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5 Molecular Taxonomy and Phylogeny 5 Molecular Taxonomy and Phylogeny Byron J. Adams1, Adler R. Dillman2 and Camille Finlinson1 1Brigham Young University, Provo, Utah, USA; 2California Institute of Technology, Pasadena, California, USA 5.1. Introduction 119 5.2. The History of Reconstructing Meloidogyne Phylogenetic History 119 5.3. Molecular Phylogenetics: Genetic Markers and Evolutionary Relationships 120 5.4. A Meloidogyne Supertree Analysis 127 5.5. Conclusions and Future Directions 130 5.6. References 135 5.1. Introduction cies descriptions) and, subsequently, phylogenetic analyses. As molecular markers increasingly dem- The genus Meloidogyne contains over 90 described onstrated improved resolving power, they became species and each of these species typically has an more commonplace as diagnostic tools, eventually extremely broad host range (as many as 3000 becoming more prominent as parts of formal plant species; Trudgill and Blok, 2001). In add- taxonomic statements (including descriptions of ition to their host-range diversity, they also exhibit new species) and phylogenetic analyses (e.g. tremendous cytogenetic variation (aneuploidy and Castillo et al., 2003; Landa et al., 2008). With the polyploidy) and mode of reproduction (from incorporation of molecular sources of characters obligatory amphimixis to meiotic and mitotic par- and refinements to phylogenetic theory, the fields thenogenesis) (Triantaphyllou, 1985; see Chitwood of taxonomy and evolutionary biology have now and Perry, Chapter 8, this volume). In current become more completely integrated as a dis- practice, identification of species is based primar- cipline, such that the terms molecular taxonomy ily on the morphological features of females, and phylogenetics are (or should be) subsumed as males and second-stage juveniles (Eisenback and a single research programme (systematics). In this Triantaphyllou, 1991; see Hunt and Handoo, chapter we present a summary of early and con- Chapter 3, this volume), as well as esterase and temporary research on the molecular systematics malate dehydrogenase isozyme profiles derived of Meloidogyne. from single females by polyacrylamide gel elecro- phoresis (Esbenshade and Triantaphyllou, 1985, 1990; Carneiro et al., 2000) and DNA-based bar- 5.2. The History of Reconstructing codes (Powers and Harris, 1993; Powers, 2004; Meloidogyne Phylogenetic History Powers et al., 2005; see Blok and Powers, Chapter 4, this volume). Historically, the diagnostic fea- Some of the earliest work on evolutionary relation- tures deemed most valuable for identification ships among species of Meloidogyne was based on commonly preceded their use as important char- morphological characteristics and relied heavily on acters for taxonomic statements (such as new spe- many of the characters used for identification ©CAB International 2009. Root-knot Nematodes (eds R.N. Perry, M. Moens and J.L. Starr) 119 PPerry_Chap-05.indderry_Chap-05.indd 111919 66/15/2009/15/2009 33:28:26:28:26 PPMM 120 B. Adams et al. (Eisenback and Triantaphyllou, 1991). Subsequent monly explained as lineage sorting among mito- efforts involved cytogenetics (Triantaphyllou, 1966, chondrial haplotypes, but, in addition, paralogous 1985), producing evidence that supported hypo- genes, such as would be expected for the rDNA theses consistent with the idea that mitotic tandem array if intraspecific concerted evolution parthenogens evolved from meiotic parthenoge- were non-uniform, or non-orthologous genes go netic ancestors, following suppression of mei- undetected (Maddison, 1997; Maddison and otic processes and establishing various ploidy Knowles, 2006). Phylogenomic analyses hold the levels. Triantaphyllou also hypothesized that the promise of resolving problematic phylogenies by amphimictic species in the genus, such as Meloidogyne swamping the data sets with signal, despite high exigua, are highly specialized parasites and should noise, by including character information from not be considered as ancestral forms (Triantaphyllou, numerous loci (Eisen, 1998; Eisen and Fraser, 1985). Cytogenetic studies, followed by protein 2003), but see Longhorn et al. (2007). Although and DNA analyses, implied a unique origin of, and phylogenomic analyses that could exhaustively monophyly among, the ameiotic species (Dickson sample all Meloidogyne are premature (if not unnec- et al., 1971; Dalmasso and Bergé, 1978; Esbenshade essary), in a preliminary effort of this kind Scholl and Triantaphyllou, 1987; Castagnone-Sereno and Bird (2005) identified numerous putative et al., 1993; Baum et al., 1994; van der Beek et al., homologues and used them to generate a phylog- 1998). Later, studies based on mitochondrial genes eny for a subset of Meloidogyne species. Although soon revealed that mitochondrial genes can be this effort was based on a small sample of taxa, the hypervariable, both in patterns of sequence substi- major contribution was the elucidation of relation- tution and in gene content and arrangement ships among three mitotic parthenogens (M. hapla, (Powers and Sandall, 1988; Powers et al., 1993). M. incognita, M. javanica) that had been poorly These properties are desirable for diagnostic or resolved in previous phylogenetic analyses. population genetic markers, or for resolving phylo- Subsequent refinements to Meloidogyne phylogeny genetic relationships among closely related species have consisted primarily of analyses that have (see Blok and Powers, Chapter 4, this volume). added new or previously unsampled taxa to exist- More recent phylogenetic analyses have utilized ing databases (Castillo et al., 2003; Landa et al., small ribosomal subunit (18S) rDNA sequences 2008). (De Ley et al., 2002), large subunit (28S) rDNA (Castillo et al., 2003), and mitochondrial DNA (mtDNA) sequences (Tigano et al., 2005). Lunt 5.3. Molecular Phylogenetics: (2008) performed separate analyses of four genes – Genetic Markers and Evolutionary dystrophin, elongation factor 1-alpha, major sperm protein, and RNA polymerase 2 – as part of a Relationships clever study to elucidate whether the origin of the asexual Meloidogyne lineages was ancient or recent 5.3.1 Nuclear Ribosomal DNA Sequences (Adams and Powers, 1996; Hugall et al., 1999). A phenomenon that emerges from each of these Nuclear ribosomal DNA is currently the most studies is the close relationships among the three extensively employed molecular marker for major mitotic parthenogenetic species: Meloidogyne Meloidogyne molecular systematics. Variation in arenaria, Meloidogyne javanica and Meloidogyne incognita. mutation rates observed among different genes Regardless of the type of phylogenetic analysis per- and spacers within an rDNA transcription unit formed, or the genetic locus examined, the pre- results in regions of adjacent DNA segments in ponderance of evidence from single gene analyses the cistron that are useful across a wide range of suggests that the mitotic parthenogens are clearly taxonomic hierarchical levels (Hillis and Dixon, evolutionarily distinct from either the meiotic or 1991). This includes conserved and variable obligatory amphimictic species. However, gene regions of the 18S and 28S subunits, and the trees are not always concordant with the evolution- more highly variable ITS region. These three ary history of independently evolving species, and rRNA gene regions are the most commonly used the discordance between the two different histories genetic markers for nematode molecular system- can confound phylogenetic inference. Discordance atics, and each of these regions has been employed between gene trees and species trees is most com- for Meloidogyne phylogenetics (Landa et al., 2008). PPerry_Chap-05.indderry_Chap-05.indd 112020 66/15/2009/15/2009 33:28:26:28:26 PPMM Molecular Taxonomy and Phylogeny 121 Whilst rRNA genes may provide optimal lev- bases, De Ley et al. (2002) were the first to use els of variation for investigating Meloidogyne phy- this locus as part of a rigorous reconstruction of logeny, they are not without significant theoretical Meloidogyne phylogeny. Their analysis included 12 and analytical drawbacks. The single biggest obs- species of Meloidogyne and four outgroup taxa tacle in using rRNA genes is that, unlike protein- subject to phylogenetic analyses generated from coding genes, they are not constrained to maintain three different multiple sequence alignment codon fidelity or even an open reading frame. methodologies and three different tree-building Whereas the length and composition of protein- optimality criteria (distance, parsimony and max- coding genes are generally subject to selection by imum likelihood). Calculations of phylogenetic codon usage, rRNA genes are not. Thus, for some signal (skewness of tree length distribution) were rDNA regions, insertion and deletion events high and intraspecific sequence polymorphism (indels) can be as frequent as transitions and trans- low, suggesting that the locus was appropriately versions, often involving blocks of multiples of robust for resolving relationships among the sam- nucleotides (Powers, 2004; Powers et al., 1997). pled species but with nodal support strongest at Indel events can result in substantial rDNA size the deeper nodes. Their analysis showed strong differences between sequences (taxa), which com- support for three clades, which they designated: plicates the process of generating multiple sequence clade I, conscribing the mitotic parthenogens alignments and reduces confidence in the hom- (M. incognita, M. arenaria and M. javanica); clade II, ology statements for each
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