Journal Articles
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Item Impact of genetic background on allele selection in a highly mutable Candida albicans gene, PNG2(PLoS ONE, 2010) Zhang N; Cannon RD; Holland BR; Patchett ML; Schmid JIn many microbes rapid mutation of highly mutable contingency genes continually replenishes a pool of variant alleles from which the most suitable are selected, assisting in rapid adaptation and evasion of the immune response. In some contingency genes mutability is achieved through DNA repeats within the coding region. The fungal human pathogen Candida albicans has 2600 repeat-containing ORFs. For those investigated (ALS genes, HYR1, HYR2, CEK1, RLM1) many protein variants with differing amino acid repeat regions exist, as expected for contingency genes. However, specific alleles dominate in different clades, which is unexpected if allele variation is used for short-term adaptation. Generation of new alleles of repeat-containing C. albicans ORFs has never been observed directly. Here we present evidence for restrictions on the emergence of new alleles in a highly mutable C. albicans repeat-containing ORF, PNG2, encoding a putative secreted or cell surface glycoamidase. In laboratory cultures new PNG2 alleles arose at a rate of 2.8x10(-5) (confidence interval 3.3x10(-6)-9. 9x10(-5)) per cell per division, comparable to rates measured for contingency genes. Among 80 clinical isolates 17 alleles of different length and 23 allele combinations were distinguishable; sequence differences between repeat regions of identical size suggest the existence of 36 protein variants. Specific allele combinations predominated in different genetic backgrounds, as defined by DNA fingerprinting and multilocus sequence typing. Given the PNG2 mutation rate, this is unexpected, unless in different genetic backgrounds selection favors different alleles. Specific alleles or allele combinations were not preferentially associated with C. albicans isolates from particular body sites or geographical regions. Our results suggest that the mutability of PNG2 is not used for short-term adaptation or evasion of the immune system. Nevertheless the large number of alleles observed indicates that mutability of PNG2 may assist C. albicans strains from different genetic backgrounds optimize their interaction with the host in the long term.Item Within and between whorls: Comparative transcriptional profiling of Aquilegia and Arabidopsis(Public Library of Science, 2010) Voelckel C; Borevitz J; Kramer E; Hodges SBACKGROUND: The genus Aquilegia is an emerging model system in plant evolutionary biology predominantly because of its wide variation in floral traits and associated floral ecology. The anatomy of the Aquilegia flower is also very distinct. There are two whorls of petaloid organs, the outer whorl of sepals and the second whorl of petals that form nectar spurs, as well as a recently evolved fifth whorl of staminodia inserted between stamens and carpels. METHODOLOGY/PRINCIPAL FINDINGS: We designed an oligonucleotide microarray based on EST sequences from a mixed tissue, normalized cDNA library of an A. formosa x A. pubescens F2 population representing 17,246 unigenes. We then used this array to analyze floral gene expression in late pre-anthesis stage floral organs from a natural A. formosa population. In particular, we tested for gene expression patterns specific to each floral whorl and to combinations of whorls that correspond to traditional and modified ABC model groupings. Similar analyses were performed on gene expression data of Arabidopsis thaliana whorls previously obtained using the Ath1 gene chips (data available through The Arabidopsis Information Resource). CONCLUSIONS/SIGNIFICANCE: Our comparative gene expression analyses suggest that 1) petaloid sepals and petals of A. formosa share gene expression patterns more than either have organ-specific patterns, 2) petals of A. formosa and A. thaliana may be independently derived, 3) staminodia express B and C genes similar to stamens but the staminodium genetic program has also converged on aspects of the carpel program and 4) staminodia have unique up-regulation of regulatory genes and genes that have been implicated with defense against microbial infection and herbivory. Our study also highlights the value of comparative gene expression profiling and the Aquilegia microarray in particular for the study of floral evolution and ecology.Item Ancient DNA resolves identity and phylogeny of New Zealand's extinct and living quail (Coturnix sp.).(PUBLIC LIBRARY SCIENCE, 2009-07-28) Seabrook-Davison M; Huynen L; Lambert DM; Brunton DHBACKGROUND: The New Zealand quail, Coturnix novaezealandiae, was widespread throughout New Zealand until its rapid extinction in the 1870's. To date, confusion continues to exist concerning the identity of C. novaezealandiae and its phylogenetic relationship to Coturnix species in neighbouring Australia, two of which, C. ypsilophora and C. pectoralis, were introduced into New Zealand as game birds. The Australian brown quail, C. ypsilophora, was the only species thought to establish with current populations distributed mainly in the northern part of the North Island of New Zealand. Owing to the similarities between C. ypsilophora, C. pectoralis, and C. novaezealandiae, uncertainty has arisen over whether the New Zealand quail is indeed extinct, with suggestions that remnant populations of C. novaezealandiae may have survived on offshore islands. METHODOLOGY/PRINCIPAL FINDINGS: Using fresh and historical samples of Coturnix sp. from New Zealand and Australia, DNA analysis of selected mitochondrial regions was carried out to determine phylogenetic relationships and species status. Results show that Coturnix sp. specimens from the New Zealand mainland and offshore island Tiritiri Matangi are not the New Zealand quail but are genetically identical to C. ypsilophora from Australia and can be classified as the same species. Furthermore, cytochrome b and COI barcoding analysis of the New Zealand quail and Australia's C. pectoralis, often confused in museum collections, show that they are indeed separate species that diverged approximately 5 million years ago (mya). Gross morphological analysis of these birds suggests a parallel loss of sustained flight with very little change in other phenotypic characters such as plumage or skeletal structure. CONCLUSION/SIGNIFICANCE: Ancient DNA has proved invaluable for the detailed analysis and identification of extinct and morphologically cryptic taxa such as that of quail and can provide insights into the timing of evolutionary changes that influence morphology.Item Testing the Effect of Metabolic Rate on DNA Variability at the Intra-Specific Level(PLoS One, 2010-03-15) McGaughran, Angela; Holland, Barbara R.We tested the metabolic rate hypothesis (whereby rates of mtDNA evolution are postulated to be mediated primarily by mutagenic by-products of respiration) by examining whether mass-specific metabolic rate was correlated with root-to-tip distance on a set of mtDNA trees for the springtail Cryptopygus antarcticus travei from sub-Antarctic Marion Island. Using Bayesian analyses and a novel application of the comparative phylogenetic method, we did not find significant evidence that contemporary metabolic rates directly correlate with mutation rate (i.e., root-to-tip distance) once the underlying phylogeny is taken into account. However, we did find significant evidence that metabolic rate is dependent on the underlying mtDNA tree, or in other words, lineages with related mtDNA also have similar metabolic rates. We anticipate that future analyses which apply this methodology to datasets with longer sequences, more taxa, or greater variability will have more power to detect a significant direct correlation between metabolic rate and mutation rate. We conclude with suggestions for future analyses that would extend the preliminary approach applied here, in particular highlighting ways to tease apart oxidative stress effects from the effects of population size and/or selection coefficients operating on the molecular evolutionary rate.Item The molecular ecology of the extinct New Zealand Huia(Public Library of Science, 2009) Lambert D; Shepherd L; Huynen L; Beans Picon G; Walter G; Millar CThe extinct Huia (Heteralocha acutirostris) of New Zealand represents the most extreme example of beak dimorphism known in birds. We used a combination of nuclear genotyping methods, molecular sexing, and morphometric analyses of museum specimens collected in the late 19th and early 20th centuries to quantify the sexual dimorphism and population structure of this extraordinary species. We report that the classical description of Huia as having distinctive sex-linked morphologies is not universally correct. Four Huia, sexed as females had short beaks and, on this basis, were indistinguishable from males. Hence, we suggest it is likely that Huia males and females were indistinguishable as juveniles and that the well-known beak dimorphism is the result of differential beak growth rates in males and females. Furthermore, we tested the prediction that the social organisation and limited powers of flight of Huia resulted in high levels of population genetic structure. Using a suite of microsatellite DNA loci, we report high levels of genetic diversity in Huia, and we detected no significant population genetic structure. In addition, using mitochondrial hypervariable region sequences, and likely mutation rates and generation times, we estimated that the census population size of Huia was moderately high. We conclude that the social organization and limited powers of flight did not result in a highly structured population.Item The Emergence of Predators in Early Life: There was No Garden of Eden(PLoS One, 2009-06-03) de Nooijer, Silvester; Holland, Barbara R.; Penny, DavidBackground: Eukaryote cells are suggested to arise somewhere between 0.85 similar to 2.7 billion years ago. However, in the present world of unicellular organisms, cells that derive their food and metabolic energy from larger cells engulfing smaller cells (phagocytosis) are almost exclusively eukaryotic. Combining these propositions, that eukaryotes were the first phagocytotic predators and that they arose only 0.85 similar to 2.7 billion years ago, leads to an unexpected prediction of a long period (similar to 1-3 billion years) with no phagocytotes - a veritable Garden of Eden. Methodology: We test whether such a long period is reasonable by simulating a population of very simple unicellular organisms - given only basic physical, biological and ecological principles. Under a wide range of initial conditions, cellular specialization occurs early in evolution; we find a range of cell types from small specialized primary producers to larger opportunistic or specialized predators. Conclusions: Both strategies, specialized smaller cells and phagocytotic larger cells are apparently fundamental biological strategies that are expected to arise early in cellular evolution. Such early predators could have been 'prokaryotes', but if the earliest cells on the eukaryote lineage were predators then this explains most of their characteristic features.Item Computational identification of four spliceosomal snRNAs from the Deep-Branching Eukaryote Giardia intestinalis(PloS ONE, 2008) Chen XS; White WT; Collins LJ; Penny DRNAs processing other RNAs is very general in eukaryotes, but is not clear to what extent it is ancestral to eukaryotes. Here we focus on pre-mRNA splicing, one of the most important RNA-processing mechanisms in eukaryotes. In most eukaryotes splicing is predominantly catalysed by the major spliceosome complex, which consists of five uridine-rich small nuclear RNAs (U-snRNAs) and over 200 proteins in humans. Three major spliceosomal introns have been found experimentally in Giardia; one Giardia U-snRNA (U5) and a number of spliceosomal proteins have also been identified. However, because of the low sequence similarity between the Giardia ncRNAs and those of other eukaryotes, the other U-snRNAs of Giardia had not been found. Using two computational methods, candidates for Giardia U1, U2, U4 and U6 snRNAs were identified in this study and shown by RT-PCR to be expressed. We found that identifying a U2 candidate helped identify U6 and U4 based on interactions between them. Secondary structural modelling of the Giardia U-snRNA candidates revealed typical features of eukaryotic U-snRNAs. We demonstrate a successful approach to combine computational and experimental methods to identify expected ncRNAs in a highly divergent protist genome. Our findings reinforce the conclusion that spliceosomal small-nuclear RNAs existed in the last common ancestor of eukaryotes.Item Egg eviction imposes a recoverable cost of virulence in chicks of a brood parasite.(PloS, 2009-11-11) Anderson MG; Moskát C; Bán M; Grim T; Cassey P; Hauber MEBACKGROUND: Chicks of virulent brood parasitic birds eliminate their nestmates and avoid costly competition for foster parental care. Yet, efforts to evict nest contents by the blind and naked common cuckoo Cuculus canorus hatchling are counterintuitive as both adult parasites and large older cuckoo chicks appear to be better suited to tossing the eggs and young of the foster parents. METHODOLOGY/PRINCIPAL FINDINGS: Here we show experimentally that egg tossing imposed a recoverable growth cost of mass gain in common cuckoo chicks during the nestling period in nests of great reed warbler Acrocephalus arundinaceus hosts. Growth rates of skeletal traits and morphological variables involved in the solicitation of foster parental care remained similar between evictor and non-evictor chicks throughout development. We also detected no increase in predation rates for evicting nests, suggesting that egg tossing behavior by common cuckoo hatchlings does not increase the conspicuousness of nests. CONCLUSION: The temporary growth cost of egg eviction by common cuckoo hatchlings is the result of constraints imposed by rejecter host adults and competitive nestmates on the timing and mechanism of parasite virulence.Item Intergenic DNA sequences from the human X chromosome reveal high rates of global gene flow(BioMed Central, 2008) Cox M; Woerner A; Wall J; Hammer MBACKGROUND:Despite intensive efforts devoted to collecting human polymorphism data, little is known about the role of gene flow in the ancestry of human populations. This is partly because most analyses have applied one of two simple models of population structure, the island model or the splitting model, which make unrealistic biological assumptions.RESULTS:Here, we analyze 98-kb of DNA sequence from 20 independently evolving intergenic regions on the X chromosome in a sample of 90 humans from six globally diverse populations. We employ an isolation-with-migration (IM) model, which assumes that populations split and subsequently exchange migrants, to independently estimate effective population sizes and migration rates. While the maximum effective size of modern humans is estimated at \~{}10,000, individual populations vary substantially in size, with African populations tending to be larger (2,300-9,000) than non-African populations (300-3,300). We estimate mean rates of bidirectional gene flow at 4.8 x 10-4/generation. Bidirectional migration rates are \~{}5-fold higher among non-African populations (1.5 x 10-3) than among African populations (2.7 x 10-4). Interestingly, because effective sizes and migration rates are inversely related in African and non-African populations, population migration rates are similar within Africa and Eurasia (e.g., global mean Nm = 2.4).CONCLUSION:We conclude that gene flow has played an important role in structuring global human populations and that migration rates should be incorporated as critical parameters in models of human demography.Item On the road to diploidization? Homoeolog loss in independently formed populations of the allopolyploid Tragopogon miscellus (Asteraceae)(BioMed Central, 2009) Tate JA; Joshi P; Soltis KA; Soltis P; Soltis DBackground: Polyploidy (whole-genome duplication) is an important speciation mechanism,particularly in plants. Gene loss, silencing, and the formation of novel gene complexes are some ofthe consequences that the new polyploid genome may experience. Despite the recurrent natureof polyploidy, little is known about the genomic outcome of independent polyploidization events.Here, we analyze the fate of genes duplicated by polyploidy (homoeologs) in multiple individualsfrom ten natural populations of Tragopogon miscellus (Asteraceae), all of which formedindependently from T. dubius and T. pratensis less than 80 years ago.Results: Of the 13 loci analyzed in 84 T. miscellus individuals, 11 showed loss of at least one parentalhomoeolog in the young allopolyploids. Two loci were retained in duplicate for all polyploidindividuals included in this study. Nearly half (48%) of the individuals examined lost a homoeologof at least one locus, with several individuals showing loss at more than one locus. Patterns of losswere stochastic among individuals from the independently formed populations, except that the T.dubius copy was lost twice as often as T. pratensis.Conclusion: This study represents the most extensive survey of the fate of genes duplicated byallopolyploidy in individuals from natural populations. Our results indicate that the road to genomedownsizing and ultimate genetic diploidization may occur quickly through homoeolog loss, but withsome genes consistently maintained as duplicates. Other genes consistently show evidence ofhomoeolog loss, suggesting repetitive aspects to polyploid genome evolution.