PHYLOGENETIC EVIDENCE FOR A MAJOR REVERSAL OF LIFE‐HISTORY EVOLUTION IN PLETHODONTID SALAMANDERS

Abstract The transition from aquatic to terrestrial eggs is a key evolutionary change that has allowed vertebrates to successfully colonize and exploit the land. Although most amphibians retain the primitive biphasic life cycle (eggs deposited in water that hatch into free‐living aquatic larvae), direct development of terrestrial eggs has evolved repeatedly and may have been critical to the evolutionary success of several amphibian groups. We provide the first conclusive evidence for evolutionary reversal of direct development in vertebrates. The family Plethodontidae (lungless salamanders) contains the majority of salamander species, including major radiations of direct developers. We reconstruct the higher level phylogenetic relationships of plethodontid salamanders using molecular and morphological data and use this phylogeny to examine the evolution of direct development. We show that the predominantly biphasic desmognathines, previously considered the sister group of other plethodontids, are nested inside a group of directdeveloping species (Plethodontini) and have re‐evolved the aquatic larval stage. Rather than being an evolutionary dead end, the reversal from direct developing to biphasic life history may have helped communities in eastern North America to achieve the highest local diversity of salamander species in the world.

[1]  D. Ord,et al.  PAUP:Phylogenetic analysis using parsi-mony , 1993 .

[2]  D. Wake,et al.  Vertebrae of Plethodontid Salamanders from the Lower Miocene of Montana , 1981 .

[3]  E. Jockusch An evolutionary correlate of genome size change in plethodontid salamanders , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[4]  N. Shubin,et al.  Earliest known crown-group salamanders , 2003, Nature.

[5]  A. Collazo,et al.  Development of Gyrinophilus porphyriticus: Identification of the ancestral developmental pattern in the salamander family plethodontidae , 1994 .

[6]  David B. Wake,et al.  EVOLUTIONARY RELATIONSHIPS WITHIN THE ENSATINA ESCHSCHOLTZII COMPLEX CONFIRM THE RING SPECIES INTERPRETATION , 1992 .

[7]  K. Crandall,et al.  Lost along the way: the significance of evolution in reverse , 2003 .

[8]  L. Maxson,et al.  Evolution of marsupial frogs hylidae hemiphractinae immunological evidence , 1988 .

[9]  J. Huelsenbeck,et al.  Bayesian phylogenetic analysis of combined data. , 2004, Systematic biology.

[10]  D. Wake,et al.  An aquatic plethodontid salamander from Oaxaca, Mexico , 2001 .

[11]  J. Edwards Spinal nerves and their bearing on, salamander phylogeny , 1976, Journal of morphology.

[12]  T. Ryan,et al.  Life history evolution and adaptive radiation of hemidactyliine salamanders , 2000 .

[13]  W. Barker Ontogeny and phylogeny. , 1980, Archives of surgery.

[14]  L. Trueb,et al.  Biology of Amphibians , 1986 .

[15]  B. Ratcliff,et al.  Development as an Evolutionary Process , 1987, The Yale Journal of Biology and Medicine.

[16]  S. Tilley Life histories and comparative demo-graphy of two salamander populations , 1980 .

[17]  N. Hairston Species Packing in Desmognathus Salamanders: Experimental Demonstration of Predation and Competition , 1986, The American Naturalist.

[18]  M. S. Gunzburger EVALUATION OF THE HATCHING TRIGGER AND LARVAL ECOLOGY OF THE SALAMANDER AMPHIUMA MEANS , 2003 .

[19]  M. C. Grover Determinants of Salamander Distributions along Moisture Gradients , 2000, Copeia.

[20]  J. Gee,et al.  Ecology (3rd edn) , 1991 .

[21]  J. Hanken Larvae in Amphibian Development and Evolution , 1999 .

[22]  R. Bonett,et al.  Speciation, phylogeography and evolution of life history and morphology in plethodontid salamanders of the Eurycea multiplicata complex , 2004, Molecular ecology.

[23]  J. Bull,et al.  An Empirical Test of Bootstrapping as a Method for Assessing Confidence in Phylogenetic Analysis , 1993 .

[24]  D. Wake,et al.  Biodiversity of Costa Rican salamanders: implications of high levels of genetic differentiation and phylogeographic structure for species formation. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[25]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[26]  M. Sanderson Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. , 2002, Molecular biology and evolution.

[27]  J. Wiens Character analysis in morphological phylogenetics: problems and solutions. , 2001, Systematic biology.

[28]  O. Rieppel,et al.  A fossil snake with limbs. , 2000, Science.

[29]  J. Wiens Widespread loss of sexually selected traits: how the peacock lost its spots , 2001 .

[30]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[31]  A. Larson,et al.  Molecular Phylogenetics of Desmognathine Salamanders (Caudata: Plethodontidae): A Reevaluation of Evolution in Ecology, Life History, and Morphology , 1996 .

[32]  J. Wiens Combining data sets with different phylogenetic histories. , 1998, Systematic biology.

[33]  D. Hillis,et al.  PHYLOGENETIC RELATIONSHIPS AND SYSTEMATIC REVISION OF CENTRAL TEXAS HEMIDACTYLIINE PLETHODONTID SALAMANDERS , 2000 .

[34]  A. Rodrigo,et al.  Likelihood-based tests of topologies in phylogenetics. , 2000, Systematic biology.

[35]  E. Cope On the primary divisions of the Salamandridae, with descriptions of two new species , 1859 .

[36]  S. Tilley Studies of Life Histories and Reproduction in North American Plethodontid Salamanders , 1977 .

[37]  D. Wake PHYLOGENETIC AND TAXONOMIC ISSUES RELATING TO SALAMANDERS OF THE FAMILY PLETHODONTIDAE , 1993 .

[38]  D. Hillis,et al.  Marsupial frogs (Anura: Hylidae: Gastrotheca) of the Ecuadorian Andes: resolution of taxonomic problems and phylogenetic relationships , 1987 .

[39]  S. Brenner,et al.  Molecular synapomorphies resolve evolutionary relationships of extant jawed vertebrates , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Hartwell H. Welsh,et al.  Population Ecology of two Relictual Salamanders from the Klamath Mountains of Northwestern California , 1992 .

[41]  D. Wake Adaptive Radiation of Salamanders in Middle American Cloud Forests , 1987 .

[42]  Xuhua Xia,et al.  Data Analysis in Molecular Biology and Evolution , 2002, Springer US.

[43]  H. Wilbur,et al.  ECOLOGY OF ECOTONES: INTERACTIONS BETWEEN SALAMANDERS ON A COMPLEX ENVIRONMENTAL GRADIENT , 2002 .

[44]  J. Sites,et al.  Mitochondrial DNA Sequence Divergence and Phylogenetic Relationships among Eight Chromosome Races of the Sceloporus Grammicus Complex (Phrynosomatidae) in Central Mexico , 1994 .

[45]  W. Duellman,et al.  Oral structures and their development in egg‐brooding hylid frog embryos and larvae: Evolutionary and ecological implications , 1984, Journal of morphology.

[46]  J. Wiens Polymorphism in Systematics and Comparative Biology , 1999 .

[47]  P. Gregory,et al.  Population structure, growth, and reproduction in a Vancouver Island population of the salamander Plethodon vehiculum , 1989 .

[48]  J. Maerz,et al.  Environmental Variation and Territorial Behavior in a Terrestrial Salamander , 2000 .

[49]  J. Petranka,et al.  Salamanders of the United States and Canada , 1998 .

[50]  J. Dent The embryonic development of Plethodon cinereus as correlated with the differentiation and functioning of the thyroid gland , 1942 .

[51]  R. Shine,et al.  REPTILIAN VIVIPARITY AND DOLLO'S LAW , 1998, Evolution; international journal of organic evolution.

[52]  R. Jaeger,et al.  An assemblage of salamanders in the southern Appalachian Mountains revisited : Competitive and predatory behavior? , 1998 .

[53]  R. Wassersug Complex Organismal Functions. Integration and Evolution in Vertebrates. D. B. Wake and G. Roth, Eds. Wiley-Interscience, New York, 1989. xiv, 451 pp., illus. $122. Life Sciences Research Reports, vol. 45. From a workshop, Berlin, F.R.G., Aug.-Sept. 1988. , 1990, Science.

[54]  Taylor J. Maxwell,et al.  Loss and recovery of wings in stick insects , 2003, Nature.

[55]  R. Elinson Change in developmental patterns: embryos of amphibians with large eggs , 1986 .

[56]  W. W. Dimmick,et al.  PHYLOGENETIC RELATIONSHIPS OF THE SALAMANDER FAMILIES: AN ANALYSIS OF CONGRUENCE AMONG MORPHOLOGICAL AND MOLECULAR CHARACTERS , 1993 .

[57]  L. Steiner,et al.  Characterization and expression of recombination activating genes (RAG-1 and RAG-2) in Xenopus laevis. , 1993, Journal of immunology.

[58]  Nancy Huntly,et al.  Herbivores and the dynamics of communities and ecosystems , 1991 .

[59]  Michael J. Sanderson,et al.  R8s: Inferring Absolute Rates of Molecular Evolution, Divergence times in the Absence of a Molecular Clock , 2003, Bioinform..

[60]  John J. Wiens,et al.  Polymorphic Characters in Phylogenetic Systematics , 1995 .

[61]  S. Evans,et al.  A metamorphosed salamander from the Early Cretaceous of Las Hoyas, Spain , 1996 .

[62]  ARBOREALITY AND MORPHOLOGICAL EVOLUTION IN GROUND BEETLES (CARABIDAE: HARPALINAE): TESTING THE TAXON PULSE MODEL , 2003, Evolution; international journal of organic evolution.

[63]  A. Kluge,et al.  Comparative morphology of the inner ear in salamanders (Caudata, Amphibia) , 1978 .

[64]  L. Houck,et al.  The Biology of Plethodontid Salamanders , 2000, Springer US.

[65]  D. Schluter,et al.  RECONSTRUCTING ANCESTOR STATES WITH MAXIMUM LIKELIHOOD : SUPPORT FOR ONE- AND TWO-RATE MODELS , 1999 .

[66]  Hidetoshi Shimodaira,et al.  Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic Inference , 1999, Molecular Biology and Evolution.

[67]  D. H. Taylor,et al.  The Reproductive Biology of Amphibians , 1977, Springer US.

[68]  X. Xia,et al.  DAMBE: software package for data analysis in molecular biology and evolution. , 2001, The Journal of heredity.

[69]  K. Wells Reproductive Biology and Phylogeny of Urodela , 2004, Copeia.

[70]  J. Lynch,et al.  The frogs of the genus Eleutherodactylus (family Leptodactylidae) at the La Planada Reserve in southwestern Colombia with descriptions of eight new species , 1990 .

[71]  M. Pagel The Maximum Likelihood Approach to Reconstructing Ancestral Character States of Discrete Characters on Phylogenies , 1999 .

[72]  D. Wake,et al.  Tongue Evolution in the Lungless Salamanders, Family Plethodontidae IV. Phylogeny of Plethodontid Salamanders and the Evolution of Feeding Dynamics , 1986 .

[73]  A. Leviton,et al.  Standards in herpetology and ichthyology : Part I. Standard symbolic codes for institutional resource collections in herpetology and ichthyology , 1985 .

[74]  D. Wake Comparative osteology and evolution of the lungless salamanders , 1966 .

[75]  D. Wake,et al.  New genera and a new species of Central American salamanders, with a review of the tropical genera (Amphibia, Caudata, Plethodontidae) , 1983, Contributions in science.

[76]  A. Collazo,et al.  DIRECT DEVELOPMENT IN DESMOGNATHUS AENEUS (CAUDATA: PLETHODONTIDAE) : A STAGING TABLE , 1998 .

[77]  R. Bonett,et al.  Ontogeny discombobulates phylogeny: paedomorphosis and higher-level salamander relationships. , 2005, Systematic biology.

[78]  D. Sever Comparative Anatomy and Phylogeny of the Cloacae of Salamanders (Amphibia: Caudata). VII. Plethodontidae , 1994 .

[79]  Gene E. Likens,et al.  Salamander populations and biomass in the Hubbard Brook Experimental Forest, New Hampshire , 1975 .

[80]  D. Sever Comparative anatomy and phylogeny of the cloacae of salamanders (Amphibia: Caudata). I, Evolution at the family level , 1991 .

[81]  James M. Clark Fossil Plethodontid Salamanders from the Latest Miocene of California , 1985 .

[82]  R. Highton Speciation in Eastern North American Salamanders of the Genus Plethodon , 1995 .

[83]  D. Cutler,et al.  Estimating divergence times in the presence of an overdispersed molecular clock. , 2000, Molecular biology and evolution.

[84]  J. Huelsenbeck,et al.  MRBAYES : Bayesian inference of phylogeny , 2001 .