Salamander Lineages Research Articles

Phalanx morphology in salamanders: A reflection of microhabitat use, life cycle or evolutionary constraints?

Morphological patterns are modeled by the interaction of functional, phylogenetic, ecological, and/or developmental constraints. In addition, the evolution of life cycle complexity can favor phenotypic diversity; however, the correlation between stages of development may constrain the evolution of some organs. Salamanders present microhabitat and life cycle diversity, providing an excellent framework for testing how these factors constrain phenotypic evolution. We reconstructed the morphological evolution of the terminal phalanx using a sample of 60 extinct and living species of salamanders. Using a geometric morphometric approach combined with comparative analyses, we further investigated the impact of phylogenetic, ecological, and/or life cycle factors on the shape of the terminal phalanx. We find that the phylogeny has some influence in determining the dorsal shape of the phalanges; whereas a relationship between microhabitat or life cycle and the dorsal and lateral shapes of the phalanx was not observed in the analyzed species. The allometric pattern found in the phalanx shape implies that small phalanges are more curved and with more truncated end than bigger phalanges. The evolutionary rate of phalanx shape was higher in the semiaquatic species, and the morphological disparity was significantly higher on biphasic groups. These results contradict the hypothesis that a complex life cycle constrains body shape. Finally, the phalanx shape of the salamander remains quite conserved from the Mesozoic. This configuration would allow them to occur in the different microhabitats occupied by the salamander lineages.

Driven to the edge: Species distribution modeling of a Clawed Salamander (Hynobiidae: Onychodactylus koreanus) predicts range shifts and drastic decrease of suitable habitats in response to climate change.

Climate change is one of the major threats to global amphibian diversity, and consequently, the species distribution is expected to shift considerably in the future. Therefore, predicting such shifts is important to guide conservation and management plans. Here, we used eight independent environmental variables and four representative concentration pathways (RCPs) to model the current and future habitat suitability of the Korean clawed salamander (Onychodactylus koreanus) and then defined the dispersal limits of the species using cost distance analysis. The current habitat suitability model generated using the maximum entropy algorithm was highly consistent with the known distribution of the species and had good predictive performance. Projections onto years 2050 and 2070 predicted a drastic decrease of habitat suitability across all RCPs, with up to 90.1% decrease of suitable area and 98.0% decrease of optimal area predicted from binary presence grids. The models also predicted a northeastward shift of habitat suitability toward high‐elevation areas and a persistence of suitability along the central ridge of the Baekdudaegan Range. This area is likely to become a climatic refugium for the species in the future, and it should be considered as an area of conservation priority. Therefore, we urge further ecological studies and population monitoring to be conducted across the range of O. koreanus. The vulnerability to rapid climate change is also shared by other congeneric species, and assessing the impacts of climate change on these other species is needed to better conserve this unique lineage of salamanders.

Pheromonal communication in urodelan amphibians.

Pheromonal communication is an ancient and pervasive sensory modality in urodelan amphibians. One family of salamander pheromones (the sodefrin precursor-like factor (SPF) family) originated 300 million years ago, at the origin of amphibians. Although salamanders are often thought of as relatively simple animals especially when compared to mammals, the pheromonal systems are varied and complex with nuanced effects on behavior. Here, we review the function and evolution of pheromonal signals involved in male-female reproductive interactions. After describing common themes of salamander pheromonal communication, we describe what is known about the rich diversity of pheromonal communication in each salamander family. Several pheromones have been described, ranging from simple, invariant molecules to complex, variable blends of pheromones. While some pheromones elicit overt behavioral responses, others have more nuanced effects. Pheromonal signals have diversified within salamander lineages and have experienced rapid evolution. Once receptors have been matched to pheromonal ligands, rapid advance can be made to better understand the olfactory detection and processing of salamander pheromones. In particular, a large number of salamander species deliver pheromones across the skin of females, perhaps reflecting a novel mode of pheromonal communication. At the end of our review, we list some of the many intriguing unanswered questions. We hope that this review will inspire a new generation of scientists to pursue work in this rewarding field.

Slender salamanders (genus Batrachoseps) reveal Southern California to be a center for the diversification, persistence, and introduction of salamander lineages.

BackgroundThe southern California biodiversity hotspot has had a complex geological history, with both plate tectonic forces and sea level changes repeatedly reconfiguring the region, and likely driving both lineage splittings and extinctions. Here we investigate patterns of genetic divergence in two species of slender salamanders (Plethodontidae: Batrachoseps) in this region. The complex geological history in combination with several organismal traits led us to predict that these species harbor multiple ancient mitochondrial lineages endemic to southern California. These species belong to a clade characterized by fine-scale mitochondrial structure, which has been shown to track ancient splits. Both focal species, Batrachoseps major and B. nigriventris, are relatively widely distributed in southern California, and estimated to have persisted there across millions of years. Recently several extralimital populations of Batrachoseps were found in the San Joaquin Valley of California, a former desert area that has been extensively modified for agriculture. The origins of these populations are unknown, but based on morphology, they are hypothesized to result from human-mediated introductions of B. major.MethodsWe sequenced the mitochondrial gene cytochrome b from a geographically comprehensive sampling of the mitochondrial lineages of B. major and B. nigriventris that are endemic to southern California. We used phylogenetic analyses to characterize phylogeographic structure and identify mitochondrial contact zones. We also included the San Joaquin Valley samples to test whether they resulted from introductions. We used a bootstrap resampling approach to compare the strength of isolation-by-distance in both Batrachoseps species and four other salamander species with which they co-occur in southern California.ResultsThe northern lineage of B. major harbors at least eight deeply differentiated, geographically cohesive mitochondrial subclades. We identify geographic contact between many of these mtDNA lineages and some biogeographic features that are concordant with lineage boundaries. Batrachoseps nigriventris also has multiple deeply differentiated clades within the region. Comparative analyses highlight the smaller spatial scales over which mitochondrial divergence accumulates in Batrachoseps relative to most other salamander species in southern California. The extralimital populations of Batrachoseps from the San Joaquin Valley are assigned to B. major and are shown to result from at least two independent introductions from different source populations. We also suggest that B. major on Catalina Island, where it is considered native, may be the result of an introduction. Some of the same traits that facilitate the build-up of deep phylogeographic structure in Batrachoseps likely also contribute to its propensity for introductions, and we anticipate that additional introduced populations will be discovered.

Hybridizing salamanders experience accelerated diversification

Whether hybridization generates or erodes species diversity has long been debated, but to date most studies have been conducted at small taxonomic scales. Salamanders (order Caudata) represent a taxonomic order in which hybridization plays a prevalent ecological and evolutionary role. We employed a recently developed model of trait-dependent diversification to test the hypothesis that hybridization impacts the diversification dynamics of species that are currently hybridizing. We find strong evidence supporting this hypothesis, showing that hybridizing salamander lineages have significantly greater net-diversification rates than non-hybridizing lineages. This pattern is driven by concurrently increased speciation rates and decreased extinction rates in hybridizing lineages. Our results support the hypothesis that hybridization can act as a generative force in macroevolutionary diversification.

Genomic Data Reveal Conserved Female Heterogamety in Giant Salamanders with Gigantic Nuclear Genomes.

Systems of genetic sex determination and the homology of sex chromosomes in different taxa vary greatly across vertebrates. Much progress remains to be made in understanding systems of genetic sex determination in non-model organisms, especially those with homomorphic sex chromosomes and/or large genomes. We used reduced representation genome sequencing to investigate genetic sex determination systems in the salamander family Cryptobranchidae (genera Cryptobranchus and Andrias), which typifies both of these inherent difficulties. We tested hypotheses of male- or female-heterogamety by sequencing hundreds of thousands of anonymous genomic regions in a panel of known-sex cryptobranchids and characterized patterns of presence/absence, inferred zygosity, and depth of coverage to identify sex-linked regions of these 56 gigabase genomes. Our results strongly support the hypothesis that all cryptobranchid species possess homologous systems of female heterogamety, despite maintenance of homomorphic sex chromosomes over nearly 60 million years. Additionally, we report a robust, non-invasive genetic assay for sex diagnosis in Cryptobranchus and Andrias which may have great utility for conservation efforts with these endangered salamanders. Co-amplification of these W-linked markers in both cryptobranchid genera provides evidence for long-term sex chromosome stasis in one of the most divergent salamander lineages. These findings inform hypotheses about the ancestral mode of sex determination in salamanders, but suggest that comparative data from other salamander families are needed. Our results further demonstrate that massive genomes are not necessarily a barrier to effective genome-wide sequencing and that the resulting data can be highly informative about sex determination systems in taxa with homomorphic sex chromosomes.

Ecological constraints associated with genome size across salamander lineages.

Salamanders have some of the largest, and most variable, genome sizes among the vertebrates. Larger genomes have been associated with larger cell sizes, lower metabolic rates, and longer embryonic and larval durations in many different taxonomic groups. These life-history traits are often important for dictating fitness under different environmental conditions, suggesting that a species' genome size may have the potential to constrain its ecological distribution. We test how genome size varies with the ephemerality of larval habitat across the salamanders, predicting that species with larger genomes will be constrained to more permanent habitats that permit slower development, while species with smaller genomes will be more broadly distributed across the gradient of habitat ephemerality. We found that salamanders with larger genomes are almost exclusively associated with permanent aquatic habitats. In addition, the evolutionary transition rate between permanent and ephemeral larval habitats is much higher in salamander lineages with smaller genome sizes. These patterns suggest that genome size may act as an evolutionary constraint on the ecological habitats of salamanders, restricting those species with large genomes and slower development to habitats with permanent sources of water.

Historical museum collections clarify the evolutionary history of cryptic species radiation in the world's largest amphibians.

Inaccurate taxonomic assessment of threatened populations can hinder conservation prioritization and management, with human‐mediated population movements obscuring biogeographic patterns and confounding reconstructions of evolutionary history. Giant salamanders were formerly distributed widely across China, and are interpreted as a single species, Andrias davidianus. Previous phylogenetic studies have identified distinct Chinese giant salamander lineages but were unable to associate these consistently with different landscapes, probably because population structure has been modified by human‐mediated translocations for recent commercial farming. We investigated the evolutionary history and relationships of allopatric Chinese giant salamander populations with Next‐Generation Sequencing methods, using historical museum specimens and late 20th‐century samples, and retrieved partial or near‐complete mitogenomes for 17 individuals. Samples from populations unlikely to have been affected by translocations form three clades from separate regions of China, spatially congruent with isolation by either major river drainages or mountain ranges. Pliocene–Pleistocene divergences for these clades are consistent with topographic modification of southern China associated with uplift of the Qinghai‐Tibet Plateau. General Mixed Yule Coalescent model analysis indicates that these clades represent separate species: Andrias davidianus (Blanchard, 1871) (northern Yangtze/Sichuan), Andrias sligoi (Boulenger, 1924) (Pearl/Nanling), and an undescribed species (Huangshan). Andrias sligoi is possibly the world's largest amphibian. Inclusion of additional reportedly wild samples from areas of known giant salamander exploitation and movement leads to increasing loss of biogeographic signal. Wild Chinese giant salamander populations are now critically depleted or extirpated, and conservation actions should be updated to recognize the existence of multiple species.

Genome-specific histories of divergence and introgression between an allopolyploid unisexual salamander lineage and two ancestral sexual species.

Quantifying introgression between sexual species and polyploid lineages traditionally thought to be asexual is an important step in understanding what drives the longevity of putatively asexual groups. Here, we capitalize on three recent innovations-ultraconserved element (UCE) sequencing, bioinformatic techniques for identifying genome-specific variation in polyploids, and model-based methods for evaluating historical gene flow-to measure the extent and tempo of introgression over the evolutionary history of an allopolyploid lineage of all-female salamanders and two ancestral sexual species. Our analyses support a scenario in which the genomes sampled in unisexual salamanders last shared a common ancestor with genomes in their parental species ∼3.4 million years ago, followed by a period of divergence between homologous genomes. Recently, secondary introgression has occurred at different times with each sexual species during the last 500,000 years. Sustained introgression of sexual genomes into the unisexual lineage is the defining characteristic of their reproductive mode, but this study provides the first evidence that unisexual genomes have undergone long periods of divergence without introgression. Unlike other sperm-dependent taxa in which introgression is rare, the alternating periods of divergence and introgression between unisexual salamanders and their sexual relatives could explain why these salamanders are among the oldest described unisexual animals.

Rapid phenotypic evolution following shifts in life cycle complexity.

Life cycle strategies have evolved extensively throughout the history of metazoans. The expression of disparate life stages within a single ontogeny can present conflicts to trait evolution, and therefore may have played a major role in shaping metazoan forms. However, few studies have examined the consequences of adding or subtracting life stages on patterns of trait evolution. By analysing trait evolution in a clade of closely related salamander lineages we show that shifts in the number of life cycle stages are associated with rapid phenotypic evolution. Specifically, salamanders with an aquatic-only (paedomorphic) life cycle have frequently added vertebrae to their trunk skeleton compared with closely related lineages with a complex aquatic-to-terrestrial (biphasic) life cycle. The rate of vertebral column evolution is also substantially lower in biphasic lineages, which may reflect the functional compromise of a complex cycle. This study demonstrates that the consequences of life cycle evolution can be detected at very fine scales of divergence. Rapid evolutionary responses can result from shifts in selective regimes following changes in life cycle complexity.

Tetrodotoxin Resistance: Natural Experiments to Understand Voltage-Gated Sodium Channel Structure and Function

Here we report data from our long-term studies of naturally occurring tetrodotoxin (TTX) resistant voltage-gated sodium channels (VGSCs) in TTX-resistant metazoans. These results identify critical biophysical properties in individual members of the VGSC gene family as well as differences between members. Members of the VGSC gene family are expressed in different excitable tissues and encode proteins with different biophysical properties. Characterizing isoform-specific properties is critical for understanding functional differences between excitable cells because, in nerve and muscle cells, the compliment of VGSCs expressed controls cell excitability. TTX is a neurotoxin used by diverse taxa including octopuses, newts, and fishes. The toxin causes paralysis and death by binding to and blocking the pore of VGSCs. Amino acid substitutions in the channel pore alter TTX binding as well as change biophysical properties such as voltage-dependence of activation and slow inactivation. Multiple species have evolved resistance to TTX through pore substitutions in their VGSCs. We have used these natural experiments to identify shared substitutions in TTX-resistant VGSC orthologs (e.g. NaV1.4) and paralogs (e.g. NaV1.5 and NaV1.7) of multiple TTX-resistant animals. By characterizing the properties of channels encoded by synthesized snake NaV1.4 genes, our work identifies interactions between pore residues and demonstrates that multiple convergent amino acid substitutions are compensatory. Specific amino acid changes rescue channel function when they occur in combination with substitutions that dramatically increase TTX resistance. Additionally, our work confirms that TTX resistance evolved prior to ecological exposure in snake and salamander lineages. These patterns suggest that selective pressures on channel function rather than a requirement for TTX resistance supported alterations in channel structure in our study taxa. By comparing convergent and divergent substitutions, we identify critical biophysical differences between members of the VGSC gene family.

Ecological opportunity, historical biogeography and diversification in a major lineage of salamanders

AbstractAimSpelerpini is a major radiation in the Plethodontidae, the largest family of salamanders. Seventy‐five percent of its species richness occurs in Eurycea, one of its six genera. We hypothesized that this was the result of the transgression of the Western Interior Seaway that provided ecological opportunity via ancestral range expansion into novel geographical regions, leading to an adaptive radiation.LocationEastern North America.MethodsWe sampled all but one species and two subspecies of extant Spelerpini, including several putative species, for four genes using maximum likelihood and Bayesian inference approaches to generate a comprehensive, robust phylogeny. We used five fossil calibrations to generate a chronogram, a likelihood framework to estimate the ancestral ranges/splits of all nodes on the phylogeny, and a Bayesian inference method to estimate diversification rate shifts putting the evolution of this group into a historical biogeographical context.ResultsA well‐resolved, strongly supported phylogeny of the Spelerpini was recovered. Eurycea is among the oldest genera within the Spelerpini, originating c. 42 Ma with an ancestor occurring in four of five physiographical regions, each corresponding to a major Eurycea lineage. There is strong support for a rate shift in the Edwards Plateau neotenic Eurycea.Main conclusionsA pattern of niche lability was found in the Spelerpini, as opposed to a pattern of niche conservatism found in other major radiations of plethodontids in eastern North America. The genus Eurycea dispersed widely into novel regions experiencing ecological opportunity as the Western Interior Seaway transgressed. This represents the first fossil calibrated and the most thoroughly sampled phylogeny of the group to date.

Heterogeneous vesicles in mucous epithelial cells of posterior esophagus of Chinese giant salamander (Andrias davidianus).

The Chinese giant salamander belongs to an old lineage of salamanders and endangered species. Many studies of breeding and disease regarding this amphibian had been implemented. However, the studies on the ultrastructure of this amphibian are rare. In this work, we provide a histological and ultra-structural investigation on posterior esophagus of Chinese giant salamander. The sections of amphibian esophagus were stained by hematoxylin & eosin (H&E). Moreover, the esophageal epithelium was observed by transmission electron microscopy (TEM). The results showed that esophageal epithelium was a single layer epithelium, which consisted of mucous cells and columnar cells. The esophageal glands were present in submucosa. The columnar cells were ciliated. According to the diverging ultrastructure of mucous vesicles, three types of mucous cells could be identified in the esophageal mucosa: i) electron-lucent vesicles mucous cell (ELV-MC); ii) electron-dense vesicles mucous cell (EDV-MC); and iii) mixed vesicles mucous cell (MV-MC).

The importance (or lack thereof) of niche divergence to the maintenance of a northern species complex: the case of the long-toed salamander (Ambystoma macrodactylum Baird).

The relative importance of ecological vs. non-ecological factors for the origin and maintenance of species is an open question in evolutionary biology. Young lineages--such as the distinct genetic groups that make up the ranges of many northern species--represent an opportunity to study the importance of ecological divergence during the early stages of diversification. Yet, few studies have examined the extent of niche divergence between lineages in previously glaciated regions and the role of ecology in maintaining the contact zones between them. In this study, we used tests of niche overlap in combination with ecological niche models to explore the extent of niche divergence between lineages of the long-toed salamander (Ambystoma macrodactylum Baird) species complex and to determine whether contact zones correspond to (divergent) niche limits. We found limited evidence for niche divergence between the different long-toed salamander lineages, substantial overlap in the predicted distribution of suitable climatic space for all lineages and range limits that are independent of niche limits. These results raise questions as to the importance of ecological divergence to the development of this widespread species complex and highlight the potential for non-ecological factors to play a more important role in the maintenance of northern taxa.

Extensive unidirectional introgression between two salamander lineages of ancient divergence and its evolutionary implications.

Hybridization and introgression, contrary to previous beliefs, are now considered to be widespread processes even among animal species. Nonetheless, the range of their possible outcomes and roles in moulding biodiversity patterns are still far from being fully appraised. Here we investigated the pattern of hybridization and introgression between Salamandrina perspicillata and S. terdigitata, two salamanders endemic to the Italian peninsula. Using a set of diagnostic or differentiated genetic markers (9 nuclear and 1 mitochondrial), we documented extensive unidirectional introgression of S. terdigitata alleles into the S. perspicillata gene pool in central Italy, indicating that barriers against hybridization were permeable when they came into secondary contact, and despite their ancient divergence. Nonetheless, purebred S. terdigitata, as well as F1, F2, and backcrosses were not found within the hybrid zone. Moreover, Bayesian analyses of population structure identified admixed populations belonging to a differentiated gene pool with respect to both parental populations. Overall, the observed genetic structure, together with their geographic pattern of distribution, suggests that Salamandrina populations in central Italy could have entered a distinct evolutionary pathway. How far they have gone along this pathway will deserve future investigation.

Individual performance in relation to cytonuclear discordance in a northern contact zone between long-toed salamander (Ambystoma macrodactylum) lineages.

Cytonuclear discordance in contact zones between related lineages is common, with mitochondrial clines often being displaced from clines in nuclear allele frequency. Proposed explanations for such a pattern include adaptive introgression of mtDNA or a neutral wake of mtDNA being left behind following hybrid zone movement. However, studies investigating these hypotheses are rare. Our previous survey of genetic variation in the long-toed salamander (Ambystoma macrodactylum) highlighted a potential case of cytonuclear discordance between two lineages in western Canada. Here, we use additional markers and samples to clarify the extent of this discordance. We simultaneously assess the feeding performance of individuals in a common environment to test for an association between mitotype and individual performance. The genetic results confirm a general pattern of cytonuclear discordance in the focal region. However, we also observed more limited introgression of a diagnostic nuclear marker. Intriguingly, although there were differences in individual performance associated with the transition between mitotypes, these differences were not fully explained by mitotype. Instead, the lowest performance was observed in individuals demonstrating the greatest mismatch between mtDNA and all nuclear markers, suggesting the potential for cytonuclear incompatibilities to be acting. These results highlight the complexity of understanding the causes and consequences of mtDNA introgression and cytonuclear discordance in contact zones.

A generalized K statistic for estimating phylogenetic signal from shape and other high-dimensional multivariate data.

Phylogenetic signal is the tendency for closely related species to display similar trait values due to their common ancestry. Several methods have been developed for quantifying phylogenetic signal in univariate traits and for sets of traits treated simultaneously, and the statistical properties of these approaches have been extensively studied. However, methods for assessing phylogenetic signal in high-dimensional multivariate traits like shape are less well developed, and their statistical performance is not well characterized. In this article, I describe a generalization of the K statistic of Blomberg et al. that is useful for quantifying and evaluating phylogenetic signal in highly dimensional multivariate data. The method (K(mult)) is found from the equivalency between statistical methods based on covariance matrices and those based on distance matrices. Using computer simulations based on Brownian motion, I demonstrate that the expected value of K(mult) remains at 1.0 as trait variation among species is increased or decreased, and as the number of trait dimensions is increased. By contrast, estimates of phylogenetic signal found with a squared-change parsimony procedure for multivariate data change with increasing trait variation among species and with increasing numbers of trait dimensions, confounding biological interpretations. I also evaluate the statistical performance of hypothesis testing procedures based on K(mult) and find that the method displays appropriate Type I error and high statistical power for detecting phylogenetic signal in high-dimensional data. Statistical properties of K(mult) were consistent for simulations using bifurcating and random phylogenies, for simulations using different numbers of species, for simulations that varied the number of trait dimensions, and for different underlying models of trait covariance structure. Overall these findings demonstrate that K(mult) provides a useful means of evaluating phylogenetic signal in high-dimensional multivariate traits. Finally, I illustrate the utility of the new approach by evaluating the strength of phylogenetic signal for head shape in a lineage of Plethodon salamanders.

Assessing trait covariation and morphological integration on phylogenies using evolutionary covariance matrices.

Morphological integration describes the degree to which sets of organismal traits covary with one another. Morphological covariation may be evaluated at various levels of biological organization, but when characterizing such patterns across species at the macroevolutionary level, phylogeny must be taken into account. We outline an analytical procedure based on the evolutionary covariance matrix that allows species-level patterns of morphological integration among structures defined by sets of traits to be evaluated while accounting for the phylogenetic relationships among taxa, providing a flexible and robust complement to related phylogenetic independent contrasts based approaches. Using computer simulations under a Brownian motion model we show that statistical tests based on the approach display appropriate Type I error rates and high statistical power for detecting known levels of integration, and these trends remain consistent for simulations using different numbers of species, and for simulations that differ in the number of trait dimensions. Thus, our procedure provides a useful means of testing hypotheses of morphological integration in a phylogenetic context. We illustrate the utility of this approach by evaluating evolutionary patterns of morphological integration in head shape for a lineage of Plethodon salamanders, and find significant integration between cranial shape and mandible shape. Finally, computer code written in R for implementing the procedure is provided.

Fetal adaptations for viviparity in amphibians

Live-bearing has evolved in all three orders of amphibians--frogs, salamanders, and caecilians. Developing young may be either yolk dependent, or maternal nutrients may be supplied after yolk is resorbed, depending on the species. Among frogs, embryos in two distantly related lineages develop in the skin of the maternal parents' backs; they are born either as advanced larvae or fully metamorphosed froglets, depending on the species. In other frogs, and in salamanders and caecilians, viviparity is intraoviductal; one lineage of salamanders includes species that are yolk dependent and born either as larvae or metamorphs, or that practice cannibalism and are born as metamorphs. Live-bearing caecilians all, so far as is known, exhaust yolk before hatching and mothers provide nutrients during the rest of the relatively long gestation period. The developing young that have maternal nutrition have a number of heterochronic changes, such as precocious development of the feeding apparatus and the gut. Furthermore, several of the fetal adaptations, such as a specialized dentition and a prolonged metamorphosis, are homoplasious and present in members of two or all three of the amphibian orders. At the same time, we know little about the developmental and functional bases for fetal adaptations, and less about the factors that drive their evolution and facilitate their maintenance.

Quantifying and Comparing Phylogenetic Evolutionary Rates for Shape and Other High-Dimensional Phenotypic Data

Many questions in evolutionary biology require the quantification and comparison of rates of phenotypic evolution. Recently, phylogenetic comparative methods have been developed for comparing evolutionary rates on a phylogeny for single, univariate traits (σ(2)), and evolutionary rate matrices (R) for sets of traits treated simultaneously. However, high-dimensional traits like shape remain under-examined with this framework, because methods suited for such data have not been fully developed. In this article, I describe a method to quantify phylogenetic evolutionary rates for high-dimensional multivariate data (σ2 mult), found from the equivalency between statistical methods based on covariance matrices and those based on distance matrices (R-mode and Q-mode methods). I then use simulations to evaluate the statistical performance of hypothesis-testing procedures that compare σ2 mult for two or more groups of species on a phylogeny. Under both isotropic and non-isotropic conditions, and for differing numbers of trait dimensions, the proposed method displays appropriate Type I error and high statistical power for detecting known differences in σ2 mult among groups. In contrast, the Type I error rate of likelihood tests based on the evolutionary rate matrix (R) increases as the number of trait dimensions (p) increases, and becomes unacceptably large when only a few trait dimensions are considered. Further, likelihood tests based on R cannot be computed when the number of trait dimensions equals or exceeds the number of taxa in the phylogeny (i.e., when p ≥ N). These results demonstrate that tests based on σ2 mult provide a useful means of comparing evolutionary rates for high-dimensional data that are otherwise not analytically accessible to methods based on the evolutionary rate matrix. This advance thus expands the phylogenetic comparative toolkit for high-dimensional phenotypic traits like shape. Finally, I illustrate the utility of the new approach by evaluating rates of head shape evolution in a lineage of Plethodon salamanders.