David B. Wake

Size and shape in ontogeny and phylogeny

We present a quantitative method for describing how heterochronic changes in ontogeny relate to phyletic trends. This is a step towards creating a unified view of developmental biology and evolu- tionary ecology in the study of morphological evolution. Using this representation, we obtain a greatly simplified and logical scheme of classification. We believe that this scheme will be particularly useful in studying the data of paleontology and comparative morphology and in the analysis of processes leading to adaptive radiation. We illustrate this scheme by examples drawn from the literature and our own work.

Are we in the midst of the sixth mass extinction? A view from the world of amphibians

Many scientists argue that we are either entering or in the midst of the sixth great mass extinction. Intense human pressure, both direct and indirect, is having profound effects on natural environments. The amphibians—frogs, salamanders, and caecilians—may be the only major group currently at risk globally. A detailed worldwide assessment and subsequent updates show that one-third or more of the 6,300 species are threatened with extinction. This trend is likely to accelerate because most amphibians occur in the tropics and have small geographic ranges that make them susceptible to extinction. The increasing pressure from habitat destruction and climate change is likely to have major impacts on narrowly adapted and distributed species. We show that salamanders on tropical mountains are particularly at risk. A new and significant threat to amphibians is a virulent, emerging infectious disease, chytridiomycosis, which appears to be globally distributed, and its effects may be exacerbated by global warming. This disease, which is caused by a fungal pathogen and implicated in serious declines and extinctions of >200 species of amphibians, poses the greatest threat to biodiversity of any known disease. Our data for frogs in the Sierra Nevada of California show that the fungus is having a devastating impact on native species, already weakened by the effects of pollution and introduced predators. A general message from amphibians is that we may have little time to stave off a potential mass extinction.

Homoplasy: The Result of Natural Selection, or Evidence of Design Limitations?

Similarity in morphological form may arise from common ancestry (failure to evolve), from parallel evolution, from convergence, or from reversal to an apparently ancestral condition. Homoplasy from convergence, parallelism, and reversal is common, and its ubiquity creates difficulties in phylogenetic analysis. Convergent evolution often is considered one of the most powerful lines of evidence for adaptive evolution. But an alternative explanation for convergence and other evolved similarities is that limited developmental and structural options exist. Identical forms can be obtained when particular developmental phenomena are triggered by very different kinds of stimuli or when constraints exist that shape external form or limit morphological expression to a few options. Examples from plethodontid salamanders are used to illustrate an approach combining internalist and externalist analytical methods. In order to explain how morphologies evolve in lineages, both functionalist and structuralist approaches are necessary, combined in a context in which phylogenetic hypotheses and their tests are continuously pursued. When homoplasy is rampant, as in salamanders, we can expect discordance with phylogenetic analyses based on nonmorphological data sets.

On the problem of stasis in organismal evolution

Abstract One of the most challenging problems in evolutionary biology is morphological stasis—the maintenance of a standard morphology over vast periods of time during which much environmental change has taken place. We review empirical data for one well studied group of vertebrates, salamanders of the family Plethodontidae. Despite much evolution at the level of allozymes, proteins such as albumin, and DNA, morphological evolution has been slow, and has been concentrated in relatively short spans of time. The dominant theme has been morphological stasis. An important contributing factor appears to be plasticity—behavioral, physiological, and developmental—which allows organisms to compensate environmental, and even genetic, perturbations without having to change morphologically. Organisms are self-produced and self-maintained systems, and we argue that the best measure of evolutionary adaptation is the persistence of this autopoietic system. Internal dynamics of the organism determine what change will occur and how it is to be expressed. Stable systems can be established which transcend species borders, and the fossil record offers no evidence with regard to speciation rates, or the relationship of speciation events to morphological evolution. We urge that more emphasis be placed on the organism in evolutionary studies.

Homoplasy: From Detecting Pattern to Determining Process and Mechanism of Evolution

Understanding the diversification of phenotypes through time—“descent with modification”—has been the focus of evolutionary biology for 150 years. If, contrary to expectations, similarity evolves in unrelated taxa, researchers are guided to uncover the genetic and developmental mechanisms responsible. Similar phenotypes may be retained from common ancestry (homology), but a phylogenetic context may instead reveal that they are independently derived, due to convergence or parallel evolution, or less likely, that they experienced reversal. Such examples of homoplasy present opportunities to discover the foundations of morphological traits. A common underlying mechanism may exist, and components may have been redeployed in a way that produces the “same” phenotype. New, robust phylogenetic hypotheses and molecular, genomic, and developmental techniques enable integrated exploration of the mechanisms by which similarity arises.

Multidimensional Analysis of an Evolving Lineage

To identify the forces directing organismal evolution, a general analytical system is developed to synthesize structuralist and Darwinian traditions in an explicitly historical framework. Morphological features of lungless salamanders are examined to identify hierarchical systems of developmental and functional constraint on evolution and their interactions with processes at the genic and populational levels. Characteristic patterns of change occur repeatedly in the evolutionary history of this group.

Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis

Amphibians highlight the global biodiversity crisis because ∼40% of all amphibian species are currently in decline. Species have disappeared even in protected habitats (e.g., the enigmatic extinction of the golden toad, Bufo periglenes, from Costa Rica). The emergence of a fungal pathogen, Batrachochytrium dendrobatidis (Bd), has been implicated in a number of declines that have occurred in the last decade, but few studies have been able to test retroactively whether Bd emergence was linked to earlier declines and extinctions. We describe a noninvasive PCR sampling technique that detects Bd in formalin-preserved museum specimens. We detected Bd by PCR in 83–90% (n = 38) of samples that were identified as positive by histology. We examined specimens collected before, during, and after major amphibian decline events at established study sites in southern Mexico, Guatemala, and Costa Rica. A pattern of Bd emergence coincident with decline at these localities is revealed—the absence of Bd over multiple years at all localities followed by the concurrent emergence of Bd in various species at each locality during a period of population decline. The geographical and chronological emergence of Bd at these localities also indicates a southbound spread from southern Mexico in the early 1970s to western Guatemala in the 1980s/1990s and to Monteverde, Costa Rica by 1987. We find evidence of a historical “Bd epidemic wave” that began in Mexico and subsequently spread to Central America. We describe a technique that can be used to screen museum specimens from other amphibian decline sites around the world.

Rapid diversification and dispersal during periods of global warming by plethodontid salamanders

A phylogeny and timescale derived from analyses of multilocus nuclear DNA sequences for Holarctic genera of plethodontid salamanders reveal them to be an old radiation whose common ancestor diverged from sister taxa in the late Jurassic and underwent rapid diversification during the late Cretaceous. A North American origin of plethodontids was followed by a continental-wide diversification, not necessarily centered only in the Appalachian region. The colonization of Eurasia by plethodontids most likely occurred once, by dispersal during the late Cretaceous. Subsequent diversification in Asia led to the origin of Hydromantes and Karsenia, with the former then dispersing both to Europe and back to North America. Salamanders underwent rapid episodes of diversification and dispersal that coincided with major global warming events during the late Cretaceous and again during the Paleocene–Eocene thermal optimum. The major clades of plethodontids were established during these episodes, contemporaneously with similar phenomena in angiosperms, arthropods, birds, and mammals. Periods of global warming may have promoted diversification and both inter- and transcontinental dispersal in northern hemisphere salamanders by making available terrain that shortened dispersal routes and offered new opportunities for adaptive and vicariant evolution.

Phylogeny and biogeography of the family Salamandridae (Amphibia: Caudata) inferred from complete mitochondrial genomes

Phylogenetic relationships of members of the salamander family Salamandridae were examined using complete mitochondrial genomes collected from 42 species representing all 20 salamandrid genera and five outgroup taxa. Weighted maximum parsimony, partitioned maximum likelihood, and partitioned Bayesian approaches all produce an identical, well-resolved phylogeny; most branches are strongly supported with greater than 90% bootstrap values and 1.0 Bayesian posterior probabilities. Our results support recent taxonomic changes in finding the traditional genera Mertensiella, Euproctus, and Triturus to be non-monophyletic species assemblages. We successfully resolved the current polytomy at the base of the salamandrid tree: the Italian newt genus Salamandrina is sister to all remaining salamandrids. Beyond Salamandrina, a clade comprising all remaining newts is separated from a clade containing the true salamanders. Among these newts, the branching orders of well-supported clades are: primitive newts (Echinotriton, Pleurodeles, and Tylototriton), New World newts (Notophthalmus-Taricha), Corsica-Sardinia newts (Euproctus), and modern European newts (Calotriton, Lissotriton, Mesotriton, Neurergus, Ommatotriton, and Triturus) plus modern Asian newts (Cynops, Pachytriton, and Paramesotriton).Two alternative sets of calibration points and two Bayesian dating methods (BEAST and MultiDivTime) were used to estimate timescales for salamandrid evolution. The estimation difference by dating methods is slight and we propose two sets of timescales based on different calibration choices. The two timescales suggest that the initial diversification of extant salamandrids took place in Europe about 97 or 69Ma. North American salamandrids were derived from their European ancestors by dispersal through North Atlantic Land Bridges in the Late Cretaceous ( approximately 69Ma) or Middle Eocene ( approximately 43Ma). Ancestors of Asian salamandrids most probably dispersed to the eastern Asia from Europe, after withdrawal of the Turgai Sea ( approximately 29Ma).

DISPERSAL OF VIVIPARITY ACROSS CONTACT ZONES IN IBERIAN POPULATIONS OF FIRE SALAMANDERS (SALAMANDRA) INFERRED FROM DISCORDANCE OF GENETIC AND MORPHOLOGICAL TRAITS

Abstract.— We used partial sequences of the cytochrome b mitochondrial DNA (mtDNA) gene, obtained from 76 individuals representing 45 populations of Iberian Salamandra salamandra plus 15 sequences of additional species of Salamandra and related genera, to investigate contact zones. These zones, identified by earlier allozymic and morphological analyses, are between populations of viviparous (S. s. bernardezi and S. s. fastuosa) and ovoviviparous (S. s. gallaica and S. s. terrestris) salamanders. The distribution of mtDNA and nuclear markers is mostly concordant at one contact zone (between S. s. gallaica and S. s. bernardezi), but at another (between S. s. fastuosa and S. s. terrestris) the markers are offset by about 250 km. The observed geographic variation fits a model of mtDNA capture. Among the potential mechanisms responsible for such discordance we favor a combination of range shifts due to climatic fluctuations and biased genetic admixture across moving contact zones. We apply our findings to the issue of possible homoplasy in the evolution of viviparity and conclude that viviparity likely arose only once within S. salamandra.