Matthew C. Brandley

Why does a trait evolve multiple times within a clade? Repeated evolution of snakelike body form in squamate reptiles

Abstract Why does a trait evolve repeatedly within a clade? When examining the evolution of a trait, evolutionary biologists typically focus on the selective advantages it may confer and the genetic and developmental mechanisms that allow it to vary. Although these factors may be necessary to explain why a trait evolves in a particular instance, they may not be sufficient to explain phylogenetic patterns of repeated evolution or conservatism. Instead, other factors may also be important, such as biogeography and competitive interactions. In squamate reptiles (lizards and snakes) a dramatic transition in body form has occurred repeatedly, from a fully limbed, lizardlike body form to a limb-reduced, elongate, snakelike body form. We analyze this trait in a phylogenetic and biogeographic context to address why this transition occurred so frequently. We included 261 species for which morphometric data and molecular phylogenetic information were available. Among the included species, snakelike body form has evolved about 25 times. Most lineages of snakelike squamates belong to one of two “ecomorphs,” either short-tailed burrowers or long-tailed surface dwellers. The repeated origins of snakelike squamates appear to be associated with the in situ evolution of these two ecomorphs on different continental regions (including multiple origins of the burrowing morph within most continents), with very little dispersal of most limb-reduced lineages between continental regions. Overall, the number of repeated origins of snakelike morphology seems to depend on large-scale biogeographic patterns and community ecology, in addition to more traditional explanations (e.g., selection, development).

Rates and Patterns in the Evolution of Snake-Like Body Form in Squamate Reptiles: Evidence for Repeated Re-Evolution of Lost Digits and Long-Term Persistence of Intermediate Body Forms

Abstract An important challenge in evolutionary biology is to understand how major changes in body form arise. The dramatic transition from a lizard-like to snake-like body form in squamate reptiles offers an exciting system for such research because this change is replicated dozens of times. Here, we use morphometric data for 258 species and a time-calibrated phylogeny to explore rates and patterns of body-form evolution across squamates. We also demonstrate how time-calibrated phylogenies may be used to make inferences about the time frame over which major morphological transitions occur. Using the morphometric data, we find that the transition from lizard-like to snake-like body form involves concerted evolution of limb reduction, digit loss, and body elongation. These correlations are similar across squamate clades, despite very different ecologies and >180 million years (My) of divergence. Using the time-calibrated phylogeny and ancestral reconstructions, we find that the dramatic transition between these body forms can occur in 20 My or less, but that seemingly intermediate morphologies can also persist for tens of millions of years. Finally, although loss of digits is common, we find statistically significant support for at least six examples of the re-evolution of lost digits in the forelimb and hind limb.

Accommodating Heterogenous Rates of Evolution in Molecular Divergence Dating Methods: An Example Using Intercontinental Dispersal of Plestiodon (Eumeces) Lizards

Identifying and dating historical biological events is a fundamental goal of evolutionary biology, and recent analytical advances permit the modeling of factors known to affect both the accuracy and the precision of molecular date estimates. As the use of multilocus data sets becomes increasingly routine, it becomes more important to evaluate the potentially confounding effects of rate heterogeneity both within (e.g., codon positions) and among loci when estimating divergence times. Here, using Plestiodon lizards as a test case, we examine the effects of accommodating rate heterogeneity among data partitions on divergence time estimation. Plestiodon inhabits both East Asia and North America, yet both the geographic origin of the genus and timing of dispersal between the continents have been debated. For each of the eight independently evolving loci and a combined data set, we conduct single model and partitioned analyses. We found that extreme saturation has obscured the underlying rate of evolution in the mitochondrial DNA (mtDNA), resulting in severe underestimation of the rate in this locus. As a result, the age of the crown Plestiodon clade was overestimated by 15-17 Myr by the unpartitioned analysis of the combined loci data. However, the application of partition-specific models to the combined data resulted in ages that were fully congruent with those inferred by the individual nuclear loci. Although partitioning improved divergence date estimates of the mtDNA-only analysis, the ages were nonetheless overestimated, thus indicating an inadequacy of our current models to capture the complex nature of mtDNA evolution in over large time scales. Finally, the statistically incongruent age distributions inferred by the partitioned and unpartitioned analyses of the combined data support mutually exclusive hypotheses of the timing of intercontinental dispersal of Plestiodon from Asia to North America. Analyses that best capture the rate of evolution in the combined data set infer that this exchange occurred via Beringia ∼18.0-30 Ma.

PHYLOGENY, ECOMORPHOLOGICAL EVOLUTION, AND HISTORICAL BIOGEOGRAPHY OF THE ANOLIS CRISTATELLUS SERIES

Abstract To determine the evolutionary relationships within the Anolis cristatellus series, we employed phylogenetic analyses of previously published karyotype and allozyme data as well as newly collected morphological data and mitochondrial DNA sequences (fragments of the 12S RNA and cytochrome b genes). The relationships inferred from continuous maximum likelihood reanalyses of allozyme data were largely poorly supported. A similar analysis of the morphological data gave strong to moderate support for sister relationships of the two included distichoid species, the two trunk-crown species, the grass-bush species A. poncensis and A. pulchellus, and a clade of trunk-ground and grass-bush species. The results of maximum likelihood and Bayesian analyses of the 12S, cyt b, and combined mtDNA data sets were largely congruent, but nonetheless exhibit some differences both with one another and with those based on the morphological data. We therefore took advantage of the additive properties of likelihoods to compare alternative phylogenetic trees and determined that the tree inferred from the combined 12S and cyt b data is also the best estimate of the phylogeny for the morphological and mtDNA data sets considered together. We also performed mixed-model Bayesian analyses of the combined morphology and mtDNA data; the resultant tree was topologically identical to the combined mtDNA tree with generally high nodal support. This phylogenetic hypothesis has a basal dichotomy between the Hispañolan distichoids and the bimaculatus series, on the one hand, and the cristatellus series inhabiting the Puerto Rican Island Bank, its satellite islands, the Bahamas, and St. Croix, on the other. The trunk-crown species form a clade, while the trunk-ground and grass-bush species do not as A. gundlachi, a trunk-ground species, is nested within a clade of grass-bush species. The patterns of relationships among the trunk-ground and grass-bush species suggest that one of these ecomorphs may have been ancestral to the other and that one or both evolved convergently. In the context of our preferred phylogeny and divergence dates estimated by NPRS analyses, we propose several biogeographical hypotheses that explain the current distribution of the cristatellus series. The presence of endemic species on the islands of the Bahamas, Desecheo, Mona, Monita, and St. Croix are likely due to over-water dispersal. Vicariance resulting from Pliocene or Pleistocene changes in sea levels likely explains the occurrence of A. cristatellus (including A. ernestwilliamsi), A. pulchellus, and A. stratulus on different islands of the Puerto Rican Bank.

Are unequal clade priors problematic for Bayesian phylogenetics

Although Bayesian phylogenetic methodologies were first developed in the 1960s (Felsenstein, 1968, 2004), the approach remained relatively obscure until the initial release of the software application MrBayes (Huelsenbeck and Ronquist, 2001). Since that time, the popularity of Bayesian phylogenetics has increased tremendously, and it now must be considered a primary method of analysis on par with maximum likelihood, parsimony, and distance methods. The popularity of Bayesian analysis can be attributed to computational efficiencies that allow for explicit model-based analyses of large data sets in real time with simultaneous estimation of nodal support in the form of posterior probability values. Despite the initial enthusiasm generated by the availability of a fast likelihood-based approach, Bayesian phylogenetic analysis remains somewhat controversial. Much of the controversy is focused on two related issues: (1) the relationship between posterior probability values and nonparametric bootstrap proportions with the nagging suspicion that posterior probabilities are too liberal (e.g., Suzuki et al., 2002), and (2) the influence of prior probabilities, especially so-called flat or uninformative priors, on resulting Bayesian posteriors (Felsenstein, 2004; Zwickl and Holder, 2004; Pickett and Randle, 2005). Although there has been a spate of simulation studies published during the past 2 years, most (Alfaro et al., 2003; Cummings et al. 2003; Douady et al., 2003; Erixon et al., 2003; Huelsenbeck and Rannala, 2004; Wilcox et al., 2002) have focused on the relationship between posterior probabilities and bootstrap proportions. The relative impact of priors on posteriors has only recently received the detailed study that is required to determine if current Bayesian implementations are appropriate and, if not, how they might be corrected (e.g., Zwickl and Holder, 2004; Lewis et al., 2005). Bayesian phylogenetic analysis requires the designation of prior probabilities for each parameter in the analysis including those for alternative tree topologies, branch lengths, and the nucleotide substitution model. In each case, we usually have little a priori information that would allow us to select an appropriate informative prior distribution, thus researchers generally attempt to accommodate their ignorance by applying uninformative priors. Because the posterior probability is proportional to the product of the prior probability and the likelihood, a truly uninformative prior should allow the likelihood function to drive the outcome of the analysis (Huelsenbeck et al., 2002; Lewis, 2001a; Zwickl and Holder, 2004). Unfortunately, the designation of truly uninformative priors is notoriously difficult (see Kass and Wasserman, 1996; Zwickl and Holder, 2004), and advocates proceed with the hope that the likelihood will overwhelm inappropriately informative priors when they cannot be avoided. The viability of Bayesian phylogenetics may depend on inferences being robust to these unavoidably informative priors. In a recent article, Pickett and Randle (2005; hereafter referred to as “PR” for the sake of brevity) provide one of the first investigations of the relationship between prior and posterior probabilities for Bayesian phylogenetic analysis when applying inappropriately informative priors (see also Zwickl and Holder, 2004). They correctly recognized that the designation of uninformative priors on the tree topology does not result in uninformative clade priors (we note that the prior probability distribution of clades can be viewed either as the joint distribution over all splits, or as the marginal prior distribution for each individual split. Here we are concerned with the former interpretation). This point was clearly illustrated by PR with a simple example—if one considers a fully bifurcating five-taxon tree, there are 15 reconstructions linking each possible pair of taxa and only 9 reconstructions linking any combination of three taxa. Thus, with rooted trees, the prior probability of larger and smaller clades will be greater than those on clades of intermediate size. All else being equal, the posterior probabilities of smaller and larger clades should be inflated relative to those of clades of intermediate size. PR presented two examples of this phenomenon by analyzing both empirical DNA and contrived data sets. We first focus on the contrived data because we believe these are the only results in the PR study that clearly indicate that informative

Homoplasy and Clade Support

Distinguishing phylogenetic signal from homoplasy (shared similarities among taxa that do not arise by common ancestry) is an implicit goal of any phylogenetic study. Large amounts of homoplasy can interfere with accurate tree inference, and it is expected that common measures of clade support, including bootstrap proportions and Bayesian posterior probabilities, should also be impacted to some degree by homoplasy. Through data simulation and analysis of 38 empirical data sets, we show that high amounts of homoplasy will affect all measures of clade support in a manner that is dependent on clade size. More specifically, the smallest taxon bipartitions in an unrooted tree topology will receive higher support relative to clades of intermediate sizes, even when all clades are supported by the same amount of data. We determine that the ultimate causes of this effect are the inclusion of random trees (due to homoplasy) during bootstrap resampling and Markov chain Monte Carlo (MCMC) topology searching and the higher relative proportion of small taxon bipartitions (i.e., 2 or 3 taxa) to larger sized bipartitions. However, the use of explicit model-based methods, especially Bayesian MCMC methods, effectively overcomes this clade size effect even when very small amounts of phylogenetic signal are present. We develop a post hoc statistic, the clade disparity index (CDI), to measure both the relative magnitude of the clade size effect and its statistical significance. In analyses of both simulated and empirical data, CDI values indicate that Bayesian MCMC analyses are substantially more likely to estimate clade support values that are uncorrelated with clade size than are maximum parsimony and maximum likelihood bootstrap analyses and thus less affected by homoplasy. These results may be especially relevant to deep phylogenetic problems, such as reconstructing the tree of life, as they represent the largest possible extremes of time and evolutionary rates, 2 factors that cause homoplasy.

Bermuda as an Evolutionary Life Raft for an Ancient Lineage of Endangered Lizards

Oceanic islands are well known for harboring diverse species assemblages and are frequently the basis of research on adaptive radiation and neoendemism. However, a commonly overlooked role of some islands is their function in preserving ancient lineages that have become extinct everywhere else (paleoendemism). The island archipelago of Bermuda is home to a single species of extant terrestrial vertebrate, the endemic skink Plestiodon (formerly Eumeces) longirostris. The presence of this species is surprising because Bermuda is an isolated, relatively young oceanic island approximately 1000 km from the eastern United States. Here, we apply Bayesian phylogenetic analyses using a relaxed molecular clock to demonstrate that the island of Bermuda, although no older than two million years, is home to the only extant representative of one of the earliest mainland North American Plestiodon lineages, which diverged from its closest living relatives 11.5 to 19.8 million years ago. This implies that, within a short geological time frame, mainland North American ancestors of P. longirostris colonized the recently emergent Bermuda and the entire lineage subsequently vanished from the mainland. Thus, our analyses reveal that Bermuda is an example of a “life raft” preserving millions of years of unique evolutionary history, now at the brink of extinction. Threats such as habitat destruction, littering, and non-native species have severely reduced the population size of this highly endangered lizard.

Karyotype and Relationships of Anolis desechensis

Abstract We determined the karyotype of Anolis desechensis and compared it with the known karyotypes of other members of the Anolis cristatellus series. The diploid (2N) number of chromosomes of two male A. desechensis was 27, with six pairs of large metacentric macrochromosomes, six pairs of microchromosomes of gradually decreasing size, and sex chromosome heteromorphism (three sex chromosomes, X1X2Y). This chromosome complement is identical to that of A. cristatellus and A. scriptus, thus providing additional evidence of a close relationship to these taxa. The evolution of chromosome number within the cristatellus series appears to have involved minimal homoplasy and therefore contains useful phylogenetic information.

Natural History Observations of the Ichthyological and Herpetological Fauna on the Island of Curaçao (Netherlands)

ABSTRACT Despite increasing popularity of the island as an ecotourist destination, the ecology and natural history of many organisms native to the Lesser Antillean island of Curaçao have remained enigmatic. We document multiple new observations of the behavioral ecology of several terrestrial and aquatic vertebrates that inhabit Curaçao. We present the first report of avian predation on the endemic Curaçao whiptail lizard, Cnemidophorus murinus, suggesting these lizards play a potentially important role in this islands food web. We also document the first instance of predation by the introduced tropical house gecko. Hemidactylus mabouia, on the native Antilles gecko, Gonatodes antillensis. Tropical house geckos are thought to be displacing native geckos through a combination of niche displacement and competitive exclusion, and our finding suggests that predation on smaller native lizards may be another factor aiding the success of this introduced gecko on Curaçao. We also present repeated observational evidence that juvenile bluehead wrasses (Thalassoma bifasciatum) seek refuge among the sessile and venomous giant Caribbean sea anemones (Condylactis gigantean).