to the exceptional diversification of flowering plants
journal, October 2018

  • Magallón, Susana; Sánchez-Reyes, Luna L.; Gómez-Acevedo, Sandra L.
  • Annals of Botany, Vol. 123, Issue 3
  • DOI: 10.1093/aob/mcy182

RPANDA : an R package for macroevolutionary analyses on phylogenetic trees
journal, November 2015

  • Morlon, Hélène; Lewitus, Eric; Condamine, Fabien L.
  • Methods in Ecology and Evolution, Vol. 7, Issue 5
  • DOI: 10.1111/2041-210X.12526

Can we build it? Yes we can, but should we use it? Assessing the quality and value of a very large phylogeny of campanulid angiosperms
journal, March 2018

  • Beaulieu, Jeremy M.; O'Meara, Brian C.
  • American Journal of Botany, Vol. 105, Issue 3
  • DOI: 10.1002/ajb2.1020

The global diversity of birds in space and time
journal, October 2012


Past, future, and present of state-dependent models of diversification
journal, May 2016

  • O'Meara, Brian C.; Beaulieu, Jeremy M.
  • American Journal of Botany, Vol. 103, Issue 5
  • DOI: 10.3732/ajb.1600012

Estimating Diversification Rates on Incompletely Sampled Phylogenies: Theoretical Concerns and Practical Solutions
journal, December 2019

  • Chang, Jonathan; Rabosky, Daniel L.; Alfaro, Michael E.
  • Systematic Biology, Vol. 69, Issue 3
  • DOI: 10.1093/sysbio/syz081

The age and diversification of the angiosperms re-revisited
journal, August 2010

  • Bell, Charles D.; Soltis, Douglas E.; Soltis, Pamela S.
  • American Journal of Botany, Vol. 97, Issue 8
  • DOI: 10.3732/ajb.0900346

IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies
journal, November 2014

  • Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt
  • Molecular Biology and Evolution, Vol. 32, Issue 1
  • DOI: 10.1093/molbev/msu300

How many species of seed plants are there?
journal, November 2001


geiger v2.0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees
journal, April 2014


Phylogenetic approaches for studying diversification
journal, February 2014


treePL: divergence time estimation using penalized likelihood for large phylogenies
journal, August 2012


RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


Absolute Diversification Rates in Angiosperm Clades
journal, September 2001


From algae to angiosperms–inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes
journal, January 2014

  • Ruhfel, Brad R.; Gitzendanner, Matthew A.; Soltis, Pamela S.
  • BMC Evolutionary Biology, Vol. 14, Issue 1
  • DOI: 10.1186/1471-2148-14-23

How Well Can We Estimate Diversity Dynamics for Clades in Diversity Decline?
journal, May 2018

  • Burin, Gustavo; Alencar, Laura R. V.; Chang, Jonathan
  • Systematic Biology, Vol. 68, Issue 1
  • DOI: 10.1093/sysbio/syy037

Slowdowns in Diversification Rates from Real Phylogenies May Not be Real
journal, June 2010


Challenges of comprehensive taxon sampling in comparative biology: Wrestling with rosids
journal, March 2018

  • Folk, Ryan A.; Sun, Miao; Soltis, Pamela S.
  • American Journal of Botany, Vol. 105, Issue 3
  • DOI: 10.1002/ajb2.1059

Estimating Trait-Dependent Speciation and Extinction Rates from Incompletely Resolved Phylogenies
journal, October 2009

  • FitzJohn, Richard G.; Maddison, Wayne P.; Otto, Sarah P.
  • Systematic Biology, Vol. 58, Issue 6
  • DOI: 10.1093/sysbio/syp067

Constructing a broadly inclusive seed plant phylogeny
journal, February 2018

  • Smith, Stephen A.; Brown, Joseph W.
  • American Journal of Botany, Vol. 105, Issue 3
  • DOI: 10.1002/ajb2.1019

Macroevolutionary diversification rates show time dependency
journal, March 2019

  • Henao Diaz, L. Francisco; Harmon, Luke J.; Sugawara, Mauro T. C.
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 15
  • DOI: 10.1073/pnas.1818058116

Global priorities for conserving the evolutionary history of sharks, rays and chimaeras
journal, January 2018

  • Stein, R. William; Mull, Christopher G.; Kuhn, Tyler S.
  • Nature Ecology & Evolution, Vol. 2, Issue 2
  • DOI: 10.1038/s41559-017-0448-4

Phylogeny of the Ants: Diversification in the Age of Angiosperms
journal, April 2006


RevBayes: Bayesian Phylogenetic Inference Using Graphical Models and an Interactive Model-Specification Language
journal, May 2016

  • Höhna, Sebastian; Landis, Michael J.; Heath, Tracy A.
  • Systematic Biology, Vol. 65, Issue 4
  • DOI: 10.1093/sysbio/syw021

Epiphytic leafy liverworts diversified in angiosperm-dominated forests
journal, August 2014

  • Feldberg, Kathrin; Schneider, Harald; Stadler, Tanja
  • Scientific Reports, Vol. 4, Issue 1
  • DOI: 10.1038/srep05974

A metacalibrated time‐tree documents the early rise of flowering plant phylogenetic diversity
journal, December 2014

  • Magallón, Susana; Gómez‐Acevedo, Sandra; Sánchez‐Reyes, Luna L.
  • New Phytologist, Vol. 207, Issue 2
  • DOI: 10.1111/nph.13264

Phyx: phylogenetic tools for unix
journal, February 2017


Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates
journal, July 2009

  • Alfaro, M. E.; Santini, F.; Brock, C.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 32
  • DOI: 10.1073/pnas.0811087106

Phylogeny of the Rosidae : A dense taxon sampling analysis: Phylogeny of the Rosidae
journal, July 2016

  • Sun, Miao; Naeem, Rehan; Su, Jun-Xia
  • Journal of Systematics and Evolution, Vol. 54, Issue 4
  • DOI: 10.1111/jse.12211

A roadmap for global synthesis of the plant tree of life
journal, March 2018

  • Eiserhardt, Wolf L.; Antonelli, Alexandre; Bennett, Dominic J.
  • American Journal of Botany, Vol. 105, Issue 3
  • DOI: 10.1002/ajb2.1041

A simple polytomy resolver for dated phylogenies: Resolving polytomies under a birth-death model
journal, March 2011


Positive association between population genetic differentiation and speciation rates in New World birds
journal, May 2017

  • Harvey, Michael G.; Seeholzer, Glenn F.; Smith, Brian Tilston
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 24
  • DOI: 10.1073/pnas.1617397114

Plastid phylogenomic analysis of green plants: A billion years of evolutionary history
journal, March 2018

  • Gitzendanner, Matthew A.; Soltis, Pamela S.; Wong, Gane K. -S.
  • American Journal of Botany, Vol. 105, Issue 3
  • DOI: 10.1002/ajb2.1048

APE: Analyses of Phylogenetics and Evolution in R language
journal, January 2004


Is BAMM Flawed? Theoretical and Practical Concerns in the Analysis of Multi-Rate Diversification Models
journal, February 2017

  • Rabosky, Daniel L.; Mitchell, Jonathan S.; Chang, Jonathan
  • Systematic Biology, Vol. 66, Issue 4
  • DOI: 10.1093/sysbio/syx037

The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae)
journal, March 2016

  • Lagomarsino, Laura P.; Condamine, Fabien L.; Antonelli, Alexandre
  • New Phytologist, Vol. 210, Issue 4
  • DOI: 10.1111/nph.13920

Likelihood of Tree Topologies with Fossils and Diversification Rate Estimation
journal, April 2017

  • Didier, Gilles; Fau, Marine; Laurin, Michel
  • Systematic Biology, Vol. 66, Issue 6
  • DOI: 10.1093/sysbio/syx045

A 4000-species dataset provides new insight into the evolution of ferns
journal, December 2016


Inferring Speciation and Extinction Rates under Different Sampling Schemes
journal, April 2011

  • Hohna, S.; Stadler, T.; Ronquist, F.
  • Molecular Biology and Evolution, Vol. 28, Issue 9
  • DOI: 10.1093/molbev/msr095

Tip rates, phylogenies and diversification: What are we estimating, and how good are the estimates?
journal, February 2019

  • Title, Pascal O.; Rabosky, Daniel L.
  • Methods in Ecology and Evolution, Vol. 10, Issue 6
  • DOI: 10.1111/2041-210X.13153

Ferns in an Angiosperm World: Cretaceous Radiation into the Epiphytic Niche and Diversification on the Forest Floor
journal, July 2012

  • Watkins, J. E.; Cardelús, Catherine L.
  • International Journal of Plant Sciences, Vol. 173, Issue 6
  • DOI: 10.1086/665974

Rosid radiation and the rapid rise of angiosperm-dominated forests
journal, February 2009

  • Wang, H.; Moore, M. J.; Soltis, P. S.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 10
  • DOI: 10.1073/pnas.0813376106

Comparing the rates of speciation and extinction between phylogenetic trees
journal, May 2018


Diversity-dependence brings molecular phylogenies closer to agreement with the fossil record
journal, October 2011

  • Etienne, Rampal S.; Haegeman, Bart; Stadler, Tanja
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 279, Issue 1732
  • DOI: 10.1098/rspb.2011.1439

Testing macro–evolutionary models using incomplete molecular phylogenies
journal, November 2000

  • Pybus, Oliver G.; Harvey, Paul H.
  • Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 267, Issue 1459
  • DOI: 10.1098/rspb.2000.1278