EVOLUTION: NEMATODE WORMS

Nematode worms are typically long, round, unsegmented, gradually tapered at both ends.

"Nematodes have many species with relatively little difference in body form.  Many are parasitic and it is thought that most species of vertebrates may have one or more parasitic nematode species unique to them.  Nematodes parasitize many other groups of animals and plants.  Many live in the intestines of animals.  One free-living nematode species lives in organic rich soil but can also live as a parasite in humans. Rotting organic matter in soil is not so different from the intestinal contents of some animals.  Both are rich in bacteria that the nematodes can feed upon.  Adapting to the rich soil made them somewhat "pre-adapted" to life as an intestinal parasite. This adaptation included an ability to live in environments with oxygen so limited many other animals could not survive." (from my unpublished 2010 manscript)

The similarity of structure of different species disappears when the mouth end, and often the anal end, are examined microscopically.  Three jaws are present in some.  The pharanyx may have a muscular bulb that probably helps ingestion of food without losing pressure, the body contents act as a hydrostatic skeleton.  The cuticular covering of the body is molted or shed typically several times in early development.  During the process of development portions of the chromosomal material can be ejected from the chromosomes; this is perhaps a result of selection for the small size of ancestors living among the sand grains of soils. In one species the ejection of chromatin occurs in all cells except the stem cell until the 32 cell stage.  Body cells of many achelminths other than nematodes also seem to have the loss of ability to regenerate that is thought to be a result of the reduced chromosomal material in body cell nuclei (or nuclei when tissues are syncytial).  Near constant number of nuclei or cells of the species are present in the tissues of many aschelminths.

I was reviewing some of Libbie Hyman's work on Aschelminthes (not accepted as a valid cluster by many zoologists), but unfortunately she did not have the benefit of knowing about gnathostomulids (first described in 1956) which were later.  Gnathostomulids seem to be descendents of the simple early flatworms that are not flat, but are adapted to living in sediments that are often anoxic.  Reidel, 1969, suggests the gnathostomulids can be placed in either the Platyhelminthes or the Aschelminthes.  The gastrotrichs may be the connecting link to rotifers.  Nematodes may have been the termination of a line orginating early in the cluster of achelminth groups; but they have a complete lack of cilia, a fact that makes them unlikely to have given rise to any other groups since arthropods also lack cilia but are so clearly derived from annelids that do have cilia.  Thus the lack of cilia in nematodes and arthropods is an analagous, not homologous, trait.

The reason I referred to Hyman was to find out about the adhesive glands or pedal glands, commonly paired on most ashelminths' posteriors, but absent in the gnathostomulids.  The glands are very small and difficult to see, especially in nematodes.  I did not see them in some nematodes I had watched in water on a microscope slide at low magnification, but those nematodes were clearly adhering by their tail as the writhed around.  One researcher (Chitwood) divided nematodes into two groups depending on whether they had phasmids at their posterior.  The mouth area and anal areas of nematodes show great variation in microcopic details not conducive to casual observation.

Such fine details can be a great help in identifying species and often show revealing variation suitable for showing evolutionary relationships.  The October 20, 2017, issue of Science has a research report detailing such a fact with feather-like hairs on water-strider feet.  In the case of water-striders, the details are limited to very close relatives.  In arthropods, similar microscopic comparisons can be made of structures limited to closely related species of the same genus and sometimes of different orders.

When the very small and the very large features match, relationship seems more likely.  To determine evolutionary relationships, neither can be ignored.  Over-dependence on one may lead to error and demonstrate why the novice or student may see things the specialist or teacher does not see, a relationship affecting creativity as noted by Tinbergen.

Among the larger features distinctive for nematodes, that show them as a terminal group in an evolutionary sense, are the muscle cells of the body of the intestinal parasite, Ascaris.  All are longitudinal and each passes a muscle cell process to the nerve enervating the muscle.  Other lines of evidence that the Ecdysozoa are an invalid group are indicated by some of the references appended.

Ascaris can grow to a foot long during it time in the intestine.  It has a simple life cycle with transmission of eggs, typically ingested with fecal contaminated food, hatching in the intestine and larve going through tissue and blood to the lungs where they break out and get coughed up, swallowed, and then comlete their life in the intestine.  Another nematode parasite of humans is thought to be the fiery serpent mentioned by Moses.  It has a big name, Dracunculus medinensis, and is known as the guinea worm.  The adult female can be as much as a meter long and live in the subcutaneous tissue under the skin.  The larvae are discharged through a hole in the skin and, if ingested by an aquatic microcrustacean named Cyclops, complete their larval development and, if Cyclops is ingested by a human, eventually reach their location under the skin.

The great variations in size, number of host species needed to complete life cycles, and adaption to a single or limited number of final hosts of most vertebrates, as well as many invertebrates, seems to indicate an ancient origin for nematodes.

Joseph G. Engemann    Emeritus Professor of Biology, Western Michigan University, Kalamazoo, Michigan   October 30, 2017

REFERENCES (comments added)

Aguinaldo, Anna Marie A., James M. Turbeville, Lawrence S. Linford, Maria C. Rivera, James R. Garey, Rudolf A. Raff, and James A. Lake.  1997.  Evidence for a clade of nematodes, arthropods and other moulting animals.  Nature, 387:489-493. Unfortunately, textbooks have picked up their grouping of nematodes with arthropods and some other molting animals in a group they named Ecdysozoa; based on 18s ribosomal DNA sequences, it is inadequate to support such a group.  They even say “It was unexpected to find nematodes contained within the Ecdysozoa because in previous molecular studies they diverged deep in the protostome tree, even before the deuterostome-protostome bifurcation.”   -page 491 has discussion of unequal rates found in other nematode studies (documented and ignored) and their search for and choice of slowly evolving representatives [almost guaranteed to put an outgroup in where it doesn’t belong]

Fraser, Hunter B., Aaron E. Hirsh, Lars M. Steinmetz, Curt Sharfe, and Marcus W. Feldman.  2002.  Evolutionary rate in the protein interaction network.  Science, 296:750-752.  (26 Apr 2002)  “We show that the connectivity of well-conserved proteins in the network is negatively correlated with their rate of evolution.”  “interacting proteins evolve at similar rates.” - used “putatively orthologous sequences between Saccharomyces cerevisiae and the nematode Caenorhabditis elegans.” 

Halanych, Kenneth M.  1996.  Testing hypotheses of chaetognath origins: long branches revealed by 18S ribosomal DNA.  Syst. Biol., 45(223-246.   Well-done study but long branches and small sample size make result of relationships beyond the nematode-chaetognath affinity somewhat dubious.

Halanych, Kenneth M., John D. Bacheller, Anna Marie A. Aguinaldo, Stephanie M. Liva, David M. Hillis, and James A. Lake.  1995.  Evidence from 18S ribosomal DNA that the lophophorates are protostome animals.  Science, 267:1641-1643.  “we propose the node-based name (16)[K. de Queiroz and J. Gauthier, Syst. Zool. 39, 307 (1990)] Lophotrochozoa, which is defined as the last common ancestor of the three traditional lophorate taxa, the mollusks, and the annelids, and all of the descendants of that common ancestor.”  Note 10 includes the following statement “Regions that could not be readily aligned were excluded from the analyses.”  Their proposal is ridiculous when all data are considered.

Halanych, Kenneth M., and Yale Passamaneck.  2001.  A brief review of metazoan phylogeny and future prospects in Hox-research.  Amer. Zool., 41:629-639.  maintain Hox gene research supports the earlier ridiculous proposals of ecdysozoans and lophotrochozoans.  Has numerous references.

Hobert, Oliver, and Gary Ruvkun.  1998.  A common theme for LIM homeobox gene function across phylogeny?  Biol. Bull., 195:377-380.  neurogenesis regulatory genes and transcription factors are very similar in vertebrates, insects, and nematodes

Hobmayer, Bert, Fabian Rentzsch, Kerstin Kuhn, Christoph M. Happel, Christoph Cramer von Laue, Petra Snyder, Ute Rothbackerm, & Thomas W. Holstein.  2000.  WNT signaling molecules act in axis formation in the diploblastic metazoan Hydra.  Nature, 407:186-189.  the WNT signaling pathway had been found in nematodes, insects and vertebrates.

Kappen, Claudia.  2000.  Analysis of a complete homeobox gene repertoire: implications for the evolution of diversity.  Proc. Natl. Acad. Sci. USA, 97:4481-4486.  used the nematode, C. elegans

Sarnat, Harvey B.  1984.  Muscle histochemistry of the planarian Dugesia tigrina (Turbellaria: Tricladida): implications in the evolution of muscle.  Trans. Am. Microsc. Soc., 103(3):284-294.  Says striated muscle is in every metazoan phylum except Porifera and adult Platyhelminthes. (oblique striations in nematodes – Rosenbuth 1965, 67  Wright 62) 

Van Auken, Kimberly, Daniel C. Weaver, Lois G. Edgar, and William B. Wood.  2000.  Caenorhabditis elegans embryonic axial patterning requires two recently discovered posterior-group Hox genes.  Proc. Natl. Acad. Sci. USA, 97:4499-4503.  “essential embryonic patterning in C. elegans requires only Hox genes of the anterior and posterior paralog groups, raising interesting questions about evolution of the medial-group genes.” Three Hox genes in the nematode

ABANDONED THEORIES and LIBBIE HYMAN

THE ANNELID THEORY

A major focus of my posts is clarifying why the abandoned annelid theory of chordate origin should be reinstated.  People don't abandon theories without reason.  But reasons for abandoning a theory may have a validity that doesn't extend to all instances where they are applied.

A theory discredited before publication

An undergraduate research project by a former student, studying the protozoan Stentor, provided new observations for us that got us quite excited.  The protozoan is one of the larger protozoans that can be seen, although poorly, with the naked eye.  They are usually attached to solid surfaces in their aquatic environment.  Like many other ciliates, they have a macronucleus with many (sets of?)chromosomes, and a micronucleus with one set.  In the photo below you can see the trumpet like shape they have when attached and the beaded macronucleus inside.  They use cilia to circulate water to the large oral end and filter out food particles.

Figure above.    Two Stentor protozoans.  The macronucleus is elongate and enclosed within a membrane that is constricted to make the macronucleus appear beaded. 

The observation that excited us was the presence of many free-swimming Stentor's taking on the shape typical of the mobile state.  There was a concentrated population and many had a large central enclosure, like the picture below shows in the upper Stentor, that encloses another Stentor.

Figure above.  Free-swimming Stentor with an enclosed Stentor.  

Some ciliates are known to reproduce by producing internal buds.  But it had never been reported for this protozoan.  So he was excited when he told me about it.  He had even dissected one to release the internal bud and when released it swam away.

Observing the process for a day or so we finally came to the awareness that it was not a bud.  It was another Stentor that had been swallowed whole.  Apparently, cannibalism occurs when food supply decreases in crowded populations.

The annelid theory

The annelid theory was popular a hundred years ago.  It may never have been universally accepted.  But it was as good as any competing theory of chordate ancestry at the time.  The clincher responsible for its rejection was the observation that developmental stages often are a great clue to relationships that are not evident in adult organisms.

The annelid theory had support for the correspondence of relationships of systems of annelids and inverted chordates, or vice versa.

Two Figures above.  Annelid/Vertebrate systems as illustrated in early 20th Century texts, the upper in Romer and the lower in Lull, with one inverted so you don't have to turn your monitor upside down.

The drastic change in embryology of annelids versus chordates was used to discredit the theory.  But the evidence I present of the probable role of pogonophorans in expediting the shift should be sufficient to reconsider the annelid theory.  Gould* presented a good assessment of why it should be reconsidered due to a better understanding of the limitations of the "biogenetic law".

In reviewing volume five of Hyman's The Invertebrates (1959, McGraw-Hill, New York), I found on page 224 the beginning statement on relationhips of pogonophorans read "It is not open to doubt that the Pogonophora belong to the Deuterostomia."  Later she says "the Pogonophora appear most closely related to the Hemichordata."  Earlier, on page 201, she said about the hemichordate-chordates, "Such identity is inconceivable except on the basis of a common ancestry.  Hence a phylogenetic relationship between hemichordates and chordates is not open to question."

Those comments were made before the evidence of relationship of pogonophorans to earlier polychaete annelids was discovered.

A bit about Libbie Henrietta Hyman

Libbie Henrietta Hyman was perhaps the most outstanding zoologist of the last century.  She produced a comparative anatomy manual used by many of the pre-med students of her era.  Then, in her position at the American Museum of Natural History in New York, she produced a multi-volume treatise on invertebrates that remains a remarkable resource.

In the final chapter of volume five discussing new developments of topics in earlier volumes she uses colorful language to express definite opinions.  For example on page 750 - "The author hoped that the enterocoel theory was dead and buried, as it deserves, but . . .".  Then "The author regards the enterocoel theory as fantastic nonsence, for which there does not exist a single scrap of genuine evidence."

She criticizes views putting Proterospongia in line with the origin of sponges.  She provides arguments that the anthozoans cannot be the earliest cnidarians.  Both of those views are contradicted in earlier posts of this blog.

She had command of a vast amount of biology of organisms so her opinions have had considerable influence.  She proposed putting several phyla in a natural grouping she named Aschelminthes.  It had some acceptance until some experts in some of the groups disagreed, perhaps they thought it minimized the importance of the groups they researched.  So she later abandoned the view although I think it was correct in the inclusion of most of the groups it included.

A lesson learned

The short life of many ideas and theories, changed because of varying emphasis on major or minor features, gives me pause when I think about my evolutionary ideas.  I have learned from the evidence to support the coalescence of the annelid theory as correct in the connection suggested, that gross features can be important.  They can also mislead, as the importance of radial versus bilateral symmetry did in forming major clusters of phyla; the transition either way among the two symmetries is eventually selected by the habit of being attached to a substrate versus having active movement over a surface.  So it is difficult to state unequivocally that some parameter is the ultimate measure of the direction of relationships.

*Gould, Stephen Jay.  2002.  The Structure of Evolutionary Theory.  The Belknap Press of Harvard University Press, Cambridge, Massachusetts.  1433 pp.

Joseph G. Engemann      March 2, 2015
Emeritus Professor of Biology, Western Michigan University