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1.
Mol Phylogenet Evol ; 79: 199-214, 2014 Oct.
Article in English | MEDLINE | ID: mdl-25017146

ABSTRACT

Short-tailed opossums (genus Monodelphis) represent one of the most speciose clades of New World marsupials, with 26 currently recognized species that collectively range from eastern Panama to northern Argentina. Here we present the first phylogenetic analyses of the genus based on dense taxonomic sampling and multiple genes. From most sampled species we obtained >4800bp of DNA sequence from one mitochondrial gene (CYTB), two autosomal exons (IRBP exon 1, BRCA1 exon 11), one autosomal intron (SLC38 intron 7), and one X-linked intron (OGT intron 14). Maximum-parsimony, maximum-likelihood and Bayesian analyses of these data strongly support the monophyly of Monodelphis and recover six major clades within the genus. Additionally, our analyses support previous suggestions that several nominal taxa are synonyms of other species (M. "sorex" of M. dimidiata, M. "theresa" of M. scalops, M. "rubida" and M. "umbristriata" of M. americana, and M. "maraxina" of M. glirina). By contrast, four unnamed lineages recovered by our analyses may represent new species. Reconstructions of ancestral states of two discrete characters-dorsal pelage color pattern and habitat-suggest that the most recent common ancestor of Monodelphis was uniformly colored (with unpatterned dorsal pelage) and inhabited moist forest. Whereas some dorsal pelage patterns appear to have evolved homoplastically in Monodelphis, dorsal stripes may have had a unique historical origin in this genus.


Subject(s)
Biological Evolution , Monodelphis/classification , Phylogeny , Animals , Bayes Theorem , Cell Nucleus/genetics , Exons , Genes, Mitochondrial , Introns , Likelihood Functions , Models, Genetic , Monodelphis/anatomy & histology , Monodelphis/genetics , Sequence Analysis, DNA
2.
Mol Phylogenet Evol ; 70: 137-51, 2014 Jan.
Article in English | MEDLINE | ID: mdl-24096147

ABSTRACT

Cryptic genetic diversity is a significant challenge for systematists faced with ever-increasing amounts of DNA sequence data. Computationally intensive coalescent-based analyses involving multiple unlinked loci are the only currently viable methods by which to assess the extent to which phenotypically similar populations (or metapopulations) are genetically distinct lineages. Although coalescent-based approaches have been tested extensively via simulations, few empirical studies have examined the impact of prior assumptions and dataset size on the ability to assess genetic isolation (evolutionary independence) using molecular data alone. Here, we consider the efficacy of two coalescent-based approaches (BPP and SpeDeSTEM) for testing the evolutionary independence of cryptic mtDNA haplogroups within three morphologically diagnosable species of Andean mouse opossums (Thylamys pallidior, T. sponsorius, and T. venustus). Fourteen anonymous nuclear loci, one X-linked nuclear intron, and one mitochondrial gene were analyzed for multiple individuals within each haplogroup of interest. We inferred individual gene trees for each locus and considered all of the nuclear loci jointly in a species-tree analysis. Using only the nuclear loci, we performed "species validation" tests for the cryptic mitochondrial lineages in SpeDeSTEM and BPP. For BPP, we also tested a wide range of prior assumptions, assessed performance of the rjMCMC algorithm, and examined how many loci were necessary to confidently delimit lineages. Results from BPP provided strong support for two independent evolutionary lineages each within T. pallidior, T. sponsorius, and T. venustus, whereas SpeDeSTEM results did not support splitting out mtDNA haplogroups as distinct evolutionary units. For most tests, BPP was robust to prior assumptions, although priors were shown to have an effect on both the strength of lineage recognition among T. venustus haplotypes and on the efficiency of the rjMCMC algorithm. Comparisons of results from datasets with different numbers of loci revealed that some cryptic lineages could be confidently delimited with as few as two loci.


Subject(s)
Marsupialia/genetics , Phylogeny , Animals , DNA, Mitochondrial/genetics , Genetic Loci , Genetic Variation , Haplotypes , Humans , Phylogeography , Sequence Analysis, DNA , South America
3.
Evolution ; 68(3): 684-95, 2014 Mar.
Article in English | MEDLINE | ID: mdl-24125654

ABSTRACT

The geological record of South American mammals is spatially biased because productive fossil sites are concentrated at high latitudes. As a result, the history of mammalian diversification in Amazonia and other tropical biomes is largely unknown. Here we report diversification analyses based on a time-calibrated molecular phylogeny of opossums (Didelphidae), a species-rich clade of mostly tropical marsupials descended from a Late Oligocene common ancestor. Optimizations of habitat and geography on this phylogeny suggest that (1) basal didelphid lineages inhabited South American moist forests; (2) didelphids did not diversify in dry-forest habitats until the Late Miocene; and (3) most didelphid lineages did not enter North America until the Pliocene. We also summarize evidence for an Early- to Middle-Miocene mass extinction event, for which alternative causal explanations are discussed. To the best of our knowledge, this study provides the first published molecular-phylogenetic evidence for mass extinction in any animal clade, and it is the first time that evidence for such an event (in any plant or animal taxon) has been tested for statistical significance. Potentially falsifying observations that could help discriminate between the proposed alternative explanations for didelphid mass extinction may be obtainable from diversification analyses of other sympatric mammalian groups.


Subject(s)
Evolution, Molecular , Genetic Variation , Opossums/genetics , Reproductive Isolation , Animals , Ecosystem , South America
4.
Toxicon ; 66: 1-6, 2013 May.
Article in English | MEDLINE | ID: mdl-23402839

ABSTRACT

Opossums and pitvipers are sympatric throughout most of the New World, but trophic relationships between these speciose clades have only recently attracted the attention of researchers. Although it is now known that some venom-resistant opossums prey on pitvipers, a review of the literature on diets shows that some Neotropical pitvipers prey on opossums. Interestingly, some pitviper species prey on opossums known or suspected to be venom resistant. If venom resistance and venom potency are coevolved traits, then these observations suggest that alternative outcomes may result in role-switching between victims and exploiters. Because molecular antagonists (e.g., venom toxins and toxin-neutralizing serum proteins) that could mediate such outcomes have been plausibly identified, this system is a potentially fruitful field for evolutionary research.


Subject(s)
Adaptation, Physiological/physiology , Biological Evolution , Opossums/physiology , Predatory Behavior/physiology , Snake Venoms/toxicity , Viperidae/physiology , Animals , Snake Venoms/metabolism
5.
Biol Rev Camb Philos Soc ; 87(4): 822-37, 2012 Nov.
Article in English | MEDLINE | ID: mdl-22404916

ABSTRACT

Mammals that prey on venomous snakes include several opossums (Didelphidae), at least two hedgehogs (Erinaceidae), several mongooses (Herpestidae), several mustelids, and some skunks (Mephitidae). As a group, these taxa do not share any distinctive morphological traits. Instead, mammalian adaptations for ophiophagy seem to consist only in the ability to resist the toxic effects of snake venom. Molecular mechanisms of venom resistance (as indicated by biochemical research on opossums, mongooses, and hedgehogs) include toxin-neutralizing serum factors and adaptive changes in venom-targeted molecules. Of these, toxin-neutralizing serum factors have received the most research attention to date. All of the toxin-neutralizing serum proteins discovered so far in both opossums and mongooses are human α1B-glycoprotein homologs that inhibit either snake-venom metalloproteinases or phospholipase A(2) myotoxins. By contrast, adaptive changes in venom-targeted molecules have received far less attention. The best-documented examples include amino-acid substitutions in mongoose nicotinic acetylcholine receptor that inhibit binding by α-neurotoxins, and amino-acid substitutions in opossum von Willebrand factor (vWF) that are hypothesized to weaken the bond between vWF and coagulopathic C-type lectins. Although multiple mechanisms of venom resistance are known from some species, the proteomic complexity of most snake venoms suggests that the evolved biochemical defences of ophiophagous mammals are likely to be far more numerous than currently recognized. Whereas most previous research in this field has been motivated by the potential for medical applications, venom resistance in ophiophagous mammals is a complex adaptation that merits attention from comparative biologists. Unfortunately, evolutionary inference is currently limited by ignorance about many relevant facts that can only be provided by future research.


Subject(s)
Blood Proteins/metabolism , Opossums/physiology , Snake Venoms/metabolism , Snake Venoms/toxicity , Adaptation, Physiological , Animals , Biological Evolution , Blood Proteins/chemistry , Protein Binding , Snake Venoms/chemistry
6.
PLoS One ; 6(6): e20997, 2011.
Article in English | MEDLINE | ID: mdl-21731638

ABSTRACT

The rapid evolution of venom toxin genes is often explained as the result of a biochemical arms race between venomous animals and their prey. However, it is not clear that an arms race analogy is appropriate in this context because there is no published evidence for rapid evolution in genes that might confer toxin resistance among routinely envenomed species. Here we report such evidence from an unusual predator-prey relationship between opossums (Marsupialia: Didelphidae) and pitvipers (Serpentes: Crotalinae). In particular, we found high ratios of replacement to silent substitutions in the gene encoding von Willebrand Factor (vWF), a venom-targeted hemostatic blood protein, in a clade of opossums known to eat pitvipers and to be resistant to their hemorrhagic venom. Observed amino-acid substitutions in venom-resistant opossums include changes in net charge and hydrophobicity that are hypothesized to weaken the bond between vWF and one of its toxic snake-venom ligands, the C-type lectin-like protein botrocetin. Our results provide the first example of rapid adaptive evolution in any venom-targeted molecule, and they support the notion that an evolutionary arms race might be driving the rapid evolution of snake venoms. However, in the arms race implied by our results, venomous snakes are prey, and their venom has a correspondingly defensive function in addition to its usual trophic role.


Subject(s)
Adaptation, Physiological/genetics , Evolution, Molecular , Feeding Behavior , Opossums/genetics , Viper Venoms/metabolism , Viperidae/physiology , von Willebrand Factor/genetics , Amino Acid Sequence , Animals , Bayes Theorem , Binding Sites , Crotalid Venoms/metabolism , Models, Molecular , Molecular Sequence Data , Phylogeny , Protein Structure, Tertiary , Quantitative Trait, Heritable , Selection, Genetic , von Willebrand Factor/chemistry
7.
Syst Biol ; 56(1): 83-96, 2007 Feb.
Article in English | MEDLINE | ID: mdl-17366139

ABSTRACT

Although theoretical studies have suggested that base-compositional heterogeneity can adversely affect phylogenetic reconstruction, only a few empirical examples of this phenomenon, mostly among ancient lineages (with divergence dates > 100 Mya), have been reported. In the course of our phylogenetic research on the New World marsupial family Didelphidae, we sequenced 2790 bp of the RAG1 exon from exemplar species of most extant genera. Phylogenetic analysis of these sequences recovered an anomalous node consisting of two clades previously shown to be distantly related based on analyses of other molecular data. These two clades show significantly increased GC content at RAG1 third codon positions, and the resulting convergence in base composition is strong enough to overwhelm phylogenetic signal from other genes (and morphology) in most analyses of concatenated datasets. This base-compositional convergence occurred relatively recently (over tens rather than hundreds of millions of years), and the affected gene region is still in a state of evolutionary disequilibrium. Both mutation rate and substitution rate are higher in GC-rich didelphid taxa, observations consistent with RAG1 sequences having experienced a higher rate of recombination in the convergent lineages.


Subject(s)
Base Composition/genetics , Evolution, Molecular , Homeodomain Proteins/genetics , Opossums/genetics , Phylogeny , Animals , Base Sequence , DNA Primers , Gene Conversion/genetics , Likelihood Functions , Models, Genetic , Molecular Sequence Data , Mutation/genetics , Sequence Analysis, DNA , Species Specificity
8.
Mol Phylogenet Evol ; 38(2): 363-80, 2006 Feb.
Article in English | MEDLINE | ID: mdl-16054401

ABSTRACT

Selection at the protein-level can influence nucleotide substitution patterns for protein-coding genes, which in turn can affect their performance as phylogenetic characters. In this study, we compare two protein-coding nuclear genes that appear to have evolved under markedly different selective constraints and evaluate how selection has shaped their phylogenetic signal. We sequenced 1,100+ bp of exon 6 of the gene encoding dentin matrix protein 1 (DMP1) from most of the currently recognized genera of New World opossums (family: Didelphidae) and compared these data to an existing matrix of sequences from the interphotoreceptor retinoid-binding protein gene (IRBP) and morphological characters. In comparison to IRBP, DMP1 has far fewer sites under strong purifying selection and exhibits a number of sites under positive directional selection. Furthermore, selection on the DMP1 protein appears to conserve short, acidic, serine-rich domains rather than primary amino acid sequence; as a result, DMP1 has significantly different nucleotide substitution patterns from IRBP. Using Bayesian methods, we determined that DMP1 evolves almost 30% faster than IRBP, has 2.5 times more variable sites, has less among-site rate heterogeneity, is skewed toward A and away from CT (IRBP has relatively even base frequencies), and has a significantly lower rate of change between adenine and any other nucleotide. Despite these different nucleotide substitution patterns, estimates of didelphid relationships based on separate phylogenetic analyses of these genes are remarkably congruent whether patterns of nucleotide substitution are explicitly modeled or not. Nonetheless, DMP1 contains more phylogenetically informative characters per unit sequence and resolves more nodes with higher support than does IRBP. Thus, for these two genes, relaxed functional constraints and positive selection appear to improve the efficiency of phylogenetic estimation without compromising its accuracy.


Subject(s)
Didelphis/classification , Evolution, Molecular , Extracellular Matrix Proteins/genetics , Retinol-Binding Proteins/genetics , Amino Acid Sequence , Amino Acid Substitution , Animals , Base Sequence , Cell Nucleus/genetics , Codon/genetics , Didelphis/genetics , Genes , Molecular Sequence Data , Phylogeny
9.
Evolution ; 46(6): 1918-1934, 1992 Dec.
Article in English | MEDLINE | ID: mdl-28567749

ABSTRACT

First principal components extracted from covariance matrices of log-transformed craniodental measurements closely approximate general size factors within field-collected samples representing 14 species in seven Neotropical muroid genera; because these samples are mixed-cross-sectional, scores are age-correlated and coefficients reflect postweaning growth allometries. Compared between congeners, sample first principal component coefficients are very similar, an observation that implies a nearly parallel orientation of ontogenetic trajectories in log-measurement space. On the assumption that a common general size factor (estimated as the first principal component of the pooled-within covariance matrix) accounts for most of the observed measurement covariance within samples, size-adjusted differences between congeneric species were estimated variable-by-variable in separate analyses of covariance; these differences reflect developmental adjustments of craniodental morphology that precede the measured interval of postweaning ontogeny. Vectors of size-adjusted difference coefficients are not similar from genus to genus, and a diversity of causal mechanisms is probably responsible. Analyses of captive-bred samples from two "species" of Zygodontomys provide prima facie evidence that size-adjusted differences estimated from field-collected samples have a genetic basis. Postweaning growth allometries in the muroid head skeleton may be conserved due to the biomechanical constraints of masticatory function; the apparent evolutionary plasticity of earlier ontogenetic adjustments may reflect the absence of such constraints in the fetus or suckling pup. The relevance of these results for current theories concerning the developmental genetics of mammalian morphometric evolution is discussed.

10.
Evolution ; 44(6): 1568-1587, 1990 Sep.
Article in English | MEDLINE | ID: mdl-28564313

ABSTRACT

Analyses of craniodental measurement data from 15 wild-collected population samples of the Neotropical muroid rodent genus Zygodontomys reveal consistent patterns of relative variability and correlation that suggest a common latent structure. Eigenanalysis of each sample covariance matrix of logarithms yields a first principal component that accounts for a large fraction of the total variance. Variances of subsequent sample principal components are much smaller, and the results of bootstrap resampling together with asymptotic statistics suggest that characteristic roots of the covariance matrix after the first are seldom distinct. The coefficients of normalized first principal components are strikingly similar from sample to sample: inner products of these vectors reveal an average between-sample correlation of 0.989, and the mean angle of divergence is only about eight degrees. Since first principal component coefficients identify the same contrasts among variables as comparisons of relative variability and correlation, we conclude that a single factor accounts for most of the common latent determination of these sample dispersions. Analyses of variance based on toothwear (a coarse index of age) and sex in the wild-collected samples, and on known age and sex in a captive-bred population, reveal that specimen scores on sample first principal components are age- and sex-dependent; residual sample dispersion, however, is essentially unaffected by age, sex, or age × sex interaction. The sample first principal component therefore reflects the covariance among measured dimensions induced by general growth, and its coefficients are interpretable as exponents of postnatal growth allometry. Path-analytic models that incorporate prior knowledge of the equivalent allometric effects of general growth within these samples can be used to decompose the between-sample variance by factors corresponding to other ontogenetic mechanisms of form change. The genetic or environmental determinants of differences in sample mean phenotypes induced by such mechanisms, however, can be demonstrated only by experiment.

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