Pogonophora - Central position in evolution

Pogonophora: Their spectacular role in animal evolution

A spectacular connection of the two main higher animal groups

Early embryology of the two main lines of animals

     The Pogonophora show how the radial and indeterminate cleavage of deuterostomes (echinoderms, hemichordates and vertebrates) came about from pre-Cambrian annelids in the deep sea while other annelids retained the spiral and determinate cleavage of protostomes as they were giving rise to arthropods and mollusks.

     The deep sea had low input of nutrients that put a premium on not investing in heavy egg shells that protected eggs of protostomes as they were confined in the spiral pattern of cleavage, a confinement that was released by less confining outer membranes that allowed a more direct radial cleavage pattern.  At the same time radial cleavage did not produce the immediate cell fate into a particular tissue, thus making possible more than one viable embryo from a single egg as each of the early cleavage cells retained all of the development potential of the original egg.  The ability to complete development without all the original cleavage products had high survival value in the rigorous deep-sea environment, although details are speculative.

    My comparative study of Tasmanian and Michigan isopods included observation of the impact of the egg membrane’s role in confining development, leading to a unique egg appendage, a clear indication that evolution can occur in developmental stages independent of adult development.  (see more on “Origin of deuterostome embryology” in blog post dated 6/24/2013)

Systems inversion

A simple process

The inverted position of blood vessels, nerves, oral openings of deuterostomes as compared to protostomes (especially the ancestral annelids of both groups) was proposed as evidence of the central role of annelids in evolution of higher animal phyla.  The original reason for rejecting the theory was the drastic difference in early embryology of the two lines of animals.  The next reason thought to negate the annelid theory as well as the embryological argument against it was the use of nucleotide and other molecular data.  Such data must be realigned taking into consideration the effect of the astronomically slow rate of genetic change in the pogonophorans ancestors.

Inversion, the first step

The inversion of annelids began with certain polychaetes that began living vertically in tubes they secreted, as seen in Sabella and many other shallow water polychaetes.   As those growing in progressively deeper water, with less food, became dependent on absorption of nutrients in pore water of the sediments they outcompeted those wasting energy on producing a mouth and some bilateral structure.  This stage is still found in abyssal pogonophorans. 

Inversion, the second step

The return of descendants to shallow seas occurred once the worst episode of pre-Cambrian asteroid bombardment eased.  As they arrived in shallower more nutrient rich areas, they reformed the remnants of their digestive system with a new mouth on the former dorsal side which became the ventral side, as they groped around the sediment surface near their tube, finding food particles that pushed the epidermal and gut layer together triggering mouth formation on the former dorsal surface without the restriction of the nervous system that originally had encircled the esophagus.  Other clues to this step are presented by the parallels of endocrine hormone function, transport, and structural similarities of vertebrates, arthropods, and annelids.

Protostome-Deuterostome links

Segmentation/Metamerism

The segmentation of annelid type was found on a short portion of the most deeply embedded part of some pogonophorans; it included setae that are a very annelid like characteristic.  A few anterior regions are noticeable but without the posterior segmented region it would be difficult to make an annelid connection.  The metamerism of chordates such as ourselves seen in bone, muscle, nervous system and blood vessels is now easily understandable with the intermediate stage of pogonophorans.

The transition from pogonophorans to chordates is best shown by the larval stage comparisons of pogonophorans and hemichordates.

Molecular evidence

Molecular features of several types show greater similarity between deuterostomes and advanced protostomes than their earliest variants found in more ancient protostomes once thought to be the closest common ancestors at the protostome-deuterostome split.

DNA/RNA studies of evolutionary relationships at the phylum level need reevaluation because major ones have ignored the mutation rate differences associated with generation times.  Many well focused studies have shown generation time does affect evolution rates.  One impact has been the Pogonophora showing up in many odd places in phylogenetic trees because they are almost unchanged since their divergence from major groups that have diverged even more from more recent relatives.

Six other posts, from June 17 to June 20, 2013 have additional clarification of the points made above.  The second June 30^th post of that year is an annotated bibliography that has some emphasis on protostome/deuterostome comparisons.

Joseph Engemann   

Emeritus Professor of Biology, Western Michigan University, Kalamazoo, Michigan    May 19, 2019

THE MAJOR EVOLUTIONARY TRANSITION

Annelid worms are ancestral to all of the advanced major phyla.  Arthropods and mollusks retained annelid features as one major grouping of advanced phyla.  Chordates and echinoderms are the other major grouping.  The two groups share some common feature as a result of their annelid ancestries.

There are eight posts in this blog-site from 6/17/13 to 6/30/13 that are a more extended description of the basis for accepting the annelid theory of chordate origin.  The annelid theory eliminates the need to (1) assume a second early origin of segmentation and/or metamerism from acoelomate protostomes, (2) explain numerous bits of molecular similarity between coelomate protostomes and deuterostomes, (3) and, with the incorporation of information about the pogonophoran bottleneck connection provided in this blog, provides a logical rationale for the embryological differences as well as the mechanism of inversion of systems in the transition of protostomes to deuterostomes.

THE ANNELID PHASE

The pogonophora are fairly well established as close relatives of some marine polychaete annelids.  The fossil record provide very little evidence of events, but some annelid descendants clearly  existed during the pre-Cambrian.

Step one.  Tube-dwelling worms such as Sabella, started the rotation as they reoriented their posterior to a position in the sediments and left their plumose tentacles up in the water.

Step two.  Those becoming pogonophorans had multiple changes selected by the rigor of life at constantly increasing depths as they struggled to survive asteroid bombardments in the pre-Cambrian.  In particular, low metabolic rates due to abyssal pressure and temperature, tubes extending deep into the sediments for absorption of fossil nutrients, as well as retention of a blood vascular system to transfer oxygen from the water to the embedded end of the worm deep in the sediments, and loss a many non-essential features.  The thinning of the eggshell enabled dropping the spiral development of annelids and the ability of eggs to develop even if some cells were lost.  Loss of obvious segmentation left only a remnant of segments at the  posterior to anchor the worm in its tube.

Part  of step two was the reduction of the digestive system, particularly the mouth and esophagus.  This allowed the later fusion of the ganglia of the head into a brain blocking the mouth formation on the old ventral side.

Step three.  As asteroid caused extinctions in the surface areas of the oceans eased, progeny of the abyssal worms survived as they moved into shallow water and benefited by mouths developing where gut remnants touched epidermis on  the old dorsal side.  As they extending from their tube they now would use their relocated mouth to feed on particulate matter in their vicinity.

Step four.  As they increased their activities they were doing it with the old dorsal side now the new ventral side.  SO THE WORMS DID NOT ROLL OVER, THEY DID A BACK-FLIP as they made their transition from annelid to pre-Chordate organisms during the pre-Cambrian.

Referring to the February 27, 2015 post on "Evolution: the body cavity" may help you understand the bit about relocation of the mouth above.  The March 2, 2015 post on "Abandoned theories and Libbie Hyman"  has a brief discussion of the annelid theory and an associated figure.

THE IMPORTANCE OF THE REGRESSIVE  POGONOPHORAN STEP

The loss of features as pogonophorans adapted to life in the deep sea were essential factors enabling the climb to the branch of the animal kingdom known as the deuterostomes, with the vertebrates members dominating life on earth.  It enabled rearrangement of the head with fusion of ganglia into a brain and mouth formation on the former dorsal surface, simplified embryology of radial cleavage and delayed determination of first cells of the embryo.  The loss of ability to form chitin in deuterostomes meant other structural materials became more important.  Hemoglobin is the only blood pigment surviving in deuterostomes although a diversity of blood pigments are found in annelids prior to the pogonophorans.

OTHER PHYLA

There are other major and minor animal groups that are side shoots at many positions along the groups of the tree of life leading to as well as following the significant deuterostome branch.  They continued, some becoming extinct, others diversifying into forms still present.  One major group of arthropods, the trilobites, dominated paleozoic seas before becoming extinct.  The sponges of today no longer include the group giving rise to early protostomes.

The above figure shows the central sequence of protostomes leading to annelids from which all above them trace their ancestry and have coelomate body cavities.  The sequence follows a time sequence of origin of groups having living representatives (except for the hypothetical protonemerteans).  The pogonophorans provide a transition from coelomate protostomes to the vertebrate line that clarifies the transition without the mystery of many unknown ancestral groups coming from flatworms.

Many invertebrate groups such as ctenophorans, chaetognathans, lophophorates, echinoderms, sipunculids, extinct groups, and many others are not represented in the diagram.

Joseph Engemann   Emeritus Professor of Biology, Western Michigan University, Kalamazoo, Michigan      July 16, 2018