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Muscling Past Homology Problems in Nature's Vertebrate Skeleton "Evolutionary Gem"

Links to our 9-Part Series Responding to Nature's Evolution Evangelism Packet:
• Part 1: Evaluating Nature's 2009 "15 Evolutionary Gems" Darwin-Evangelism Kit
• Part 2: Microevolutionary Gems: Lizards, Fish, Snakes, and Clams
• Part 3: Microevolutionary Gems: Bird-Sized Evolutionary Change
• Part 4: Microevolutionary Gems: Flea and Guppy-Sized Evolutionary Change
• Part 5: Microevolution Meets Microevolution
• Part 6: Evolutionary "Gems" or "Narrative Gloss"?
• Part 7: Muscling Past Homology Problems in Nature's Vertebrate Skeleton "Evolutionary Gem"
• Part 8: Of Whale and Feather Evolution: Two Macroevolutionary Lumps of Coal
• Part 9: Evolutionary Biologists Are Unaware of Their Own Arguments: Reappraising Nature's Prized "Gem," Tiktaalik
In the prior post responding to Nature's 2009 evolution-evangelism packet, I recounted Phil Skell's observation that for much research, evolution is not foundational but added in after-the-fact as "narrative gloss." One of Nature's evolutionary "gems" helped itself to a generous dose of evolutionary gloss. Given the messy picture its evolutionary thinking paints of vertebrate skeletal and muscle development, the authors may wish they'd gone on a gloss-free diet.

Nature's evolution-evangelism packet titles this gem "The origin of the vertebrate skeleton" -- but it's not necessarily the kind of "origin" you'd expect. At best, this research explains not evolutionary origins but developmental origins -- e.g., it examined the biological mechanisms that control the growth of the bones and muscles in the neck and shoulder region. What is more, those findings regarding developmental origins are applicable, at this point, only to the mouse. Whether their model can be extended generally to all "vertebrates" is another question that hasn't yet been addressed. In any case, Nature's evolution-evangelism packet describes the relevant paper, "Neural crest origins of the neck and shoulder," this way:

One key mystery, for example, is how much of the vertebrate skull is contributed by neural-crest cells and how much comes from deeper layers of tissue. New techniques have allowed researchers to label and follow individual cells as embryos develop. They have revealed the boundaries of the bone derived from the neural crest, down to the single-cell level, in the neck and shoulders. Tissue derived from the neural crest anchors the head onto the front lining of the shoulder girdle, whereas the skeleton forming the back of the neck and shoulder grows from a deeper layer of tissue called the mesoderm.

With these new techniques, researchers were able to determine exactly which parts of bones and muscle, "down to the single-cell level" in the neck and shoulder region of mice, are derived from the embryological tissue called the neural crest. They made the surprising discovery that neural crest cells migrate down into the spine of the scapula bone and many other neck and shoulder bones where they serve as attachment points for muscles.

This is absolutely fascinating research and the researchers' methods have huge potential to shed light on developmental processes. Yet one might have undertaken this study of developmental patterns simply by studying comparative development -- without assuming common ancestry. Their data about development is the same whether one assumes common ancestry or not. In fact, the findings of this research pose severe quandaries for the concept of homology.

The textbook Explore Evolution discusses how common ancestry faces a problem when purportedly homologous structures develop via different, non-homologous pathways:

In sharks, for example, the gut develops from cells in the roof of the embryonic cavity. In lampreys, the gut develops from cells on the floor of the cavity. And in frogs, the gut develops from cells from both the roof and the floor of the embryonic cavity. This discovery -- that homologous structures can be produced by different developmental pathways -- contradicts what we would expect to find if all vertebrates share a common ancestor. (Explore Evolution, p. 44)

The problem cited in this passage is encountered with the purportedly homologous neck muscles and their attachment points in mice. As the article called a "gem" by Nature explains:

[T]he pattern of neck muscles is far more conserved than the ossification modes of the shoulder bones to which these muscles are attached. This poses a serious problem for muscle homologies: in all cranial and trunk regions of the vertebrate body so far examined the embryonic cellular origin of muscle connective tissues and their respective skeletal attachment regions are identical. This implies that if attachment regions change in their cellular origins and ossification type, their coordinated muscle connective tissues also change in their composition. This would force us to reject the homology of all neck musculature in jawed vertebrates, although it has a highly similar and complex connectivity pattern.

(Toshiyuki Matsuoka, Per E. Ahlberg, Nicoletta Kessaris, Palma Iannarelli, Ulla Dennehy, William D. Richardson, Andrew P. McMahon, & Georgy Koentges, "Neural crest origins of the neck and shoulder," Nature 436:347-355 (July 21, 2005) (internal figure and citation references omitted).)

The paper tries to avoid these problems by assuming that the truly homologous entity is not the neck and shoulders bones but rather the "highly conserved" pattern of neck muscles (and their attachment points) -- what they call the "muscle scaffold." Although the neck and shoulder bones of various vertebrates often have essentially identical locations, shapes, and functions, their developmental pathways can be highly variable, so they can't be homologous. Most would think that muscles grow around bones, but the evolutionary mandate that 'something here must be homologous' leads to the absurd notion that neck and shoulder bones develop as they "'morph' around a highly constrained muscle attachment scaffold," and then on to the following equally absurd claim:

The rather counterintuitive "scaffold model" perceives muscle connectivities as the basic units (because they precisely correspond to cell populations) but considers the bones that everyone can see as mere epiphenomena and subjects of change.

(Matsuoka et al., "Neural crest origins of the neck and shoulder," Nature 436:347-355 (July 21, 2005).)

So if we assume that 'something here must be homologous', then only the muscles are programmed for development, and bones are now mere "epiphenomena" that "morph" their way around the "muscle scaffold." The view that bone structures are an epiphenomenal byproduct of development is called a "counterintuitive" interpretation being forced upon the authors by evolutionary thinking. These are the bizarre conclusions forced upon those who are unwilling to question the mandate of universal common ancestry.

And problems still remain. While their "muscle scaffold" model may solve some problems of homology, the model has implications that do not fit neatly under the standard vertebrate phylogeny. Nature's evolution-evangelism packet boasts that this research "allows the tracing of ... the location of the major shoulder bone of extinct land vertebrate ancestors, the cleithrum." That's not quite correct, since the cleithrum isn't known only in "extinct land vertebrate ancestors" -- it's also found in living frogs.

Given that frogs have a cleithrum whereas other land-vertebrates do not, the researchers' "muscle scaffold model" of homology forces them to conclude that the lack of a cleithrum is in fact not a primitive trait among extant land-vertebrates, but is the result of convergent evolution. "Thus," they write, "the cleithrum has been lost at least four times independently: in salamanders, mammals, turtles and diapsids [crocodiles, snakes, lizards, and birds]."

Their "muscle scaffold" model forces them to believe that various similar patterns of bone development -- once thought to be homologous -- in fact evolved convergently:

It remains to illuminate the molecular causes for this unidirectional trend to dismantle the dermal shoulder girdle, replace it by endochondral skeleton or lose it altogether, which seems to continue in mammals and amphibians and also extends to other bones such as the clavicle. In the framework of the highly constrained neck muscle scaffolds we find no evidence for histogenetic reversals; that is, that endochondral bones of ancestors turned into dermal bones of descendants during the course of evolution. We speculate that a common, as yet unknown, genomic cis-regulatory architecture governing neck ossifications in tetrapod ancestors might have predisposed different descending tetrapod lineages to similar parallel trends.

(Matsuoka et al., "Neural crest origins of the neck and shoulder," Nature 436:347-355 (July 21, 2005) (internal citations omitted).)

You've got to love the last sentence, which is worth repeating: "We speculate that a common, as yet unknown, genomic cis-regulatory architecture governing neck ossifications in tetrapod ancestors might have predisposed different descending tetrapod lineages to similar parallel trends." This is almost starting to sound like teleological evolution--but of course that's not allowed in Darwinian thinking, so it's just by the luck of the draw that all of these taxa independently arrived at the same bone structure.

Moreover, as we saw in the prior installment of this series, vague appeals to mutations in cis-regulatory elements may be a non-starter -- especially when one is trying to explain something as unlikely as genetic and developmental convergent evolution.

As Explore Evolution suggests, the problem here is that common ancestry is leading to irreconcilable predictions about homology -- either homologous bones have non-homologous developmental pathways, or the only homologous pattern is the "muscle scaffolding" and highly similar bones are mere "epiphenomena" that "morph" around the muscle scaffold.

The research is fascinating but the rather implausible evolutionary speculations are, as Phil Skell observed, mere "narrative gloss."