It is clear to us that genomic information should be an active component of modern taxonomy, but DNA should not be the sole source of information retrieval. ‘Fashionable DNA bar-coding methods are a breakthrough for identification, but they will not supplant the need to formulate and rigorously test species hypotheses.’ (Wheeler et al. 2004
, p. 285). A barcode should incorporate diagnostic characters both from the classical morphological approach and from the newer molecular approaches; one without the other misses the synergy that an integrated taxonomy is capable of attaining (Godfray 2002
). We see a major strength to an integrated approach in that descriptive taxonomy and phylogenetic taxonomy together produce a synergy of resolution that neither can attain in the current fragmented ‘tower of babel’ (Mallet & Willmott 2003
). It should also be clear that integration of the ‘fashionable’ molecular approaches with the classical taxonomic approach is a critical component of reconciling both camps and to move towards the use of barcodes in modern biology. Consequently we present an operational, integrative approach to taxonomy that attempts to reconcile molecular information with other sources of characters.
(a) The taxonomic circle; breaking out
We offer as a heuristic for how modern taxonomy can be viewed. While any diagram describing the workings of taxonomy would suffer from over-simplification of the intellectual process that taxonomists use in plying their trade, we feel captures many elements of modern taxonomy—hypothesis testing, corroboration, reciprocal illumination and revision. The main problem that needs to be addressed in any attempt to determine the boundary of a species and hence raise the entity to species status is to avoid circular or tautological reasoning. Breaking out of the circle of inference (, central diagram) in species delineation work is one descriptive way to describe the job of the taxonomist and hence the role of DNA sequence information (and barcoding) in taxonomy.
Figure 2 The taxonomic circle. The dotted lines that traverse the inner part of the circle indicate experimental routes that can be taken in taxonomic endeavour to accomplish corroboration of taxonomic hypotheses. The only way to delineate a new taxon is to break (more ...)
shows a highly simplified version of several taxonomic problems that have faced systematists and DNA barcoders. The classical process of using morphology in taxonomy is shown first (, panel A). In this diagram the data points on the ‘taxonomy’ circle consist of geographical, morphological, ecological, reproductive and behavioural information. In most morphological taxonomic studies an initial hypothesis based on geography is made. The taxonomist then crosses over the interior of the circle to either ecological characters or to morphological characters to test the geographical hypothesis. If morphological, behavioural, reproductive or ecological information relevant to the geographical hypothesis assist in rejecting the null hypothesis that there is no differentiation of the two geographical entities, then the taxonomist can ‘break out’ of the circle.
Cryptic species detected by DNA approaches is shown next (, panel B). In this case we add DNA sequence information to the circle. Initially a geographical hypothesis is formulated, a null hypothesis established and tested with the classical tools of the taxonomist. In this case, none of the classical tools—reproductive biology, morphological, behavioural or ecological characters—can reject the null hypothesis. The taxonomist can turn to DNA sequences where the null hypothesis based on geography is rejected because of fixed DNA differences among the aggregates hypothesized by geography. In essence, the aggregates contain morphologically cryptic species that are only detected at the DNA sequence level, which allows the taxonomist to break out of the circle.
The third panel in (panel C) shows the case of lack of ability by all methods to lead to rejection of a geographical null hypothesis. In this case, the putative species entities suggested by geography cannot be corroborated and hence the taxonomist is constrained to remain in the circle. The conclusion by the taxonomist should be that there is a single taxonomic entity. The fourth panel (, panel D) represents the power of integrating novel methods into this operational scheme. In this case, several individuals within a single geographic area show morphological differences. Because these individuals are considered to reside in the same geographic region, a geographical hypothesis cannot be made. But in this case the morphologically different entities can be aggregated and tested for fixed differences with other sources of data. In the case in the diagram, we imply that DNA sequence information can be used and if fixed DNA differences corroborate the morphological hypothesis then the conclusion of the analysis is that two species exist in sympatry and can be delineated by morphological differences.
The converse situation is also possible—a researcher could examine a ‘population’ of organisms with morphology and see no morphological differences. When the genomes of the organism are examined, the researcher might discover a DNA sequence polymorphism that clearly separates the single population into individuals with one haplotype and individuals with a distinct second haplotype. The only way to break out of the circle here would be to re-examine morphology or to move on to some other source of information. If no corroboration of the molecular aggregation can be found then the conclusion should be that a single population with two clearly distinct haplotypes exist. If corroboration is attained, then two distinct entities should be concluded to exist.