1700American Journal of Botany 91(10): 1700–1708. 2004.RECONSTRUCTING PATTERNS OF RETICULATEEVOLUTION IN PLANTS1C. RANDALLINDER2,4ANDLORENH. RIESEBERG32Section of Integrative Biology and the Center for Computational Biology and Bioinformatics, University of Texas–Austin,1 University Station—A6700, Austin, Texas 78712 USA; and3Department of Biology, Jordan Hall, Indiana University,Bloomington, Indiana 47405 USAUntil recently, rigorously reconstructing the many hybrid speciation events in plants has not been practical because of the limitednumber of molecular markers available for plant phylogenetic reconstruction and the lack of good, biologically based methods forinferring reticulation (network) events. This situation should change rapidly with the development of multiple nuclear markers forphylogenetic reconstruction and new methods for reconstructing reticulate evolution. These developments will necessitate a muchgreater incorporation of population genetics into phylogenetic reconstruction than has been common. Population genetic events suchas gene duplication coupled with lineage sorting and meiotic and sexual recombination have always had the potential to affectphylogenetic inference. For tree reconstruction, these problems are usually minimized by using uniparental markers and nuclear markersthat undergo rapid concerted evolution. Because reconstruction of reticulate speciation events will require nuclear markers that lackthese characteristics, effects of population genetics on phylogenetic inference will need to be addressed directly. Current models andmethods that allow hybrid speciation to be detected and reconstructed are discussed, with a focus on how lineage sorting and meioticand sexual recombination affect network reconstruction. Approaches that would allow inference of phylogenetic networks in theirpresence are suggested.Key words: gene tree/species tree; hybrid speciation; phylogenetics; polyploidy; population genetics; recombination.Phylogenetic trees are the main tool for representing evo-lutionary relationships among biological entities at the levelof species and above. Biologists, mathematicians, statisticians,and computer scientists have developed a variety of methodsfor reconstructing these events, with the usual model being aphylogenetic tree. Over the last 30 years, biologists have cometo embrace reconstruction of phylogenetic trees as a majorresearch goal (Hillis, 1997; Huelsenbeck et al., 1997; Felsen-stein, 2001) with the ultimate aim of inferring the evolutionaryrelationships of all of the extant and, whenever possible, fossilspecies on the earth (Soltis and Soltis, 2001; Bininda-Emondset al., 2002; Watanabe, 2002).Phylogenetics, because it reflects the history of transmissionof life’s genetic information, has unique power to organize ourknowledge of diverse organisms, genomes, and molecules be-yond merely providing the order and timing of speciationevents. A reconstructed phylogeny helps guide interpretationof the evolution of organismal characteristics, providing hy-potheses about the lineages in which traits arose and underwhat circumstances, thus playing a vital role in studies of ad-aptation and evolutionary constraints (e.g., Felsenstein, 1985;Maddison, 1990; Martins, 1995; Liberles et al., 2001; Merrittand Quattro, 2001). Phylogenetic trees also help elucidate pat-terns and dynamics of speciation and, to some extent, extinc-tion when fossil data are available (Futuyma, 1998; Carroll etal., 2001).In the second half of the twentieth century, trees were in-ferred primarily from morphological characters, but in the lastdecade or so, DNA sequences have become the primary datafor phylogenetic inference. DNA sequences have a number ofadvantages in phylogenetic reconstruction, but they are not1Manuscript received 26 December 2003; revision accepted 22 June 2004.The authors thank Lucinda McDade, Jeff Palmer, and one anonymous re-viewer for their constructive comments on this paper and the NSF (CRL,LHR) and NIH (LHR) for funding to study hybrid speciation.4E-mail: [email protected] their problems. Points of strength include presence innearly all organisms, a near perfect guarantee that sequenceinformation is heritable, an abundant set of characters for re-construction, sequences that evolve at different rates, and goodmodels of sequence evolution for use in reconstruction. On thenegative side are potential problems with paralogous sequenc-es, aligning sequences so that positional homology of individ-ual nucleotides is maintained, and the limited number of char-acter states for nucleotides (Hillis et al., 1996; Moritz and Hil-lis, 1996). Usually these problems can be dealt with, mostlyby careful selection of molecules that evolve at appropriaterates and that are either uniparentally inherited or that areknown or assumed to undergo rapid concerted evolution.Nonetheless, the green-plant clade of the tree of life has somespecial characteristics relative to most of the animal and fungalclades that bring some of these problems to the fore and thatdemand our attention if we are to correctly infer relationshipsamong plants. In particular, the evolutionary history of plantsis not really a tree at all for some taxa. Rather it is a network,in which there have been a large number of reticulate evolu-tionary events, especially hybrid speciation, both polyploidand diploid (Stebbins, 1950; Grant, 1981; Arnold, 1997; Ottoand Whitton, 2000). As Ford Doolittle (1999, p. 2124) wrote,‘‘Molecular phylogeneticists will [fail] to find the ‘true tree’,not because their methods are inadequate or because they havechosen the wrong genes, but because the history of life cannotproperly be represented as a tree.’’Routine reconstruction of hybrid speciation in the mannerof phylogenetic trees—for example, (1) searches of alternativereconstructions using optimality criteria and algorithms or heu-ristics with explicit evolutionary models, (2) extensive testingof methods on large sets of simulated phylogenies, and (3)parametric and nonparametric methods for assessing supportfor particular solutions—requires special methods that are, asyet, largely unavailable. Moreover, unlike tree reconstruction,numerous independently inherited sequences are required forOctober 2004] 1701LINDER ANDRIESEBERG—RETICULATE EVOLUTION IN PLANTSFig. 1. Example of a phylogenetic network with a single hybrid species(B). Internal branches are numbered to allow the
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