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T Uzzell

Publications and source records attributed to T Uzzell.

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Antiquity of clonal salamander lineages revealed by mitochondrial DNA.

The existence of clonally reproducing vertebrates has often served as a foil in attempts to explain the near-ubiquity of sexual reproduction in eukaryotes, but the absence of recombination, with its attendant limitation of new genotypes to those produced through mutations, restricts the adaptive ability of clonal organisms. It has been argued, therefore, that clonal vertebrate taxa have short lifespans. Variation in mitochondrial DNA (mtDNA) within clonal populations is interpreted instead as reflecting multiple, although limited, independent hybridization events. On the basis of an analysis of an average of 373 nucleotide pairs, we report here that the mtDNA of clonal, hybrid, gynogenetic mole salamanders (Ambystoma, Ambystomatidae) differs by 5% or more from mtDNA of their closest possible sexual relatives (A. jeffersonianum, A. laterale and A. texanum). Assuming usual rates of mtDNA divergence, these lineages have persisted for about 5 million years, far longer than estimated for other clonal vertebrate populations. The low mtDNA variability in the clonal lineages suggests that they have undergone population reductions during the Pleistocene.

Ambystoma

Lampbrush and mitotic chromosomes of the hemiclonally reproducing hybrid Rana esculenta and its parental species.

Mitotic chromosomes of the European water frogs Rana ridibunda and Rana lessonae, the parental species of Rana esculenta, differ significantly in their centromeric regions: when C-banded or when made fluorescent, the centromeres of R. ridibunda (and of ridibunda chromosomes in R. esculenta) are visible as a conspicuous dark granule or as a conspicuous fluorescent spot; the centromeres of R. lessonae (and of the lessonae chromosomes in R. esculenta) are inconspicuous or not fluorescent. Lampbrush chromosomes of these three taxa are described in detail for the first time; those of R. ridibunda and R. lessonae differ significantly in morphostructural characters such as conspicuousness of centromeres and number, form, and location of giant loops as well as in chiasma frequency. Chromosomes of the two parental species can thus be distinguished when present in lampbrush complements of hybrids. Reproduction in both sexes of natural R. esculenta lineages is hemiclonal: only the unrecombined genome of one parental species, usually R. ridibunda, is transmitted to haploid gametes (hybridogenesis). In 18 hybrids from natural populations of Poland, somatic tissues had allodiploid complements with chromosomes from each parental species. In contrast, spermatocytes I of five males and oocytes I of seven of eight females (221 of 222 oocytes) were autodiploid and contained only R. ridibunda chromosomes that formed n bivalents. These 12 hybrids thus were hybridogenetic. A single female hybrid had oocytes I (33 of 34) with genomes of both parental species; they showed various disturbances including tetraploidy, reduced number of chiasmata, and incomplete synapsis resulting in univalents. This individual thus was not hybridogenetic. The irregular lampbrush patterns indicate that such hybrids will have severely reduced fertility and most of their successful gametes will result in allotriploid progeny.

Animals

Evolutionary history of the hybridogenetic hybrid frog Rana esculenta as deduced from mtDNA analyses.

mtDNA of the hybridogenetic hybrid frog Rana esculenta from Switzerland, Austria, and Poland was compared to mtDNA of the parental species R. ridibunda and R. lessonae using electrophoretic analysis of restriction enzyme fragments. Two mtDNA phenotypes, with 3.4% sequence divergence, are present in R. lessonae: type C is found in Poland, and type D is found in Switzerland. Rana ridibunda from Poland has either of two mtDNA phenotypes: type A is the typical ridibunda mtDNA, and type B is a lessonae mitochondrial genome, introgressed into R. ridibunda, that differs from type C mtDNA of R. lessonae by only 0.3%. Each of the three lessonae genomes differs from A, the typical ridibunda mtDNA, by approximately 8%. All four types of mtDNA (A and B of R. ridibunda, C and D of R. lessonae) are found in R. esculenta. Of 62 R. esculenta from Poland, 58 had type C, three had type A, and one had type B mtDNA. All nine R. esculenta from Switzerland had type D mtDNA. All three R. esculenta from Austria, from a population in which males of R. esculenta are rare, had ridibunda mtDNA, two having type B and one having type A. Both field observations and studies of mating preference indicate that the primary hybridizations that produce R. esculenta are between R. ridibunda females and R. lessonae males; thereafter, R. esculenta lineages are usually maintained by matings of R. esculenta females with R. lessonae males. The presence of ridibunda mtDNA in the three R. esculenta sampled from Austria, its occasional presence in R. esculenta populations in Poland, and its absence from R. esculenta in Switzerland support both the direction of the original hybridization and the rarity of formation of new R. esculenta lineages. The preponderance of R. esculenta individuals with lessonae mtDNA in our samples from central Europe suggests that most lineages have gone through at least one mating between an R. lessonae female and an R. esculenta male. This reveals a greater reproductive role for R. esculenta males than their partial sterility and infrequent matings would suggest.

Animals

Natural interspecies transfer of mitochondrial DNA in amphibians.

mtDNAs of two Central European water frog species, Rana ridibunda and Rana lessonae, were examined by electrophoresis of restriction enzyme fragments. Two types of mtDNA occur in R. ridibunda. One shares with mtDNA of R. lessonae 25.8% of 132 fragments generated by 19 enzymes, corresponding to a nucleotide sequence divergence of 8.1%; the other has diverged from R. lessonae mtDNA by only 0.3%. This latter type is a variant R. lessonae mtDNA that has been transferred into R. ridibunda; the introgression may have occurred via the hybridogenetic hybrid lineages collectively known as Rana esculenta. Of 37 R. ridibunda from Poland, 59% had the typical R. ridibunda mtDNA; 41% had the modified R. lessonae mtDNA as did a single individual from Switzerland (introduced). A single R. ridibunda from Turkey, outside the present range of R. lessonae, had the typical R. ridibunda mtDNA phenotype. Discordancies between inheritance of mitochondrial and nuclear genomes point up the danger of relying on a single molecular feature in reconstructing phylogeny. In addition, studies of mtDNA provide otherwise inaccessible information on complex evolutionary histories of closely related species. A knowledge of these complexities is important to an understanding of phylogenetic relationships and of the genetic processes that underlie the evolution of clonal taxa.

Animals

Fitting discrete probability distributions to evolutionary events.

The assumptions underlying the use of the Poisson distribution are essentially that the probability of an event is small but nearly identical for all occurrences and that the occurrence of an event does not alter the probability of recurrence of such events. These assumptions do not seem to be met for evolutionary events since (i) the probability of fixing nucleotide codon substitutions is not equal for all substitutions at a codon, and probably varies for the same substitution in different lineages; (ii) the probability of fixing codon substitutions varies among positions of a cistron; and (iii) the fixation of a nucleotide codon substitution at one position in a cistron modifies, and may even promote, the fixation of a codon substitution elsewhere along the cistron. Natural selection presumably is the causative factor that acts to modify the probability of a nucleotide codon substitution's being fixed in a population. The use of the negative binomial distribution is consistent with the evidence that selective pressure on amino acid or nucleotide codon positions varies both among codon positions of a cistron and at a particular position during evolutionary time. If the number of fixations of nucleotide codon substitutions per position of cistrons encoding cytochromes c are phyletically inferred (phylogeny based on a paleontological record) rather than phenetically inferred (based on paired comparisons of extant species' differences in the absence of a phylogeny) the distribution of these fixation data cannot be described adequately by a single Poisson distribution. The fit of these same data to a negative binomial distribution is very satisfactory. It has been argued that the fit of phenetically inferred fixation data, which do not take account of parallel or reverse fixations, to the Poisson distribution was supportive evidence for the hypothesis that protein evolution results from the fixation of selectively neutral codon substitutions. This argument now appears to be undercut by the evidence that data on nucleotide codon fixation are more probably distributed according to the negative binomial distribution. The fact that fixation data can be described by a particular discrete probability distribution does not of itself provide insight into the mechanisms of the evolutionary process. However, the facts-(i) that the assumptions underlying the use of the negative binomial distribution adequately deal with the varying probability of fixing amino acid or nucleotide codon substitutions at and among the positions of a cistron and (ii) that the negative binomial distribution provides an excellent fit for the phyletically inferred fixation data-suggest that the negative binomial is a very appropriate discrete probability distribution for describing evolutionary events. Amino acids or their nucleotide codon substitutions may be fixed at a position of a cistron as though selectively neutral relative to the codon being replaced, even though the codon position will not be selectively neutral, since many amino acids cannot function there. The negative binomial distribution treats this situation well whereas a single Poisson distribution could only be satisfactory if all codon positions that could vary were selectively neutral.

Amino Acid Sequence