Does the development within the salamander family Plethodontidae violate Dollo’s law?

A paper appeared recently in Evolution (R.R Kerney et al., 2011 check out the link) pertaining to Dollo’s law and the re-evolution of larval characteristics in salamanders. Dollo’s law basically states that a complex phenotype once lost is unlikely to be regained. One example of a violation of this law is the development in the salamander family Plethodontidae. Salamanders either undergo metamorphosis or direct development, but the ancestral state is metamorphosis. Members of the recently derived family, Plethodontidae  have for the most part direct development which is to say they pop out as mini forms of their adult counterparts. The exception to this trend is the genus Desmognathus which is nested all up in the family, but the majority of their species metamorphose. Basically you have one genus of metamorphosing species inside a massive clade with a totally different life history employing direct development. Moreover, the earliest branching lineages are direct developers. This would point to the larval characters and metamorphosis of later Desmognathus sp. as a re-evolved state.

Is this a violation of Dollo’s law?

Basically the authors examined skeletal characters from an embryo of a direct developing representative (Plethodon cinereus). Interestingly, the authors chose P. cinereus instead of comparing one of the direct developing species in Desmognathus or comparing all three.

One would expect that if these traits had re-evolved one would not see evidence of the similarity of characters in a direct developing embryo when compared to a metamorphosing specimen. Evidence was found to the contrary, and the larval characteristics were found in the developing embryo of P. cinereus. The character analysis of the hyobranchial skeleton is all very technical, but the remodeling that occurs during both embryonic development of P. cinereus is much like that of development during metamorphosis within the genus Desmognathus. The authors posit this study as “a cautionary tale” in evaluating Dollo’s law. I would agree and add this study provides evidence to suggest rethinking the way in which life-history traits are given weight in evaluating  phylogeny.

Fingers-crossed for a follow-up paper that evaluates the plasticity of development and environmental pressures and interactions.

Chippindale, P.T., R.M. Bonnet, A.S. Baldwin, and J.J. Wiens. 2004. Phylogenetic evidence for a major reversal of life-history evolution in plethodontid salamanders. Evolution 58: 2809-2822.

Dollo, L., 1893. Les lois de l’evolution. Bull. Soc. Belge. Geol. Pal. Hydr. 7: 164-166.

Kerney, R.R., D.C. Blackburn, H. Muller, and J. Hanken. 2011. Do larval traits re-evolve? Evidence from the embryogenesis of a direct-developing salamander, Plethodon cinereus. Evolution 66-1: 252-262.

Titus, T., and A. Larson. 1996. Molecular phylogenetics of desmognathine salamanders (Caudata:  Plethodontidae): a reevalutation of evolution in ecology, life history, and morphology. Syst. Biol. 45:451-472.

5 Responses to Does the development within the salamander family Plethodontidae violate Dollo’s law?

  1. Other examples of violations of Dollo’s law?

  2. Here’s another good article on violating Dollo’s law.

    http://life.bio.sunysb.edu/ee/wienslab/wienspdfs/2011/Wiens_2011_Evolution.pdf

    I suspect they used P. cinereus for a couple reasons.
    1. They are very common in their area and somewhat of a model. D. wrighti and aeneus are also very small and probably harder to work with and get eggs.
    2. They probably did this study at the same time as another on lung development in Plethodontids.
    http://0-www.sciencedirect.com.library.utulsa.edu/science/article/pii/S0012160611008578 (Don’t know if you will be able to open that….)

    I also think direct development/larval periods is highly plastic in many Desmognathus, in particularly D. ocoee.

    I have often found nests adjacent to streams with females guarding, where the larva would have to make a decent journey to get into water and have also found incredibly small metamorphosed Desmogs which I think never actually went through a larval stage per say.

    Its also interesting that it took so long since the 2004 paper for this data to actually be compiled and published. I know the authors of the 2004 paper and whenever I talked to them about how this phenomenon works they always talked about developing in the egg being the mechanism and I guess sorta thought it was address somewhere already.

    Mike

  3. A similar argument could be made for paedomophs bs. metamorphs in terms of evaluating differences in context instead of at an absolute level.

  4. Yeah, your right. Its all really just a form of heterochrony.

  5. As an evolutionary biologist deeply frustrated with the simple-minded approach to the study of character evolution (including asymmetry and irreversibility), I find this paper particularly refreshing:

    http://dspace.mit.edu/handle/1721.1/65355)

    P.S. “Les lois de l’Évolution” is from 1893, not 1983. (flip the digits)

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