Dollo's Law: made to be broken?

Maybe it's time to retire Dollo's Law, the idea that once a trait has disappeared from a lineage, it can't reappear.  Louis Dollo was a Belgian paleoanthropologist who proposed in the late 19th century that once gone, a trait was lost forever.  Evolution could not repeat itself.  We have blogged about this before, e.g. when a paper appeared in the journal Evolution in 20011 suggesting that mandibular teeth had reappeared in a frog lineage after more than 200 million years.

Holly brought a new paper in Evolution to our attention, also detailing instances in which traits long lost have reappeared.  Most previous examples have been of hard tissue reversions, but in this paper, Rui Diogo and Bernard Wood document numerous instances of reversions to previous muscle structures in primates, and suggest what this might mean about development and evolution.

Diogo and colleagues have been involved in a long term comparative study of the anatomy of non-primate vertebrates, and of primates, looking at "homologies and evolution of the head, neck, pector and forelimb muscles of all major groups...based on dissection of hundreds of specimens and on a review of the literature".  They used this extensive data set to do parsimony and Bayesian cladistic analyses (a statistical method for classifying organisms into biologically similar groups based on whatever trait of interest) of the muscle data for primates.  They built a phylogenetic tree based on the cladistic analysis of 166  characters of head, neck, pectoral and upper limb muscles. 

...of the 220 character state changes unambiguously optimized in the most parsimonious primate tree, 28 (13%) are evolutionary reversions, and of these 28 reversions six (21%) occurred in the nodes that lead to the origin of modern humans; nine (32%) violate Dollo's law.

Without going into the anatomical details covered in the paper, suffice it to say that they found more anatomical reversions to an earlier state in head and neck muscles than in the chest or upper limb, and conclude that evolutionary reversions were significant in primate and human evolution.  Their explanation for why so many exceptions to Dollo's Law have been documented is that the developmental pathways that formed these structures were maintained over evolutionary time, perhaps because the pathways were used in the development of other structures, so that they could be readily recruited for the re-development of a once-lost trait.  Chickens, for example, still have some of the developmental pathways for teeth, although they haven't actually had teeth for 60 million years.  Some constraint on the pathways would explain its continued existence. 

It has also been found that during ontogeny, say of the hand muscles, various muscles develop that are subsequently lost as the embryo grows.  One example is the contrahentes muscle that extends to various fingers in an early human embryo, but is then lost later in development.  This is a muscle that adult chimpanzees do have, though adult humans do not.  Diogo and Wood report this same developmental story for multiple muscles.  This means that the developmental pathway has been retained, even if the specific trait has not -- 'hidden variation'. 

According to some authors, cases where complex structures are formed early in ontogeny just to become lost/indistinct in later developmental stages (the so called 'hidden variation') may allow organisms to have a great ontogenetic potential early in development, that is if there are for instance external perturbations (i.e., change in the environment, e.g., climate change, environment occupied by new species, etc.) evolution can use that potential (adaptive plasticity) (e.g, West-Eberhard 2003).

Others (Stephen J Gould, e.g.) have argued that rather than an argument for plasticity, this means that evolution is constrained, contingent on what is already there: the embryo couldn't develop properly if these pathways to nowhere were to change.  Some argue that hidden variation is not responsible for evolutionary novelty, though, as Diogo and Wood suggest, it can explain the reappearance of traits.

In essence, Dollo's "law" is a principle that something genetically complex is difficult to undo because mutation will remove order if not opposed by some form of selection.  The more steps removed, the more 'canalized' a trait would tend to be and the less flexible.  Indeed, 'canalized' is a word used early in the 20th century by CH Waddington for the persistence of fundamental traits.   Reversals may also be apparent rather than real: new mechanisms might bring about a similar appearance at the trait level without being a literal 'reversal'.  The nature of evolution is to avoid being put in a box out of which organisms couldn't evolve.

So whatever the explanation for these specific instances of violations of Dollo's Law, it's clear yet again that any evolutionary law is made to be broken.