Tuesday, February 1, 2011

Lost and found -- Breaking Dollo's Law

It has long been thought that once a species loses a trait, that trait is gone forever.  The loss can't be reversed.  This is so well-accepted that it's risen to the status of a law of nature, Dollo's Law.  Dollo was a Belgian paleontologist working around the turn of the last century, and as he put it,  "An organism is unable to return, even partially, to a previous stage already realized in the ranks of its ancestors."  So, for example, according to Dollo's Law, we have lost the tail our ancestors had, and we won't regain it, reptiles that have made the transition from egg-laying to giving birth to live offspring can't go back, and so on.

From the BBC
But laws are made to be broken, and the idea that life follows 'laws' the way gravity and chemistry do is tenuous at best.  In this case, Dollo's 'Law' is currently under challenge.  A paper published online in Evolution on Jan 27, and discussed on the BBC website, describes the re-evolution of mandibular teeth in frogs after more than 200 million years.  Recent reports of exceptions to the irreversibility principle -- wings lost and regained in stick insects, the re-evolution of coiling in snail shells, re-evolved ocelli in cave crickets, wings in water spiders, and so forth -- have been called into question for methodological reasons, but the re-evolution of frogs teeth and other examples look pretty solid.  As Wiens concludes,
The results presented here offer an incontrovertible phylogenetic example of trait re-evolution, showing that mandibular teeth were lost in the ancestor of all living frogs and then re-evolved in the hemiphractid species G. guentheri. The alternate hypothesis, that mandibular teeth were lost independently in each of the dozens of lineages leading up to G. guentheri, is statistically unsupported and seems incredibly unlikely. Although the hypothesis that G. guentheri re-evolved mandibular teeth may be unsurprising to experts in amphibian anatomy, this compelling example has been ignored in the recent literature on Dollo's law. Further, this example is made remarkable by the application of a time scale for this event: mandibular teeth were absent for at least 225 million years (and likely much longer) before being regained.

Another example of an exception to Dollo's Law is described by Lynch and Wagner in the Jan 2010 issue of Evolution.  They present evidence for the re-evolution of oviparity, or egg laying, in "Old World sand boas in the genus Eryx nearly 60 million years after the initial boid transition to viviparity" based on a phylogenetic analysis of genetic data from boid snakes and other related groups.  In addition to the statistical support for re-evolution, they note that morphological evidence includes the fact that, like live born boas, the hatchlings of the "oviparous Eryx lack an egg-tooth providing independent evidence that oviparity is a derived state in these species."  And, the shells of the boas that have re-evolved oviparity are extremely thin compared with the shells of other boas, suggesting that the structure of the eggshell re-evolved as well.

The argument over whether Dollo's Law can be violated may primarily reflect the way we classify species and think about phylogenies.  As Wiens says,
...the observation that most well-documented cases of trait re-evolution occur after a period of trait loss of greater than 15 million years (Table 2) may also reflect methodological bias. A complex structure that re-evolves may need to be absent for tens of millions of years before its re-acquisition can be confidently distinguished from multiple losses (e.g., given typical diversification rates, this period of time may be needed for a group to diversify enough to have species nested deep in the phylogeny). Yet, if the gain of lost traits is possible, a consideration of the underlying genetics suggests that it should be much more likely soon after the trait is lost (Marshall et al. 1994). Thus, trait re-evolution may actually be hardest to detect under the conditions when it is most likely to occur, raising the question of whether trait re-evolution might be more widespread but frequently undetected due to methodological biases.
So, how is the re-evolution of a trait explained genetically?  Weins suggests that the fact that G. Guentheri still have teeth in their upper jaw facilitates the repositioning of teeth to the lower jaw.  The structural genes are there, they just need to be recruited for expression in a different place.  Generally, this is not very perplexing.  Single gene expression changes can lead to signaling environments that, in relevant tissues, can induce cascades of patterning-gene interactions that produce structures like teeth.

Indeed, the normal tissue is not required.  There are mouse and human examples in which hair or teeth grow where the other normally does.  Ovarian teratomas are disorganized tumor-like structures of disorganized embryos that, as was known even in the early 1800's (and cited by Darwin), developed hair and teeth (even chicks do not have enamel genes, but teeth can be induced to form by genetically similar processes as hair or feathers, and transgenic expression of some environment-preparing genes in embryonic chick jaws can lead to tooth-like structures).

Dental formulas (numbers and shapes of teeth in upper and lower jaws) and hair or coloration patterns can come and go for similar reasons.  In many cases, the genetic change can be a modification of existing genes and tissues.  Similar dental formulas have evolved numerous times in vertebrates.  In others, there are different pathways to similar outcomes.  This is what happens in some selection experiments, and seems, if we recall correctly, to be the case with ocelli in insects.  But the overall pathways are presumably rather simple, or the different activations activate similar pathways that are conserved because they are still doing something.  In the frogs, they're making teeth in the upper jaw, a tissue histologically similar to lower jaws.

The point here is not that reversals are trivial or uninteresting, but they are explicable when they occur.  However, highly organized or complex structures are unlikely to recur after too long of divergence.  If we re-evolved, say, swimming anatomy it would not likely be the same as what is found in fish.  Indeed, that is what whales did, and they swim by up and down motion rather than the side to side motion of fish, because their mechanism is anatomically different.

Again, these instances are interesting, and perhaps most interesting is that even before the genetic age anyone should have suggested, much less canonized, 'laws' about how evolution works.  At most they are statistical generalizations that, in genetic terms, relate to the likelihood of the same genetic mechanism re-evolving.


orang said...

Recent reports of exceptions to the irreversibility principle -- wings lost and regained in stick insects, the re-evolution of coiling in snail shells, re-evolved ocelli in cave crickets, wings in water spiders, and so forth -- have been called into question for methodological reasons

Which "methodological reasons"? Where can I read about this?

Anne Buchanan said...

From the Wiens paper: "Recently, Goldberg and Igic (2008) suggested that violation of Dollo's law is a “spectacular claim” (p. 2730) and that many of these examples may simply be the result of “devastating flaws” (p. 2727) in the methods used. Specifically, they suggested that previous studies were compromised by assumptions about state frequencies at the root of these phylogenies and by failure to account for the possible impact of the character on patterns of diversification (speciation and extinction)."

However, both the Lynch and Wagner and the Wiens paper disagree.

orang said...

Thanks! I was wondering because last year I had the pleasure to extensively discuss the issue with Wagner and a couple of other "specialists" at a small but fine meeting in Germany. Well, and there was no word at all about potential methodological problems with said studies.

Anne Buchanan said...

I see. Interesting. From these papers, it does seem that the evidence that re-evolution can happen is pretty solid.

Holly Dunsworth said...

Wait, the stick insect study showing how they evolved wings in parallel in different clades and even re-evolved wings too, is being questioned? I ask because I use this example in class.

Anne Buchanan said...

Holly, someone else will have to answer the question of whether Lynch and Wagner or Wiens, in presenting support for their own examples, also support those that Goldberg and Igic call into question.

CPJ said...

Lynch and Wagner use methods that may have exactly the same problems as Goldberg and Igic point out, and those are pervasive. I don't think they disagree. The insect wing regain hypothesis (which you use in your class, apparently) is very likely incorrect. It also seems to me that Wiens only points out that there are other reasons why phylogenetic reconstructions can mislead (in the opposite direction, and probably rarely, because the conditions he specifies are very unlikely). The frog teeth regain is sketchy as an example of Dollo's law: they have teeth all along on the upper mandible, so the regain is no more surprising than that of, say, number of teeth.

And, Anne, yes, it is clear re-evolution can happen. But it's unclear that it happened in any of these examples, where it is claimed, which possibly involve genetically complicated and homologous traits.