ORIGINAL ARTICLE
doi:10.1111/j.1558-5646.2011.01426.x
DO LARVAL TRAITS RE-EVOLVE? EVIDENCE FROM THE EMBRYOGENESIS OF A DIRECT-DEVELOPING SALAMANDER, PLETHODON CINEREUS
Ryan R. Kerney,1,2,3 David C. Blackburn,3,4 Hendrik Muller,¨ 5,6 and James Hanken6 1Biology Department, Dalhousie University, 1355 Oxford St., Halifax, Nova Scotia B3H 4J1, Canada 2E-mail: [email protected] 4Natural History Museum and Biodiversity Institute, University of Kansas, Lawrence, Kansas 66045 5Institut fur¨ Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, Friedrich-Schiller-Universitat¨ Jena, Erbertstr. 1, 07743 Jena, Germany 6Museum of Comparative Zoology and Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138
Received January 28, 2011 Accepted July 9, 2011
Recent molecular phylogenies suggest the surprising reacquisition of posthatching metamorphosis within an otherwise direct- developing clade of lungless salamanders (family Plethodontidae). Metamorphosis was long regarded as plesiomorphic for plethod- ontids, yet the genus Desmognathus, which primarily includes metamorphosing species, is now nested within a much larger clade of direct-developing species. The extent to which the putative reacquisition of metamorphosis in Desmognathus represents a true evolutionary reversal is contingent upon the extent to which both larva-specific features and metamorphosis were actually lost during the evolution of direct development. In this study we analyze development of the hyobranchial skeleton, which is dramatically remodeled during salamander metamorphosis, in the direct-developing red-backed salamander, Plethodon cinereus. We find dramatic remodeling of the hyobranchial skeleton during embryogenesis in P. cinereus and the transient appearance of larva-specific cartilages. Hyobranchial development in this direct-developing plethodontid is highly similar to that in metamor- phosing plethodontids (e.g., Desmognathus). The proposed reacquisition of hyobranchial metamorphosis within Desmognathus does not represent the “re-evolution” of a lost phenotype, but instead the elaboration of an existing developmental sequence.
KEY WORDS: Development, direct development, Dollo’s Law, evolutionary developmental biology, life history evolution, Plethodontidae.
“Dollo’s Law” posits that complex phenotypes are unlikely to then regained in particular lineages (e.g., Whiting et al. 2003; be regained once they are lost (Dollo 1893; Gould 1970). Re- Collin 2004, but see Collin and Miglietta 2008; Goldberg and cent studies of trait evolution in a phylogenetic context chal- Igic´ 2008). One particularly striking case is the proposed reacqui- lenge this claim by providing examples of complex phenotypes, sition of an aquatic larval stage in plethodontid salamanders of including entire life-history stages, that are allegedly lost and the genus Desmognathus, which is nested within a larger clade of direct-developing species (Chippindale et al. 2004; Mueller et al. 3These authors made equal contributions to this work 2004; Macey 2005; Kozak et al. 2005, 2009; Vieites et al. 2007,