title: Phylogeny and the inference of evolutionary trajectories.
abstract: Most important organismal adaptations are not actually single traits, but complex trait syndromes that are evolutionarily integrated into a single emergent phenotype. Two alternative photosynthetic pathways, C4 photosynthesis and crassulacean acid metabolism (CAM), are primary plant adaptations of this sort, each requiring multiple biochemical and anatomical modifications. Phylogenetic methods are a promising approach for teasing apart the order of character acquisition during the evolution of complex traits, and the phylogenetic placement of intermediate phenotypes as sister taxa to fully optimized syndromes has been taken as good evidence of an 'ordered' evolutionary trajectory. But how much power does the phylogenetic approach have to detect ordered evolution? This study simulated ordered and unordered character evolution across a diverse set of phylogenetic trees to understand how tree size, models of evolution, and sampling efforts influence the ability to detect an evolutionary trajectory. The simulations show that small trees (15 taxa) do not contain enough information to correctly infer either an ordered or unordered trajectory, although inference improves as tree size and sampling increases. However, even when working with a 1000-taxon tree, the possibility of inferring the incorrect evolutionary model (type I/type II error) remains. Caution is needed when interpreting the phylogenetic placement of intermediate phenotypes, especially in small lineages. Such phylogenetic patterns can provide a line of evidence for the existence of a particular evolutionary trajectory, but they should be coupled with other types of data to infer the stepwise evolution of a complex character trait.
authors.affiliation: Department of Ecology and Evolutionary Biology, Brown University, Box G-W, 80 Waterman St, Providence, RI 02912, USA Lillian_Hancock@brown.edu.
authors.forename: Lillian
authors.initials: L
authors.lastname: Hancock
authors.affiliation: Department of Ecology and Evolutionary Biology, Brown University, Box G-W, 80 Waterman St, Providence, RI 02912, USA.
authors.forename: Erika J
authors.initials: EJ
authors.lastname: Edwards
mesh_terms: D005075:Biological Evolution; D003198:Computer Simulation; D008962:Models, Theoretical; D010641:Phenotype; D010788:Photosynthesis / Q000235:genetics*; D010802:Phylogeny; D014197:Trees / Q000145:classification / Q000235:genetics* / Q000502:physiology
keywords: C4 photosynthesis; crassulacean acid metabolism; evolution; intermediate phenotypes; phylogenetic approach; phylogeny.
references.citation: Trends Ecol Evol. 2010 Jul;25(7):403-9
references.pmid: 20605250
references.citation: Cell. 2013 Jun 20;153(7):1579-88
references.pmid: 23791184
references.citation: J Exp Bot. 2012 Oct;63(17):6297-308
references.pmid: 23077201
references.citation: Ann Bot. 2004 Jun;93(6):629-52
references.pmid: 15150072
references.citation: Plant Cell Environ. 2007 Oct;30(10):1337-45
references.pmid: 17727423
references.citation: Funct Plant Biol. 2002 Jun;29(6):775-785
references.pmid: 32689525
references.citation: J Exp Bot. 2002 Apr;53(369):569-80
references.pmid: 11886877
references.citation: Bioinformatics. 2008 Jan 1;24(1):129-31
references.pmid: 18006550
references.citation: Mol Biol Evol. 2009 Aug;26(8):1909-19
references.pmid: 19461115
references.citation: Science. 1983 May 27;220(4600):947-9
references.pmid: 17816018
references.citation: J Exp Bot. 2014 Jul;65(13):3609-21
references.pmid: 24638902
references.citation: J Exp Bot. 2008;59(7):1829-40
references.pmid: 18440928
references.citation: Annu Rev Plant Biol. 2012;63:19-47
references.pmid: 22404472
references.citation: New Phytol. 2004 Feb;161(2):341-370
references.pmid: 33873498
references.citation: Science. 1974 Jun 7;184(4141):1087-9
references.pmid: 17736195
references.citation: Plant Physiol. 1991 Aug;96(4):1118-24
references.pmid: 16668307
references.citation: Am J Bot. 2005 Nov;92(11):1911-28
references.pmid: 21646108
references.citation: Plant Physiol. 2001 Dec;127(4):1439-48
references.pmid: 11743087
references.citation: Plant J. 2007 Sep;51(5):886-96
references.pmid: 17692080
references.citation: Plant Physiol. 1984 Mar;74(3):557-61
references.pmid: 16663460
references.citation: Evolution. 2011 Mar;65(3):643-60
references.pmid: 20955197
references.citation: BMC Bioinformatics. 2006 Feb 23;7:88
references.pmid: 16504105
references.citation: Plant Physiol. 1973 Nov;52(5):427-30
references.pmid: 16658576
references.citation: Am J Bot. 2013 Dec;100(12):2388-402
references.pmid: 24259525
references.citation: Bioinformatics. 2004 Jan 22;20(2):289-90
references.pmid: 14734327
references.citation: Elife. 2013 Sep 28;2:e00961
references.pmid: 24082995