Accuracy of ancestral state reconstruction for non-neutral traits.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
06 05 2020
Historique:
received: 04 12 2019
accepted: 09 04 2020
entrez: 8 5 2020
pubmed: 8 5 2020
medline: 8 5 2020
Statut: epublish

Résumé

The assumptions underpinning ancestral state reconstruction are violated in many evolutionary systems, especially for traits under directional selection. However, the accuracy of ancestral state reconstruction for non-neutral traits is poorly understood. To investigate the accuracy of ancestral state reconstruction methods, trees and binary characters were simulated under the BiSSE (Binary State Speciation and Extinction) model using a wide range of character-state-dependent rates of speciation, extinction and character-state transition. We used maximum parsimony (MP), BiSSE and two-state Markov (Mk2) models to reconstruct ancestral states. Under each method, error rates increased with node depth, true number of state transitions, and rates of state transition and extinction; exceeding 30% for the deepest 10% of nodes and highest rates of extinction and character-state transition. Where rates of character-state transition were asymmetrical, error rates were greater when the rate away from the ancestral state was largest. Preferential extinction of species with the ancestral character state also led to higher error rates. BiSSE outperformed Mk2 in all scenarios where either speciation or extinction was state dependent and outperformed MP under most conditions. MP outperformed Mk2 in most scenarios except when the rates of character-state transition and/or extinction were highly asymmetrical and the ancestral state was unfavoured.

Identifiants

pubmed: 32376845
doi: 10.1038/s41598-020-64647-4
pii: 10.1038/s41598-020-64647-4
pmc: PMC7203120
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

7644

Références

Cunningham, C. W., Omland, K. E. & Oakley, T. H. Reconstructing ancestral character states: A critical reappraisal. Trends Ecol. Evol. 13, 361–366 (1998).
pubmed: 21238344
Lemey, P., Rambaut, A., Drummond, A. J. & Suchard, M. A. Bayesian phylogeography finds its roots. Plos Comput. Biol. 5 (2009).
Huelsenbeck, J. P. & Bollback, J. P. Empirical and Hierarchical Bayesian Estimation of Ancestral States. Syst. Biol. 50, 351–366 (2001).
pubmed: 12116580
Hahn, M. W. & Nakhleh, L. Irrational exuberance for resolved species trees. Evolution (N. Y). 70, 7–17 (2015).
Duchêne, S. & Lanfear, R. Phylogenetic uncertainty can bias the number of evolutionary transitions estimated from ancestral state reconstruction methods. J. Exp. Zool. Part B Mol. Dev. Evol. 324, 517–524 (2015).
Yang, Z. Phylogenetic analysis using parsimony and likelihood methods. J. Mol. Evol. 42, 294–307 (1996).
pubmed: 8919881
Schluter, D., Price, T., Mooers, A. Ø. & Ludwig, D. Likelihood of ancestor states in adaptive radiation. Evolution (N. Y). 51, 1699–1711 (1997).
Cunningham, C. W. Some limitations of ancestral character-state reconstruction when testing evolutionary hypotheses. Syst. Biol. 48, 665–674 (1999).
Litsios, G. & Salamin, N. Effects of phylogenetic signal on ancestral state reconstruction. Syst. Biol. 61, 533–538 (2012).
pubmed: 22223447
Rabosky, D. L. Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. Plos One 9 (2014).
Reyes, E., Nadot, S., von Balthazar, M., Schönenberger, J. & Sauquet, H. Testing the impact of morphological rate heterogeneity on ancestral state reconstruction of five floral traits in angiosperms. Sci. Rep. 8, 9473 (2018).
pubmed: 29930308 pmcid: 6013437
King, B. & Lee, M. S. Y. Ancestral State Reconstruction, Rate Heterogeneity, and the Evolution of Reptile Viviparity. Syst. Biol. 64, 532–544 (2015).
pubmed: 25616375
Bokma, F. 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 (N. Y). 62, 2718–2726 (2008).
Ree, R. H. & Smith, S. A. Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Syst. Biol. 57, 4–14 (2008).
pubmed: 18253896
Givnish, T. J. Adaptive significance of evergreen vs. deciduous leaves: Solving the triple paradox. Silva Fenn. 36, 703–743 (2002).
Wiens, J. J., Bonett, R. M. & Chippindale, P. T. Ontogeny discombobulates phylogeny: Paedomorphosis and higher-level salamander relationships. Syst. Biol. 54, 91–110 (2005).
pubmed: 15805013
Holland, B. R., Spencer, H. G., Worthy, T. H. & Kennedy, M. Identifying cliques of convergent characters: Concerted evolution in the cormorants and shags. Syst. Biol. 59 (2010).
Guerrero, R. F. & Hahn, M. W. Quantifying the risk of hemiplasy in phylogenetic inference. Proc. Natl. Acad. Sci. USA 115, 12787–12792 (2018).
pubmed: 30482861
Arenas, M. & Posada, D. The effect of recombination on the reconstruction of ancestral sequences. Genetics 184, 1133–1139 (2010).
pubmed: 20124027 pmcid: 2865913
Arenas, M., Weber, C. C., Liberles, D. A. & Bastolla, U. ProtASR: An Evolutionary Framework for Ancestral Protein Reconstruction with Selection on Folding Stability. Syst. Biol. 66, 1054–1064 (2017).
pubmed: 28057858
Klopfstein, S., Vilhelmsen, L. & Ronquist, F. A Nonstationary Markov Model Detects Directional Evolution in Hymenopteran Morphology. Syst. Biol. 64, 1089–1103 (2015).
pubmed: 26272507 pmcid: 4604834
Berner, R. A. & Kothavala, Z. Geocarb III: A revised model of atmospheric CO
Zachos, J., Pagani, H., Sloan, L., Thomas, E. & Billups, K. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science (80-.). 292, 686–693 (2001).
Hill, R. S. Origins of the southeastern Australian vegetation. Philos. Trans. R. Soc. London Ser. B-Biological Sci. 359, 1537–1549 (2004).
Dunn, R. E., Strömberg, C. A. E., Madden, R. H., Kohn, M. J. & Carlini, A. A. Linked canopy, climate, and faunal change in the Cenozoic of Patagonia. Science (80-.). 347, 258–261 (2015).
Maia, R., Rubenstein, D. R. & Shawkey, M. D. Key ornamental innovations facilitate diversification in an avian radiation. Proc. Natl. Acad. Sci. USA 110, 10687–10692 (2013).
pubmed: 23754395
Vamosi, J. C., Magallón, S., Mayrose, I., Otto, S. P. & Sauquet, H. Macroevolutionary Patterns of Flowering Plant Speciation and Extinction. Annu. Rev. Plant Biol. 69, 685–706 (2018).
pubmed: 29489399
Ng, J. & Smith, S. D. How traits shape trees: new approaches for detecting character state-dependent lineage diversification. J. Evol. Biol. 27, 2035–2045 (2014).
pubmed: 25066512
Maddison, W. P., Midford, P. E. & Otto, S. P. Estimating a binary character’s effect on speciation and extinction. Syst. Biol. 56, 701–710 (2007).
pubmed: 17849325
Fitzjohn, R. G. Quantitative traits and diversification. Syst. Biol. 59, 619–633 (2010).
pubmed: 20884813
Davis, M. P., Midford, P. E. & Maddison, W. Exploring power and parameter estimation of the BiSSE method for analyzing species diversification. BMC Evol. Biol. 13, (2013).
Rabosky, D. L. & Goldberg, E. E. Model Inadequacy and Mistaken Inferences of Trait-Dependent Speciation. Syst. Biol. 64, 340–355 (2015).
pubmed: 25601943
Beaulieu, J. M. & O’Meara, B. C. Detecting Hidden Diversification Shifts in Models of Trait-Dependent Speciation and Extinction. Syst. Biol. 65, 583–601 (2016).
pubmed: 27016728
Goldberg, E. E. & Igić, B. On phylogenetic tests of irreversible evolution. Evolution (N. Y). 62, 2727–2741 (2008).
Wright, A. M., Lyons, K. M., Brandley, M. C. & Hillis, D. M. Which came first: The lizard or the egg? Robustness in phylogenetic reconstruction of ancestral states. J. Exp. Zool. Part B Mol. Dev. Evol. 324, 504–516 (2015).
Gascuel, O. & Steel, M. Predicting the ancestral character changes in a tree is typically easier than predicting the root state. Syst. Biol. 63, 421–435 (2014).
pubmed: 24562915
Lewis, P. O. A likelihood approach to estimating phylogeny from discrete morphological character data. Syst. Biol. 50, 913–925 (2001).
pubmed: 12116640
Ricklefs, R. E. Global diversification rates of passerine birds. Proc. R. Soc. B Biol. Sci. 270, 2285–2291 (2003).
Ricklefs, R. E., Losos, J. B. & Townsend, T. M. Evolutionary diversification of clades of squamate reptiles. J. Evol. Biol. 20, 1751–1762 (2007).
pubmed: 17714293
Fitzjohn, R. G. Diversitree: Comparative phylogenetic analyses of diversification in R. Methods Ecol. Evol. 3, 1084–1092 (2012).
R Core Team. R: A language and environment for statistical computing. (R Foundation for Statistical Computing, Vienna, Austria, 2014).
Tange, O. GNU Parallel: the command-line power tool.;login USENIX Mag., https://doi.org/10.5281/zenodo.16303 (2011).
Paradis, E. et al. Package ‘ape’. (2011).
Hanazawa, M., Narushima, H. & Minaka, N. Generating most parsimonious reconstructions on a tree: A generalization of the Farris-Swofford-Maddison method. Discret. Appl. Math. 56, 245–265 (1995).
Narushima, H. & Hanazawa, M. A more efficient algorithm for MPR problems in phylogeny. Discret. Appl. Math. 80, 231–238 (1997).
Oakley, T. H. & Cunningham, C. W. Independent contrasts succeed where ancestor reconstruction fails in a known bacteriophage phylogeny. Evolution (N. Y). 54, 397–405 (2000).
Pimm, S. L. & Joppa, L. N. How many plant species are there, where are they, and at what rate are they going extinct? Ann. Missouri Bot. Gard. 100, 170–176 (2015).
Beaulieu, J. M., O’Meara, B. C. & Donoghue, M. J. Identifying hidden rate changes in the evolution of a binary morphological character: The evolution of plant habit in campanulid angiosperms. Syst. Biol. 62, 725–737 (2013).
pubmed: 23676760

Auteurs

Barbara R Holland (BR)

School of Natural Sciences, University of Tasmania, Private Bag 55, Hobart, Tas, 7001, Australia. Barbara.Holland@utas.edu.au.

Saan Ketelaar-Jones (S)

School of Natural Sciences, University of Tasmania, Private Bag 55, Hobart, Tas, 7001, Australia.

Aidan R O'Mara (AR)

School of Health Sciences, University of Tasmania, Private Bag 121, Hobart, Tas, 7001, Australia.

Michael D Woodhams (MD)

School of Natural Sciences, University of Tasmania, Private Bag 55, Hobart, Tas, 7001, Australia.

Gregory J Jordan (GJ)

School of Natural Sciences, University of Tasmania, Private Bag 55, Hobart, Tas, 7001, Australia.

Classifications MeSH