EVOLUTION - SINGLE ORIGIN OF COELOMATES

MONOPHYLETIC ORIGIN OF COELOMATES

Segmentation as a starting point

Annelids are the animals most like the ancestral form of all coelomates.  Their segmentation enabled the speedy evolution of diversity.  That diversity includes forms that show little evidence of the remnants of segmentation.  Metamerism, of chordates and some other phyla, is the repetition of organs or structure along the length of a body that no longer has segmentation.

The serial repetition of structures enables regional modification of appendages and other structures from a relatively complex base with minimal genetic changes.  This is illustrated most clearly by arthropod appendages.  It is evident in our own pectoral and pelvic appendages, although not so obviously having an early stage of origin in segmentation.  Our early embryo has some of the more convincing evidence in myotomes; adults have vertebrae with paired nerves, blood vessels, and muscles that may also be convincing.

Reduction of segmentation in the chordate line was a result of its loss by pogonophorans in the portion of the body retained in hemichordate evolution.  Most mollusks lost evidence of metamerism as a result of the shell removing benefits of obvious metamerism. A vermiform fossil shows evidence of the annelid origin of mollusks (Sutton et al. 2001); and a fossil, Neopilina, shows a more molluscan intermediate stage (Lemche, 1957).   Arthropods have striking evidence of metamerism externally in most groups, both with skeletal segmentation and appendages

Just as segmentation was modified beyond easy recognition, the coelom was also greatly modified as higher animals diversified.  Coeloms, found in both the protostome line and the deuterostome line, but not in animals earlier than annelids, provide evidence of the annelid origin of coelomates.

Nephridia

Water and salt regulation is an important function of our kidney.  The annelid nephridium, with pairs in most of their segments, was modified by evolution into the nephrons of our kidneys; an intermediate connection is shown by Ruppert and Balser, 1986.  The oviduct also seems to be a nephron modification.  The water-vascular system of echinoderms may be derived from nephridia; the water-vascular system stays open to the exterior, indicating the echinoderms have probably lost the benefits of osmoregulation and thus never were able to survive in fresh water.

Blood

The central position of annelids in the ancestry of coelomates may be illustrated by blood pigments.  Polychaete worms have as many as four different oxygen transporting pigments in the blood.  Higher forms typically have one of those pigments, in our case, hemoglobin.

Other Molecular Evidence

Once I thought the Pogonophora were the deuterostome connection to protostomes (1983), I found a lot of supporting molecular evidence.  One of the first was the finding of Lipman and Pearson (1985) that crayfish Trypsin I is high-scoring for similarity to bovine trypsinogen.

The interpretation of molecular evidence is complicated by the fact that vertebrates tend to have some important genetic features in family clusters of genes whereas other animals typically have only one from a family.  Also, the same molecules may act in somewhat similar but different ways in different groups.  Hobmayer et al. (2000) found the WNT signaling pathway that had been found in nematodes, insects, and vertebrates (all with bilateral symmetry) also acted in axis formation of a radially symmetric cnidarian.

The protostome-deuterostome transition via pogonophorans may be returned to at some later date.  I expect to end the topic with my next post of a few additional references, some annotated, from my reference file that deal in some way with the topic, most about molecular evidence.

In summary, a wide variety of evidence points to the basic truth of the annelid theory of chordate origin.

References

   Hobmayer, Bert, Fabian Rentzsch, and 6 others.  2000.  WNT signaling molecules act in axis formation in the diploblastic metazoan Hydra.  Nature, 407:186-189.

   Lemche, H.  1957.  A new living deep-sea mollusk of the Cambro-Devonian class Monoplacophora.  Nature, 179:413-416.

   Lipman, David J., and William R. Pearson.  1985.  Rapid and sensitive protein similarity searches.  Science, 227:1435-1441.

   Ruppert, Edward E., and Elizabeth J. Balser.  1986.  Nephridia in the larvae of hemichordates and echinoderms.  Biol. Bull., 171:188-196.

   Sutton, Mark D., Derek E. G. Briggs, David J. Siveter and Derek J. Siveter.  2001.  An exceptionally preserved vermiform mollusc from the Silurian of England.  Nature, 410:461-463.

Joseph G. Engemann    June 30, 2013

EVOLUTION of systems inversion

EVOLUTION – ORIGIN OF DEUTEROSTOME SYSTEM INVERSION

Several major steps were involved in the inversion of systems as polychaete annelids gave rise to the chordate line of deuterostomes. 

First a branch of tube-dwelling, bottom-dwelling polychaetes evolved with some reduction of clear segmentation; development of a plume of tentacles for feeding and/or respiration probably was occurring as well.  A variety of marine species having a similar intermediate condition still exist.

The second major step involved the complete adaptation to life in abyssal sediments as pogonophoran worms.  This included (1) a loss of dorso-ventral distinctions common to species ancestral to groups with radial symmetry, (2) reduction of development of the gut, (3) increased reliance on passive absorption of nutrients, and (3) retention of the circulatory system to provide oxygen to the portion of the worm embedded in low oxygen sediments. 

The embryological changes noted in the previous post were occurring simultaneously with these changes.  They now are the pogonophorans, well-adapted to survive the extinction events of pre-Cambrian times.  The major feature identifying them as annelid descendants was the extreme lower segmented and setae bearing portion that was not noticed in specimens of early collections made by dredges that did not retrieve whole worms; the deeply embedded part presumably was left in the ocean bottom.

The third major step in the protostome-deuterostome journey was the sequence of changes as descendants moved to shallower seas during the period following the intense asteroid bombardment (see May 11 post).  Those moving from their tubes to reach particulate food more abundant on shallower sea sediments found it less jarring to the nervous system to emerge with the previous ventral nervous system of the annelids positioned so it was nearer the upper surface.  In such a position, a remnant of the gut, perhaps more substantial because of the greater abundance of food, put endodermal and ectodermal tissue closer together to induce the mouth formation associated with such an event.

A further consequence of this new position of the mouth enabled fusion of ganglia and connectives to form a brain without encircling the esophagus.  These and other changes above were facilitated by natural selection of those with genetic modifications better serving the processes.

The culmination of this process needed very little fine tuning to make a hemichordate, probably the closest annelid derivative to the chordate line of deuterostomes.  The larval stages of pogonophorans and hemichordates are very similar.  Correspondence of the anterior of a hemichordate and the upper portion of a certain pogonophorans is quite similar.  The lowest segmented portion of the pogonophoran degenerated to leave three body regions some think are characteristic of chordates.  Previous discussions indicated the speed of loss of features not contributing to survival by the greater energy left over for reproduction is a common feature in evolutionary events.

Clearly, pogonophorans are excellent candidates for the missing link clarifying the inversion of systems suggested by the annelid theory of chordate origin.  

BRING BACK THE ANNELID THEORY.

Joseph G. Engemann    June 28, 2013

EVOLUTION - THE PROTOSTOME-DEUTEROSTOME LINK

ORIGIN OF DEUTEROSTOME EMBRYOLOGY

Annelid theory as a working hypothesis

Since Gans and Northcutt (1983) provided evidence of a close relative of annelids having some features of development resembling deuterostomes, as noted in the previous post, it is reasonable to evaluate other evidence.  Inversion of systems, the primary evidence supporting the annelid theory, has been deemed inadequate by those who comment.  But much other evidence is available.  The biggest impediment had been the drastic embryological differences between protostomes and deuterostomes.

Embryological evidence

My doctoral thesis research included a comparison of development of two species of isopods with very different life cycle rates of development as well as a new embryological structure in one species.  The rapidly developing egg of the Michigan species was smaller, had a thinner egg shell, and two appendages on the egg.  The Tasmanian one had a thicker egg shell and no appendage; but on the each side of the embryo within the egg was a yolk filled bulge in the position from which the other ones had their egg appendages develop.

Otherwise, both embryos packed the egg fully.  They both developed in a folded position, legs outermost.  But the flattening differs so the Tasmanian one filled up space with the yolk filled bulge.  The Tasmanian species has less change from ancestral crustacean features; they also lack the abundant source of food from deciduous tree leaves as available for the Michigan ones.

The main point of this isopod egg observation is that the evolution of a new feature in the egg goes counter to what many biologists think was perhaps a valid portion of the discredited “biogenetic law”.  The law is not absolute, especially as my observation showed me, evolution can occur by the development of new features in the earliest life stages of an organism.  Clearly, embryological stages do not faithfully repeat steps in the evolution of the organism. 

Since the pogonophorans are likely candidates as intermediates, in spite of the general opinion that they were an evolutionary dead-end, what do they contribute to the story?  Well, they have lost the annelid digestive system in the adult, their segmentation has nearly disappeared, and they live in an abyssal world with a very low rate of input of food.  Such a regime would drastically select options or mutations that save energy. 

Why protostome spiral cleavage became deuterostome radial cleavage

The thinning of the egg shell would not constrain the early dividing cells into the packed spiral pattern of ancestral protostomes but it would conserve resources otherwise used for a strong egg shell.  Consequently, the loss of structural integrity of the egg shell would not impose the constraints for efficient use of space as in spiral cleavage.

Limited energy and resulting low reproductive potential puts survival at a premium for the individual.  Thus, although the first cell divisions (cleavage) of protostome eggs end the potential of the daughter cells to each develop into individuals, it is possible for each of the early dividing cells of the deuterostome egg.  Injury or death of one of the first few cells of a deuterostome egg would not necessarily result in death.  In fact, identical twins, triplets, and other genetically identical individuals could not have developed if deuterostomes had retained the features of spiral cleavage.  The survival advantage of this feature for pogonophoran species in the nutrient poor abyss should be an obvious benefit.

In both cases it is a loss, loss or reduced production of shell, loss of control of early developmental specification.  As discussed in an earlier post, loss can occur more rapidly than gain of a feature.  The rates are relative to other factors such as food supply, generation time, and value of the features for survival.  But clearly, pogonophorans are excellent candidates for the missing link connecting embryological features of protostomes and deuterostomes.  The conclusion is hypothetical.  The event described was undoubtedly a Pre-Cambrian occurrence.  But the conclusion is based on comparative evidence consistent with similar conclusions that will be presented for other evidence.

Interesting, but somewhat irrelevant to the current discussion is the fact that the Michigan isopod egg appendage had the cellular appearance of adult respiratory tissue and must aide their relatively rapid development.

References

Engemann, Joseph G.  1963.  A Comparison of the Anatomy and Natural History of Colubotelson thomsoni Nicholls, a South Temperate, Fresh-water Isopod and Asellus communis Say, a North Temperate, Fresh-water Isopod.  Ph.D. Thesis, Michigan State University, East Lansing.  146 pp.

Gans, Carl, and R. Glenn Northcutt.  1983.  Neural crest and the origin of vertebrates: a new head.  Science, 220:268-274.

Acknowledgements

A United States Fulbright Grant for study in Australia, aide of staff and use of facilities at the University of Tasmania and Michigan State University, as well as a Faculty Research Grant at Western Michigan University, were instrumental in my making many observations involved in this series of blogs.  Many individuals deserve my thanks as well.

Joseph G. Engemann     June 24, 2013