The
Lophotrochozoa Ecdysozoa mistake
A
big mistake in the tree of life – ignoring generation time
How it started
What should be one of the crowning jewels of achievement in
molecular biology has been plagued by an unwarranted suggestion in an otherwise
outstanding seminal paper (Zuckerkandl and Pauling, 1965) detailing the theory
of molecular clocks. They clearly laid
out the factors determining genetic changes over time. One of the factors was generation time of
organisms. They opined that it was
impossible to determine the past generation times involved in the evolution of
species, but that variation in generation time factors speeding and slowing
rates would average out so generation time could be ignored. The big mistake had its basis in this
presumption.
Why it should have stopped
Within a few years, Kimura and Ohta (1971) noted that the
pauling (a rate of substitution of ten to the minus nine per amino acid site
per year) varied from one centipauling for histones to four paulings for fibrinopeptide
A. Of course the mutation rate for the
nucleotides of DNA would be somewhat higher than 400-fold because of the
redundancies in the DNA coding for amino acids.
Laird, McConaughy, and McCarthy (1969) already had reported a
ten-fold higher rate of nucleotide sequence variation for rodents compared to
artiodactyls when time estimates were in years and said “This difference
diminishes if generations, rather than years, represent the appropriate
interval of evolutionary divergence.”
Britten (1986) noted that “Examination of available measurements shows
that rates of DNA change of different phylogenetic groups differ by a factor of
5.”
Miyamoto, Sllghtom, and Goodman (1987) reported “. . the
slowdown in the rate of sequence evolution evident in higher primates is
especially pronounced in humans.” Field et al. (1988) noted that “For distantly related organisms, it is not possible
to establish homology between nucleotides in the rapidly evolving portions of
the molecule; thus, even if the entire 18s rRNA sequence is known, only some
parts of it can be used for phylogenetic inference.”
What should have stopped
Publication and acceptance by scientists in general of the
Lophotrochozoa and Ecdysozoa; papers describing the Lophotrochozoa in 1995 (Halanych
et al.), the Ecdysozoa in 1997
(Aguinaldo et al.), should have been
rejected by peer review. Both studies were
based on 18S ribosomal DNA sequences. Both
run counter to results of classical phylogeny studies preceding molecular
phylogenies; then the establishment accepts the contrary results of these two
small samples although the authors noted several things that should have raised
questions.
For the 1995 Lophotrochozoa study, note 10 includes the following
statement “Regions that could not be readily aligned were excluded from the
analyses.” And the 1997 Ecdysozoa paper
says “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.” It seems that both reports were state of the
art for molecular phylogeny studies of smaller evolutionary units having less
variation in basic life cycles and molecular features. So the problem is one of scale; errors are compounded
when generation time is ignored. The
fact that small scale projections are not greatly affected must have made the
authors and their peers think the new broad-scale studies were correct. Big mistake.
It has been said that hindsight is 20/20
Sanderson (1996) would have shown them their sample size was
too small. Other alerts are now
available from Maley and Marshall (1998), Martin and Palumbi (1993), Wägele
(1999), and many others. But with no correction
for generation time in their algorithms, it was GIGO. Computers can generate trees regardless of
the quality of the input. Unfortunately,
the flawed results have been accepted and perpetuated in textbooks and
additional research.
Disclaimer for conflict of interest
I admit to a certain amount of pique with both Nature and Science for having rejected manuscripts I submitted years ago that
might have had a role in providing a better solution to the evolutionary tree
of life. I understand the need to
reject over 90% of submissions means life is not necessarily fair for those
seeking publication. I made a 1988
presentation to the Michigan Academy entitled “A life cycle adjustment is
needed for molecular clocks”. In 2004 I
presented “Ecdysozoa, Lophotrochozoa, and Other Molecular Phylogeny,
Peer-Review Failures. “ The abstract was
in the Michigan Academician,
36(1):118-119. I intended to submit the full paper to Science, but found their new submission rules beyond my digital
capabilities. More about the answers I
have for evolutionary questions will be presented in future postings. I might have accepted the Lophotrochozoa and
Ecdysozoa proposal if I did not already have knowledge of a tree of life that better
fits the facts; the pogonophorans provide critical information supporting the
tree.
Joseph G. Engemann, Emeritus Professor of Biological
Science, Western Michigan University, Kalamazoo, MI May 31, 2013
References cited
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.
Britten, Roy J.
1986. Rates of DNA sequence
evolution differ between taxonomic groups.
Science, 231:1393-1398.
Field, Katharine G., Gary J.
Olsen, David J. Lane, Stephen J. Giovannoni, Michael T. Ghiselin, Elizabeth C.
Raff, Norman R. Pace, and Rudolf A. Raff.
1988. Molecular phylogeny of the
animal kingdom. Science, 239:748-753.
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.
Kimura, Motoo, and Tomoko
Ohta. 1971. On the rate of molecular
evolution. J. Molec. Evolution, 1:1-17.
Laird, Charles D., Betty L. McConaughy, and Brian J.
McCarthy. 1969. Rate of fixation of nucleotide substitutions
in evolution. Nature, 224:149-154.
Maley, Laura E., and Charles R. Marshall. 1998.
The coming of age of molecular systematics. Science,
279:505-506.
Martin, Andrew P., and
Stephen R. Palumbi. 1993. Body size, metabolic rate, generation time,
and the molecular clock. Proc. Natl. Acad. Sci. USA, 90:4087-4091.
Miyamoto, Michael M., Jerry L. Slightom, and Morris
Goodman. 1987. Phylogenetic relations of humans and African
apes from DNA sequences in the ψη-globin region. Science,
238:369-373.
Sanderson, Michael J.
1996. How many taxa must be
sampled to identify the root node of a large clade? Syst.
Biol., 45:168-173.
Wägele, Johann-Wolfgang.
1999. Major sources of errors in
phylogenetic systematics. Zool. Anz., 283:329-337.
Zuckerkandl, Emile, and Linus
Pauling. 1965. Evolutionary divergence and convergence in
proteins. Pp. 97-166. In: V. Bryson and H. J. Vogel (eds.). Evolving
Genes and Proteins. Academic Press,
N. Y.