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155
Department of Zoology, The Natural History Museum, Cromwell Rd, London SW7 5BD, U.K.
Division of Life Sciences, Kings College, University of London, London W8 7AH, U.K. ( author for
correspondence)
2
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ing the confusion presented by existing morphological
data (e.g. see Rohde, 1994; Rieger & Tyler, 1995),
and yet, comparing phylogenies derived from independent data sets is by far the most valuable approach
since all available evidence is taken into consideration.
Although, sensu stricto this is not the total-evidence
approach of Kluge (1989), it is certainly one which
involves all phylogenetic data.
Some systematists may be alienated by a molecular phylogeny presented without consideration of its
biological significance, and it is now generally recognised that a morphological versus molecular debate
is redundant and counter-productive (Hillis, 1987;
Miyamoto & Fitch, 1995). In a strict sense, data sets
and their individual characters are of value because
they represent statements about homology, i.e. features supporting similarity by common ancestry or genetic relatedness. Recognising homology is the foundation underlying phylogenetic reconstruction; for an
expansive treatment on homology in morphological
and molecular studies see papers in Hall (1994). Homoplasy, the counterpart of homology, where characters have undergone convergent or parallel evolution,
is the noise which dampens phylogenetic signal. Unfortunately, homoplasious characters are unavoidable
and where the noise they generate is large, we aim
to reduce it by adding more data or by recognising
homoplasious characters and eliminating them from
the analysis. The recognition of homoplasy may be
easier with morphological data (e.g. see Tyler, 1988).
Often it is easier to add more molecular data than
to resolve contention over homologous morphological
characters, although this approach is not necessarily
more productive. Adding new nucleotide data must be
done with care as nucleotide positions can quickly become saturated with change if the nucleotide sequence
is evolving too rapidly and prohibitively expensive
if it is evolving too slowly to generate additional
phylogenetically informative data.
Molecular systematics may hold a key to resolving turbellarian phylogeny but, as Margulis (1996, p.
1074) recently stated, natural selection acts throughout the life-history of all organisms in specific habitats
at given times . . . therefore, whole-organism biology
(including all genetics and metabolism that determines
life cycle) not just molecular sequence must undergird
phylogenetic classification. Both morphological and
molecular data play important roles in phylogenetic
reconstruction but we do not recognise any one technique as a substitute for another. Here we advocate
a total-evidence approach utilising all available data,
157
et al.s (1985b) analysis of the Digenea, and found a
high level of error. Few morphologically based character matrices for flatworm groups have found widespread acceptance and yet authors who publish them
should be praised for presenting data for scrutiny.
For higher-level phylogenies, ultrastructure appears to add much useful data (e.g. sperm morphology,
Watson & Rohde, 1995; protonephridial structure,
Rohde, 1993), although no formalised character matrix has yet been constructed for these data. Watson
& Rohde (1995) warn of various problems with the
current status of our knowledge of sperm ultrastructure. Indeed, our own preliminary analyses with these
characters yield a highly polytomous tree [data from
Table 1 of Watson & Rohde, 1995 analysed with
MacClade (Maddison & Maddison, 1992) and PAUP
(Swofford, 1993); results not shown]. It may well be
that at the ultrastructural level, morphological homology is easier to recognize and score although denser
sampling is still required. In contrast, Tyler (1979)
suggests that homology may be more difficult to establish at the ultrastructural level. As with molecular
data in phylogenetics, morphological data (from the
gross anatomic to the ultrastructural) lend themselves
to use at different taxonomic levels.
What is neededin the future is more phylogenetically centred descriptive work. If it became standard for systematists to include matrices in their
descriptive papers, or at least to deposit them
in a suitable electronic database (e.g. TreeBase;
http://herbaria.harvard.edu/treebase/), then phylogenetic considerations would enter at an early stage,
and the assessment of homologies and character-state
identity be made with specimens at hand. In the meantime it seems incumbent upon the morphologist to
present annotated morphological character matrices
which can be used as a basis for debate and more thorough cladistic analyses. We hope to utilize existing literature to present formal character matrices for analysis and discussion although we realise that turbellarian systematics and the distribution of morphological
features about the phylum are still poorly known.
Molecular data
Choice of taxa
At the moment this manuscript was being prepared (July 1996) there were 2204 nucleotide and
624 protein sequences for Platyhelminthes registered
and available from GenBank (NCBI). Schistosoma
mansoni (Digenea: Strigeidida: Schistosomatida) sequences accounted for over 79% and 44% of the
158
only choice of taxa affects the robustness and topology of trees, but so too does the density of sampled
taxa per presumed monophyletic group and the choice
and sampling of outgroups (Patterson, 1989; Lecointre et al., 1993). Parsimony analysis, for example,
works on the principle of establishing common ancestry through the least number of character changes. To
gain confidence in the tree we should aim to reconstruct common ancestors of the groups in question by
sequencing the clade densely and not relying on single
representatives. In other words, we should be sampling
at a taxonomic category lower than the one that will
make up the tree; e.g., sequence various and distinct
genera for family level resolution, various and distinct
families for order level-resolution, and so on. Ideally,
subsampling any combination of taxa from the clades
under scrutiny will generate the same tree topology,
and as clades are more densely sampled the tree will
become more robust.
A review of molecular phylogenetic studies at
higher taxonomic levels of platyhelminths highlights
the problem of poor species sampling e.g., poor
sampling in Baverstock et al. (1991) and Rohde et al.
(1993) lead to contentious conclusions regarding the
interrelationships of the phylum. Many studies have
involved the sequencing of single species, adding to
small existing data sets and subsequently drawing farreaching conclusions about the orders to which they
belong e.g., Rohde et al. (1994) placing the enigmatic Kronborgia isopodicola, and subsequently the
fecampiid rhabdocoels in a wider phylogenetic context, or a similar attempt by Blair (1993) to place
the aspidobothreans on the basis of a single sequence.
Although these data are unquestionably useful, the
groupings and phylogenetic solutions they support still
need to be tested further with the denser sampling of
key taxa, particularly so that long branches can be split
up.
Choice of gene
There are no hard-and-fast rules for determining the
phylogenetic informativeness of any particular gene
for any particular taxonomic problem. However, the
history of molecular systematics has tended to set
precedents for tackling divergences over different time
scales (e.g. Hillis & Dixon, 1991). Also, more ribosomal RNA gene sequences are available for analysis
than any other gene and it has been more convenient
to add to these data sets. There seem to be no studies comparing or contrasting the phylogenetic utility
159
bases can be scored as purines (R) or pyrimidines (Y).
As with a full alignment, ambiguous positions should
be removed from the analysis.
Consensus sequences reduce the number of taxa
markedly and allow branch-and-bound or even exhaustive searches to be performed. In this way we
can detect phylogenetic signal (Hillis, 1991; Hillis &
Huelsenbeck, 1992), compare the phylogenies of solutions close to the most parsimonious, and bootstrap
all the sequence data more quickly without losing any
signal in the individual sequences that make up the
consensus.
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