The Biology of Nematodes

Donald L Lee, Donald L Lee

• Editorial: CRC Press
• Año: 2002
• ISBN:
  9781134485345
• Edición: 1
• Categoría: Scienze biologiche
• Categoría: Entomologia

The Biology of Nematodes synthesizes literature on free-living, plant-parasitic, and animal-parasitic nematodes. Topics covered include systematics and phylogeny, neuromuscular physiology, locomotion, sense organs, behavior, aging, the nematode genome, survival strategies, immunology, structure and organization, gametes and fertilization, and feeding and metabolism. This volume, the most authoritative available, includes contributions from researchers working on groundbreaking molecular techniques leading to new approaches in the study of nematode worms. It provides an important resource for research scientists working in a number of agricultural, medical, and biological fields.

1.
Systematic Position and Phylogeny

Paul De Ley^*
Vakgroep Biologie, Universiteit Gent, Ledeganckstraat 35, B-9000 Gent,
Belgium

Mark Blaxter
Institute of Cell, Animal and Population Biology, King’s Buildings,
University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK

Keywords

Classification, morphology, sequence analysis, Ecdysozoa, invertebrates, parasitism

Introduction

Nematodes are a highly diverse and very important group of multicellular animals, but their systematics have always been volatile and are currently entering a new phase of turbulence. At the moment of writing this chapter, molecular methods and phylogenetic models are bringing new insights that require significant changes in nematode systematics. To provide an overview at this particular time is therefore both an exciting and impossible challenge, since we can roughly predict the extent of the changes to come, but not yet stipulate their precise form.

Several authors have reviewed the complex history of nematode systematics over the past 150 years, and the many individuals that contributed to it (e.g. Micoletzky, 1921; Andrαssy, 1976; Lorenzen, 1983; Inglis, 1983). In this chapter, we therefore do not attempt to present a comprehensive overview of the many different classifications of nematodes proposed in the past. Rather, we will sketch the history of past phylogenetic frameworks for nematodes, briefly discuss how these phylogenies were translated into classifications, and compare them with the first results from molecular phylogenetic analyses. We will also elaborate a first tentative approximation to a classification based on these molecular analyses, combined with morphological data.

Fundamental questions of organismal classification and phylogenetic inference are continuously being debated in ever-growing numbers of books and journals. These debates are becoming ever more specialised and complex, suggesting that a consensus will not be reached any time soon. Our purpose here is not to add our own voice to the chorus, neither by attempting to establish any purported ‘supremacy’ of molecular phylogenies over morphological data (cf. Moritz and Hillis, 1996 for a sensible assessment), nor by providing the ‘one true and definitive’ classification for nematodes. Irrespective of all debates about the best methods and data, we only wish to demonstrate three practical points:

• There is a substantial degree of overall congruence between morphological and molecular phylogenetic analyses of nematodes.
• Nematode phylogeny is not an intractable problem—although certainly not an easy one either.
• Nematologists must incorporate the latest methods of phylogenetic inference into their repertoire as an integral part of nematode systematics.

We believe the latter point is an essential prerequisite for the continued survival and renewed growth of nematology in the new century (cf. Ferris, 1994). Nematode taxonomy will not be able to assume its proper place within biological systematics unless it catches up with the newest developments of systematic theory and practice, and unless it proves able to estimate nematode diversity, recover nematode relationships, and hierarchically organise nematode classification on a genealogical basis.

The Higher Classification
Nemata or Nematoda?

Taxonomic nomenclature provides the basis for recording and communicating classifications. It is therefore an essential biological tool, but not a fundamental axiom underpinning all inferences and assumptions. We consider it of great importance that systematic hierarchies are proposed, compared and rejected, based on the theoretical and relational framework provided by phylogenetic inference. We consider it far less important which names exactly are assigned to the different taxa occurring within such hierarchies, as long as the great majority of users of any given system will understand which taxon is represented by which name.

A good example of a long-lasting nomenclatorial debate about taxon names in nematodes, is the name of the encompassing taxon itself: Nemata or Nematoda? At present, it is nearly universally agreed that nematodes should indeed be ranked as a phylum, especially now that the older encompassing taxa Aschelminth(e)s or Nemathelminth(e)s are more and more being questioned (see page). Adherents to the name Nemata argue that this was the name used in the first proposal (by Cobb, 1919) of phylum rank for nematodes, and that it should therefore be upheld over the corrupted name Nematoda (Chitwood, 1957, 1958). The latter was a modification of Nematodes as first used at family level by Burmeister (1837), and ultimately derives from Nematoidea, an order- level name originally proposed by Rudolphi (1808). On the other hand (see Steiner, 1960), Nematoda has been in use longer, and the original proposal of the phylum by Cobb (1919) actually introduced the name Nemates, which was only later amended to Nemate by Chitwood (1958).

The International Code for Zoological Nomenclature does not rule on taxon names above family level, and for decisions on name validity at lower levels it applies a combination of both chronological priority (arguably favoring Nematoda) with rank-specificity (arguably favoring Nemata). Hence, there is no obvious official guideline or precedent to be followed—which undoubtedly contributes to the further life of the issue. Since there is no convincing solution in sight, and an ever-growing list of scientifically more interesting questions remain to be answered, we do not wish to devote more time and space to the matter than necessary. We leave it to the reader to apply his or her preferred choice of phylum name as he or she sees fit. In this chapter, we have opted to use the name ‘Nematoda’ only for pragmatic purposes, i.e. due to its older and somewhat more widespread usage.

New Data and Old Questions: The Uncertain Position of Nematodes in Metazoa

The settings

In the last few decades, molecular approaches to biological systematics have pervaded the field, providing fresh perspectives on a wealth of new and old issues. This transformation is most evident in traditionally popular groups such as vertebrates (Mallat and Sullivan, 1998; Alvarez et al., 1999), vascular plants (Hoot, Magallon and Crane, 1999; Qiu and Palmer, 1999) and arthropods (Eernisse, 1997; Spears and Abele, 1997; Yeates and Wiegmann, 1999), but the practical and theoretical implications and applications of molecular evolution have also drastically redirected research on many other biota (Stenroos and De Priest, 1998; Lang et al., 1999; Sogin and Silbermann, 1998; Brinkmann and Philippe, 1999).

Taxonomical studies on microscopic organisms such as nematodes traditionally receive little attention, and have often generated considerable frustration for both their scientific producers and users alike. This is partly due to the severe practical difficulties of obtaining a representative sampling of all relevant taxa. An even greater constraint is formed by observational restrictions on the number of characters available for diagnosis and classification within such groups. In the case of nematodes, this has typically led to textbook phrases referring to the ‘great morphological uniformity of nematodes’. This persistent myth was based on a mere handful of well studied model species and largely ignores the numerous bizarre and perplexing morphologies, ecologies and ontogenies described in specialised literature for over a century (see De Ley, 2000). Nematode morphology is actually rich in potentially useful characters, but an ideal instrument for observation is still missing: light microscopy does not provide enough resolution and requires substantial experience, while electron microscopy (particularly TEM) is far too costly in time and equipment for effective use on a routine basis.

By comparison, modern molecular tools can quickly and affordably provide a wealth of characters, using standardised basic methods applicable in almost any taxon. The systematics of ‘morphologically uniform’ groups therefore stands to benefit tremendously from these new approaches. In microbiology, for example, prokaryote taxonomy has been revolutionised and is now firmly based on DNA sequence data and the application of the latest methods for computer assisted character analysis (Woese, 1994, 1996; Brinkmann and Philippe, 1999). Sequence analyses of nematode relationships have also begun to appear at a rapidly increasing pace, addressing such issues as the position of nematodes within Metazoa (Sidow and Thomas, 1994; Vanfleteren et al., 1994; Aguinaldo et al., 1997; Aleshin et al., 1998c), relationships among higher-level taxa within nematodes (Vanfleteren et al., 1994; Kampfer, Sturmbauer and Ott, 1998; Blaxter et al., 1998; Aleshin et al., 1998a, b), and relationships within and among previously intractable families and genera (see Fitch, Bugaj-gaweda and Emmons, 1995; Al-banna, Williamson and Gardner, 1997; Nadler and Hudspeth, 1998; Adams, 1998a, b; De Ley et al., 1999).

Another potentially vast source of taxonomic characters is developmental lineage mapping. Like Transmission Electron Microscopy, this technique remains more limited in routine applicability and cost-effectiveness, but lineaging and TEM can nevertheless provide far superior character resolution than light microscopy of preserved material. They are especially powerful when combined with phylogenetic frame-works provided by sequence analyses (cf. Baldwin et al. 1997a, b; Goldstein, Frisse and Thomas, 1998; Sommer et al., 1999).

Apart from increasing character resolution as such, alternatives to light-microscopical morphology are of fundamental importance for a second reason: character diversity and divergence in nematode taxa is often quite different depending on the character suites in question. Thus, divergence in ribosomal DNA sequence is remarkably high within certain nematode clades with fairly low morphological diversity, and remarkably low in other clades with much higher morphological diversity (Blaxter et al., 1998). There is no obvious correlation between rates of morphological evolution and rates of fixation of mutations. In a developmental analog, nematodes can exhibit substantial diversity in the mechanisms that specify cell fates, even in the absence of any evident differences in ultimate cell fates themselves, i.e. differences in final morphology (see review by Félix, 1999).

Any classification that claims to represent ‘natural relationships’ must therefore attempt to combine morphology with other character suites—and this even when relatedness is not directly equated to phylogeny. In this chapter, we assume that classification should be based primarily on phylogenetic relationships, even though we are aware that phylogenetic analysis of biological organisms (like any other scientific methodology) is not an infallible approach guaranteed to produce definite answers to all pertinent problems. Rather, our point is that phylogeny provides (a) a neutral ground for analysing, comparing and combining any set of characters reflecting evolutionary history and (b) a theoretical framework for translating that evolutionary history into classification along less arbitrary lines than those followed by individual intuition. Within a phylogenetic framework, new character suites such as molecular data do not replace morphological data, but rather they reduce the number of inconclusive or deficient analyses and thus improve the overall outcome (Patterson, Williams and Humphries, 1993).

Understanding the results obtained with molecular and embryological methodologies requires skills and knowledge that were hardly relevant to nematological systematics before, but which are rapidly becoming essential for both the users and suppliers of nematode classifications. Thus, a new phase is reached in the continuing process of taxonomic revision as driven by advances in accuracy and resolution of characters. Some excellent examples of the concomitant advantages, pitfalls and continuities are provided by recent developments in studies on the phylogenetic position of nematodes within Metazoa, and we will first focus on this issue.

New life for an old debate

The use of molecular datasets for the analysis of metazoan phylogeny has a short and s...