American Journal of Botany 91 10 1700 1708 2004 RECONSTRUCTING PATTERNS OF RETICULATE EVOLUTION IN PLANTS1 C RANDAL LINDER2 4 LOREN H RIESEBERG3 AND Section of Integrative Biology and the Center for Computational Biology and Bioinformatics University of Texas Austin 1 University Station A6700 Austin Texas 78712 USA and 3Department of Biology Jordan Hall Indiana University Bloomington Indiana 47405 USA 2 Until recently rigorously reconstructing the many hybrid speciation events in plants has not been practical because of the limited number of molecular markers available for plant phylogenetic reconstruction and the lack of good biologically based methods for inferring reticulation network events This situation should change rapidly with the development of multiple nuclear markers for phylogenetic reconstruction and new methods for reconstructing reticulate evolution These developments will necessitate a much greater incorporation of population genetics into phylogenetic reconstruction than has been common Population genetic events such as gene duplication coupled with lineage sorting and meiotic and sexual recombination have always had the potential to affect phylogenetic inference For tree reconstruction these problems are usually minimized by using uniparental markers and nuclear markers that undergo rapid concerted evolution Because reconstruction of reticulate speciation events will require nuclear markers that lack these characteristics effects of population genetics on phylogenetic inference will need to be addressed directly Current models and methods that allow hybrid speciation to be detected and reconstructed are discussed with a focus on how lineage sorting and meiotic and sexual recombination affect network reconstruction Approaches that would allow inference of phylogenetic networks in their presence are suggested Key words gene tree species tree hybrid speciation phylogenetics polyploidy population genetics recombination Phylogenetic trees are the main tool for representing evolutionary relationships among biological entities at the level of species and above Biologists mathematicians statisticians and computer scientists have developed a variety of methods for reconstructing these events with the usual model being a phylogenetic tree Over the last 30 years biologists have come to embrace reconstruction of phylogenetic trees as a major research goal Hillis 1997 Huelsenbeck et al 1997 Felsenstein 2001 with the ultimate aim of inferring the evolutionary relationships of all of the extant and whenever possible fossil species on the earth Soltis and Soltis 2001 Bininda Emonds et al 2002 Watanabe 2002 Phylogenetics because it reflects the history of transmission of life s genetic information has unique power to organize our knowledge of diverse organisms genomes and molecules beyond merely providing the order and timing of speciation events A reconstructed phylogeny helps guide interpretation of the evolution of organismal characteristics providing hypotheses about the lineages in which traits arose and under what circumstances thus playing a vital role in studies of adaptation and evolutionary constraints e g Felsenstein 1985 Maddison 1990 Martins 1995 Liberles et al 2001 Merritt and Quattro 2001 Phylogenetic trees also help elucidate patterns and dynamics of speciation and to some extent extinction when fossil data are available Futuyma 1998 Carroll et al 2001 In the second half of the twentieth century trees were inferred primarily from morphological characters but in the last decade or so DNA sequences have become the primary data for phylogenetic inference DNA sequences have a number of advantages in phylogenetic reconstruction but they are not Manuscript received 26 December 2003 revision accepted 22 June 2004 The authors thank Lucinda McDade Jeff Palmer and one anonymous reviewer for their constructive comments on this paper and the NSF CRL LHR and NIH LHR for funding to study hybrid speciation 4 E mail rlinder mail utexas edu 1 without their problems Points of strength include presence in nearly all organisms a near perfect guarantee that sequence information is heritable an abundant set of characters for reconstruction sequences that evolve at different rates and good models of sequence evolution for use in reconstruction On the negative side are potential problems with paralogous sequences aligning sequences so that positional homology of individual nucleotides is maintained and the limited number of character states for nucleotides Hillis et al 1996 Moritz and Hillis 1996 Usually these problems can be dealt with mostly by careful selection of molecules that evolve at appropriate rates and that are either uniparentally inherited or that are known or assumed to undergo rapid concerted evolution Nonetheless the green plant clade of the tree of life has some special characteristics relative to most of the animal and fungal clades that bring some of these problems to the fore and that demand our attention if we are to correctly infer relationships among plants In particular the evolutionary history of plants is not really a tree at all for some taxa Rather it is a network in which there have been a large number of reticulate evolutionary events especially hybrid speciation both polyploid and diploid Stebbins 1950 Grant 1981 Arnold 1997 Otto and 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 have chosen the wrong genes but because the history of life cannot properly be represented as a tree Routine reconstruction of hybrid speciation in the manner of phylogenetic trees for example 1 searches of alternative reconstructions using optimality criteria and algorithms or heuristics with explicit evolutionary models 2 extensive testing of methods on large sets of simulated phylogenies and 3 parametric and nonparametric methods for assessing support for particular solutions requires special methods that are as yet largely unavailable Moreover unlike tree reconstruction numerous independently inherited sequences are required for 1700 October 2004 LINDER AND RIESEBERG RETICULATE EVOLUTION IN PLANTS 1701 lated from their parent they are more properly considered a specialized form of normal bifurcating speciation because only a single parental species is involved in their production Fig 1 Example of a phylogenetic network with a single hybrid species B Internal
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