Paraphyly and the Species Concept, a Reply to Ebach &

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Paraphyly and the Species Concept, a Reply to Ebach & TAXON 56 (3) • August 2007: 642–644 Letters to the editor Paraphyly and the species concept, a reply to Ebach & al. Several recent Letters to the Editor and other Taxon modification. But, following Alexander’s (2006) argu- papers have questioned the evolutionary base of modern ments, descent of what, and exactly what is modified? phylogenetics (Alexander, 2006; Hörandl, 2006, 2007), Traditional classification is a best attempt at designating promoted the use of paraphyly in classification when as basic units of taxonomy, groups of populations with appropriate (Sosef, 1997; Brummitt & Sosef, 1998; similar phenotype, reproductive behavior, and manner Brummitt, 2003, 2006; Dias & al., 2005; Nordal & Stedje, of interaction with the environment (“biorole”). Morpho- 2005), or downgraded the primacy of molecularly based logical traits are important in traditional classification classifications (Lee, 2006). Others have provided rebut- when they are very unusual or differentially functional. tals (Nelson & al., 2003; Potter & Freudenstein, 2005; Phylogenetic analysis, however, has introduced three new Williams & al., 2005; Ebach & al., 2006). My comments concepts of taxa (presented as OTUs in cladograms), generally support aspects of what has been written critical based on evidence from either morphology, nuclear DNA, of modern phylogenetics and its use in classification, but or organellar DNA. also expand on questioning the value of monophyly itself (1) Phylogenetic analysis of morphology produces when used to extend an inferred genealogy to concepts a parsimonious tree involving potentially all apparently of taxa. independent traits of all taxa in the dataset. What de- The traditional species concept is commonly ac- scends is not the traditional species but a construct based cepted as tripartite: (1) a biological species concept that on all traits used in the tree. Evolutionary modification is appropriate for well-studied species, like birds, with a is expressed by a series of morphological state changes distinct gene pool or potentially interbreeding populations extracted from a miscellany of traits, which may or may and generally clearly marked morphological differences not have selective advantages. Note here that if there are associated with habitat, but is problematic in cryptic spe- surviving ancestors, any morphological autapomorphy cies; (2) an ecological species concept (van Valen, 1976; needs to be regarded as a synapomorphy with reversal or Andersson, 1990, 1992; Bremer & Eriksson, 1992) that change in the sister taxon, an increase in tree length with is appropriate for organisms that may or may not have no change in topology. All but one terminal taxon can be, interbreeding populations but, when taken as a unit, have theoretically, a surviving ancestor. essentially identical morphotypes, reproductive strategies, (2) Phylogenetic analysis of nuclear DNA tracks and environmental preferences and interactions; and (3) phylogeny by assuming the biological species concept an “alpha taxonomic” concept appropriate for species that and asking the question: “Of any three OTUs, which are expected by experts to eventually fit a biological or two probabilistically share a most recent event of genetic ecological species concept when better studied. All three isolation?” With any event of isolation, neutral mutations concepts provide basic taxonomic units that react alike in accumulate in both the newly isolated population and the experimental studies or in nature and are of practical use ancestral population. The two changing populations may in science (Raven, 1974). be called “sister taxa” as they arise from the inferred con- The ecological species concept as basic taxonomic dition of the ancestral population prior to the split. This unit is not the same as the basic evolutionary unit, which is implies monophyly involving three taxa, two new sister usually considered to be one population as affected by the taxa and the ancestral taxon when the latter did not disap- fitness of its individuals due to (1) selection (selectionistic pear (Hörandl, 2006). The OTU, representing that which interpretation of evolution; e.g., Gillespie, 1991; Pianka, descends, is either a continuously and gradually mutating 2000), or (2) rapid decline in population size (bottleneck- ancestral line or the separately mutating newly isolated ing) followed by genetic drift that changes relative numbers lineage. Phenotypic interactions with the environment are of mutations in the population (neutralistic interpretation not tracked except as miscellaneous morphological traits of evolution; e.g., Nei, 2005). The second interpretation mapped on the molecular tree. The OTU does not represent is supported by the recent discovery of massive though the traditional species but a freely interbreeding popula- gradual changes in apparently neutral DNA bases over tion, in which any recombinant mutation may merge with time, suggesting that selection may be less important than other lines in the gene pool. Populations of the species that neutral exon changes in affecting the phenotype. are genetically isolated though remaining nearly identical The selectionistic and neutralistic theories of evo- in phenome and niche are not evaluated or are considered lution have bearing on the different approaches to clas- different, cryptic species. In classification, they must be sification and the paraphyly debate. It is reasonable to named as separate lineages, otherwise monophyly and the assume that classifications should reflect descent with biological species concept are not respected. 1 Letters to the editor TAXON 56 (3) • August 2007: 642–644 (3) Phylogenetic analysis of matrilineally inherited combing through all evidence and rigorous testing. Eval- loci of organellar, chloroplast and mitochondrial DNA, uation of descent with modification involving functional involves separately mutating descendents of an individual. evolution is a difficult and intellectually taxing study All progeny accumulate neutral mutations without recom- (e.g., Robinson, 1990; Hearn, 2006), while phylogenetic bination and are tracked as to their pedigree. The OTU in analysis, perhaps with morphology mapped to the mo- this case does not represent the traditional taxon but an lecular tree, is relatively easy. Even if many organismal inferred line of descent of individuals genetically isolated structures have unknown function, the morphology as by birth. Using loci at a high enough rate of mutation, clue to phenome/environment interaction should charac- any individual as OTU may be termed a basic unit of terize the taxon. Although the analysis of evolutionary classification, reflecting a kind of fractal speciation. and developmental process has been accused of being as- Although the results of the phylogenetic analyses sumption- and theory-laden (e.g., Cracraft, 2005), testing would, of course, be of value in creating a classification theory is the foundation of science. Hörandl (2007) gave reflecting descent with modification of, for instance, a fine comparison of the major features distinguishing inferred bioroles, none directly track bioroles. Molecular cladistic and evolutionary classification. techniques, focusing largely on evolutionarily neutral or According to Blomberg (1987), there are two ap- nearly neutral nucleotide base changes that occur in all proaches to historical criticism: evidentialism and presup- lineages, cannot distinguish between surviving ancestors positionalism. The evidentialist applies accepted historical and new lineages with different functional evolution, nor criteria to demonstrate reliability. The presuppositionalist can they deal directly with intraspecific genetic isolation. first assumes reliability of data and method, then attempts Given that new taxa may arise out of any population, and, to show that the data and method generate a consistent given that there may be much phylogenetic structure in, whole, confirming the presuppositions. It is the consistent at least, plant taxa, then most newly evolved taxa must whole of the cladogram, being the internal simplicity of be phylogenetically embedded within a larger ancestral phylogeny isolated from evolutionary theory, that has taxon. Most speciation must therefore involve paraphyly. been substituted for efforts at understanding evolution By extension, paraphyly must be expected among genera that systematists tragically abandoned thirty years ago, and families. For species consisting of many populations, namely “biosystematics” associated with the Modern the patristic distance between two isolated populations Synthesis. The problem is global in that the evolution- of that species may in fact be greater than that between ary dimension in systematics should allow biodiversity one of these and a new species originating from a third studies to follow and to some extent predict changes in population. niches and the taxa that fill them. This is not the case Given that OTUs resulting from analysis of morphol- with systematics now often defined as phylogenetics with ogy, nuclear DNA, or organellar DNA represent three dif- applications in classification. ferent hypothetical descending entities (apples, oranges, In sum, monophyly is convenient for developing a lemons) and changing traits, combining all data as “total simple, artificial classification from dichotomous trees of evidence” yields OTUs that represent no clear hypotheses a medley of morphological traits parsimoniously distrib- of what is descending and what is being modified
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