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Introduction to Arthropod Phylogeny - Are They Polyphyletic? lecture by Stephanie Zaklan

Biology 606 Lecture Summary by Mark Steinhilber

The phylum Arthropoda is divided into four subphyla: Chelicerata, Trilobitomorpha, Crustacea, and Atelocerata (or Uniramia). The hypothetical ancestor of the group is believed to be an annelid-like worm although there is much debate over whether a single form gave rise to all four subphyla.

Possible ancestral roots of the arthropod lineage include the remipedes and branchiopods (the latter is suggested by Fryer based on possession of a non-focussed feeding system). Proposed monophyletic evolutionary trees unified arthropods on the basis of such characters as sperm morphology, segmentation, and mandible structure and function. Polyphyletic hypotheses, such as those of Fryer, propose multiple origins of the major subphyla.

The monophyly vs polyphyly debate began with Haeckel's hypothesis of monophyly in the mid-1800s. Except for a brief time following the discovery of Peripatrusin the late 1800s, monophyly prevailed until 1957 when Tiegs and Manton suggested that similarities in arthropod mouthparts were convergent and the group was polyphyletic. Today, the monophyletic hypothesis is resurfacing although many examples of convergence are recognized.

The monophyly/polyphyly debate has included arguments based on morphology, development, fossils, and molecular evidence.

1) Morphology.The evolution of mouthparts from limbs, the types of mouthparts (gnathobasic vs whole limb), and their movement patterns have been used to hypothesize the number of possible arthropod ancestors. Manton believed that the gnathobasic jaw could not have led to the whole limb configuration and therefore felt the group must be polyphyletic. Kukalova-Peck, however, argued the 5 coxal segments found in all arthropods suggested monophyly. She also believed that the polyramous leg was ancestral, although this condition has been interpreted by others as uniramous with modification. It remains uncertain which condition originated first. Haemocoele invagination patterns, central nervous system structure, segmentation, and eye structure are considered homologous by some but convergent by others and therefore have not led to conclusive evidence for either monophyly or polyphyly.

2) Development.Using antibody staining techniques, differential expression of the Distal-lessgene was found in taxa depending on whether proximal or distal limb segments were involved in the jaws. Crustacean jaws, derived from proximal segments, should not show Distal-lessexpression. However, it has been reported in malacostracan and branchiopod mandibles (both are crustaceans) so this feature is suspect. The expression of the Engrailedgene in some groups (e.g., arthropods and annelids) has been interpreted as suggesting monophyly however this is an ancient gene which probably predates arthropodization and is therefore not useful for establishing monophyly.

3) Fossils.Contrary to Kukalova-Peck, fossil evidence suggests uniramous appendages are ancestral.

4) Molecular data.Recent studies provide varying phylogenetic conclusions. Some are incongruent with fossil evidence, others admit strong dependence on the taxa chosen or refute long-established groups. Molecular phylogenies must be interpreted carefully. Several statements summarized the study of arthropod evolution: 1) Polyphyly is unencumbered with proof of common ancestor 2) Understanding arthropod evolution is difficult because of the antiquity of the group. 3) Polyphyly appears the least improbable hypothesis; proponents of monophyly must prove otherwise.

Introduction to Arthropod Phylogeny - Are They Polyphyletic?

Summary of Discussion Based on Focal Paper by Fryer (1996)

Fryer's "polyphyletic" phylogeny actually appears monophyletic. The timing of arthropodization - before or after divergence from the proposed annelid ancestor - is a critical question. Fryer's contention that divergence and establishment of all arthropod subphyla occurred in 5 million years is questionable. This short time span creates problems for molecular analyses however if there is enough divergence to create subphyla there must also be some molecular divergence. If the time frame is correct, it may be difficult to explain the divergence based on either morphological or molecular data. One should not put too much emphasis on this 5 million year time span.

Fryer's evidence for convergence was questioned and the relative "strength" of convergence vs divergence was discussed. It was felt that traditional characters that define arthropods are still good.

The problem of different character sets producing different phylogenies was discussed. Additional data sets must be acquired if incongruent phylogenies result from the use of different characters. It was felt that features of the arthropod cuticle (e.g., ultrastructure and biochemistry) might have been informative in Fryer's analysis. It was also suggested that pleisiomorphic characters may be important, especially when rapid adaptive radiation is suspected.

Manton's belief that different basal arthropod types could not have given rise to each other (therefore the group must be polyphyletic) was countered with the argument that they all could have had a similar origin. Fryer, like Manton, wants to define arthropods in the same lineage. His obsession with the monophyly vs polyphyly debate was considered misguided - arthropods are monophyletic at some level. The definition of monophyly and polyphyly is important in this context but the real question is: what was the original ancestor like? It may be more productive to argue the validity of characters than monophyly vs polyphyly.

An argument for monophyly was proposed which involved the loss of epidermal cilia, a feature uniting arthropods. It seems highly improbable that all arthropods independently lost the external and internal cilia which is widespread in annelids (the hypothetical ancestor). Fryer apparently ignored this character.

A debate arose over whether the function of ancestral characters must be determined and if evidence that they would work is needed. Some felt the difficulties in reconstructing function might unduly constrain phylogenetic study. In addition, much DNA and some morphological characters have no specific function. Others believed there should be a logical functional connection between the evolutionary origin and endpoint of a structure. Simply because one cannot imagine or find a feature does not mean it cannot exist. However, it is possible to prove that a structure cannot work.

The difficulties in resolving arthropod phylogenies due to the time scales involved was reiterated. It was agreed that the discovery of major gene rearrangements and/or good fossil evidence could bring relationships to light.

The discussion ended with the suggestion that Fryer has made some claims outside his area of expertise and that he should have included more phylogenetic trees to back up these claims.

Fryer, G. 1996. Reflections on arthropod evolution. Biol. J. Linn. Soc. 58:1-55

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