Person: Pierce, Naomi
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Pierce
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Naomi
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Pierce, Naomi
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Publication Herbivorous turtle ants obtain essential nutrients from a conserved nitrogen-recycling gut microbiome(Nature Publishing Group UK, 2018) Hu, Yi; Sanders, Jon G.; Łukasik, Piotr; D’Amelio, Catherine L.; Millar, John S.; Vann, David R.; Lan, Yemin; Newton, Justin A.; Schotanus, Mark; Kronauer, Daniel J. C.; Pierce, Naomi; Moreau, Corrie S.; Wertz, John T.; Engel, Philipp; Russell, Jacob A.Nitrogen acquisition is a major challenge for herbivorous animals, and the repeated origins of herbivory across the ants have raised expectations that nutritional symbionts have shaped their diversification. Direct evidence for N provisioning by internally housed symbionts is rare in animals; among the ants, it has been documented for just one lineage. In this study we dissect functional contributions by bacteria from a conserved, multi-partite gut symbiosis in herbivorous Cephalotes ants through in vivo experiments, metagenomics, and in vitro assays. Gut bacteria recycle urea, and likely uric acid, using recycled N to synthesize essential amino acids that are acquired by hosts in substantial quantities. Specialized core symbionts of 17 studied Cephalotes species encode the pathways directing these activities, and several recycle N in vitro. These findings point to a highly efficient N economy, and a nutritional mutualism preserved for millions of years through the derived behaviors and gut anatomy of Cephalotes ants.Publication Author Correction: Spatial fidelity of workers predicts collective response to disturbance in a social insect(Nature Publishing Group UK, 2018) Crall, James; Gravish, Nick; Mountcastle, Andrew M.; Kocher, Sarah D.; Oppenheimer, Robert L.; Pierce, Naomi; Combes, Stacey A.Publication Polygyny does not explain the superior competitive ability of dominant ant associates in the African ant‐plant, Acacia (Vachellia) drepanolobium(John Wiley and Sons Inc., 2017) Boyle, John H.; Martins, Dino J.; Pelaez, Julianne; Musili, Paul M.; Kibet, Staline; Ndung'u, S. Kimani; Kenfack, David; Pierce, NaomiAbstract The Acacia drepanolobium (also known as Vachellia drepanolobium) ant‐plant symbiosis is considered a classic case of species coexistence, in which four species of tree‐defending ants compete for nesting space in a single host tree species. Coexistence in this system has been explained by trade‐offs in the ability of the ant associates to compete with each other for occupied trees versus the ability to colonize unoccupied trees. We seek to understand the proximal reasons for how and why the ant species vary in competitive or colonizing abilities, which are largely unknown. In this study, we use RADseq‐derived SNPs to identify relatedness of workers in colonies to test the hypothesis that competitively dominant ants reach large colony sizes due to polygyny, that is, the presence of multiple egg‐laying queens in a single colony. We find that variation in polygyny is not associated with competitive ability; in fact, the most dominant species, unexpectedly, showed little evidence of polygyny. We also use these markers to investigate variation in mating behavior among the ant species and find that different species vary in the number of males fathering the offspring of each colony. Finally, we show that the nature of polygyny varies between the two commonly polygynous species, Crematogaster mimosae and Tetraponera penzigi: in C. mimosae, queens in the same colony are often related, while this is not the case for T. penzigi. These results shed light on factors influencing the evolution of species coexistence in an ant‐plant mutualism, as well as demonstrating the effectiveness of RADseq‐derived SNPs for parentage analysis.Publication Anchored phylogenomics illuminates the skipper butterfly tree of life(BioMed Central, 2018) Toussaint, Emmanuel F. A.; Breinholt, Jesse W.; Earl, Chandra; Warren, Andrew D.; Brower, Andrew V. Z.; Yago, Masaya; Dexter, Kelly M.; Espeland, Marianne; Pierce, Naomi; Lohman, David J.; Kawahara, Akito Y.Background: Butterflies (Papilionoidea) are perhaps the most charismatic insect lineage, yet phylogenetic relationships among them remain incompletely studied and controversial. This is especially true for skippers (Hesperiidae), one of the most species-rich and poorly studied butterfly families. Methods: To infer a robust phylogenomic hypothesis for Hesperiidae, we sequenced nearly 400 loci using Anchored Hybrid Enrichment and sampled all tribes and more than 120 genera of skippers. Molecular datasets were analyzed using maximum-likelihood, parsimony and coalescent multi-species phylogenetic methods. Results: All analyses converged on a novel, robust phylogenetic hypothesis for skippers. Different optimality criteria and methodologies recovered almost identical phylogenetic trees with strong nodal support at nearly all nodes and all taxonomic levels. Our results support Coeliadinae as the sister group to the remaining skippers, the monotypic Euschemoninae as the sister group to all other subfamilies but Coeliadinae, and the monophyly of Eudaminae plus Pyrginae. Within Pyrginae, Celaenorrhinini and Tagiadini are sister groups, the Neotropical firetips, Pyrrhopygini, are sister to all other tribes but Celaenorrhinini and Tagiadini. Achlyodini is recovered as the sister group to Carcharodini, and Erynnini as sister group to Pyrgini. Within the grass skippers (Hesperiinae), there is strong support for the monophyly of Aeromachini plus remaining Hesperiinae. The giant skippers (Agathymus and Megathymus) once classified as a subfamily, are recovered as monophyletic with strong support, but are deeply nested within Hesperiinae. Conclusions: Anchored Hybrid Enrichment sequencing resulted in a large amount of data that built the foundation for a new, robust evolutionary tree of skippers. The newly inferred phylogenetic tree resolves long-standing systematic issues and changes our understanding of the skipper tree of life. These resultsenhance understanding of the evolution of one of the most species-rich butterfly families. Electronic supplementary material The online version of this article (10.1186/s12862-018-1216-z) contains supplementary material, which is available to authorized users.Publication Author Correction: Herbivorous turtle ants obtain essential nutrients from a conserved nitrogen-recycling gut microbiome(Nature Publishing Group UK, 2018) Hu, Yi; Sanders, Jon G.; Łukasik, Piotr; D’Amelio, Catherine L.; Millar, John S.; Vann, David R.; Lan, Yemin; Newton, Justin A.; Schotanus, Mark; Kronauer, Daniel J. C.; Pierce, Naomi; Moreau, Corrie S.; Wertz, John T.; Engel, Philipp; Russell, Jacob A.Publication Asexual reproduction in introduced and native populations of the antCerapachys biroi(Wiley-Blackwell, 2012) Kronauer, Daniel J. C.; Pierce, Naomi; Keller, LaurentAsexual reproduction is particularly common among introduced species, probably because it helps to overcome the negative effects associated with low population densities during colonization. The ant Cerapachys biroi has been introduced to tropical and subtropical islands around the world since the beginning of the last century. In this species, workers can reproduce via thelytokous parthenogenesis. Here, we use genetic markers to reconstruct the history of anthropogenic introductions of C. biroi, and to address the prevalence of female parthenogenesis in introduced and native populations. We show that at least four genetically distinct lineages have been introduced from continental Asia and have led to the species' circumtropical establishment. Our analyses demonstrate that asexual reproduction dominates in the introduced range and is also common in the native range. Given that C. biroi is the only dorylomorph ant that has successfully become established outside of its native range, this unusual mode of reproduction probably facilitated the species' worldwide spread. On the other hand, the rare occurrence of haploid males and at least one clear case of sexual recombination in the introduced range show that C. biroi has not lost the potential for sex. Finally, we show that thelytoky in C. biroi probably has a genetic rather than an infectious origin, and that automixis with central fusion is the most likely underlying cytological mechanism. This is in accordance with what is known for other thelytokous eusocial Hymenoptera.Publication Genes Involved in the Evolution of Herbivory by a Leaf-Mining, Drosophilid Fly(Oxford University Press (OUP), 2012) Whiteman, Noah K.; Gloss, Andrew D.; Sackton, Timothy; Groen, Simon C.; Humphrey, Parris T.; Lapoint, Richard T.; Sønderby, Ida E.; Halkier, Barbara A.; Kocks, Christine; Ausubel, Frederick; Pierce, NaomiHerbivorous insects are among the most successful radiations of life. However, we know little about the processes underpinning the evolution of herbivory. We examined the evolution of herbivory in the fly, Scaptomyza flava, whose larvae are leaf miners on species of Brassicaceae, including the widely studied reference plant, Arabidopsis thaliana (Arabidopsis). Scaptomyza flava is phylogenetically nested within the paraphyletic genus Drosophila, and the whole genome sequences available for 12 species of Drosophila facilitated phylogenetic analysis and assembly of a transcriptome for S. flava. A time-calibrated phylogeny indicated that leaf mining in Scaptomyza evolved between 6 and 16 million years ago. Feeding assays showed that biosynthesis of glucosinolates, the major class of antiherbivore chemical defense compounds in mustard leaves, was upregulated by S. flava larval feeding. The presence of glucosinolates in wild-type (WT) Arabidopsis plants reduced S. flava larval weight gain and increased egg–adult development time relative to flies reared in glucosinolate knockout (GKO) plants. An analysis of gene expression differences in 5-day-old larvae reared on WT versus GKO plants showed a total of 341 transcripts that were differentially regulated by glucosinolate uptake in larval S. flava. Of these, approximately a third corresponded to homologs of Drosophila melanogaster genes associated with starvation, dietary toxin-, heat-, oxidation-, and aging-related stress. The upregulated transcripts exhibited elevated rates of protein evolution compared with unregulated transcripts. The remaining differentially regulated transcripts also contained a higher proportion of novel genes than the unregulated transcripts. Thus, the transition to herbivory in Scaptomyza appears to be coupled with the evolution of novel genes and the co-option of conserved stress-related genes.Publication Establishing criteria for higher-level classification using molecular data: the systematics ofPolyommatusblue butterflies (Lepidoptera, Lycaenidae)(Wiley-Blackwell, 2012) Talavera, Gerard; Lukhtanov, Vladimir A.; Pierce, Naomi; Vila, RogerMost taxonomists agree on the need to adapt current classifications to recognize monophyletic units. However, delineations between higher taxonomic units can be based on the relative ages of different lineages and/or the level of morphological differentiation. In this paper, we address these issues in considering the species-rich Polyommatus section, a group of butterflies whose taxonomy has been highly controversial. We propose a taxonomy-friendly, flexible temporal scheme for higher-level classification. Using molecular data from nine markers (6666 bp) for 104 representatives of the Polyommatus section, representing all but two of the 81 described genera/subgenera and five outgroups, we obtained a complete and well resolved phylogeny for this clade. We use this to revise the systematics of the Polyommatus blues, and to define criteria that best accommodate the described genera within a phylogenetic framework. First, we normalize the concept of section (Polyommatus) and propose the use of subtribe (Polyommatina) instead. To preserve taxonomic stability and traditionally recognized taxa, we designate an age interval (4–5 Myr) instead of a fixed minimum age to define genera. The application of these criteria results in the retention of 31 genera of the 81 formally described generic names, and necessitates the description of one new genus (Rueckbeilia gen. nov.). We note that while classifications should be based on phylogenetic data, applying a rigid universal scheme is rarely feasible. Ideally, taxon age limits should be applied according to the particularities and pre-existing taxonomy of each group. We demonstrate that the concept of a morphological gap may be misleading at the genus level and can produce polyphyletic genera, and we propose that recognition of the existence of cryptic genera may be useful in taxonomy.Publication The draft genome of a socially polymorphic halictid bee, Lasioglossum albipes(BioMed Central, 2013) Kocher, Sarah D; Li, Cai; Yang, Wei; Tan, Hao; Yi, Soojin V; Yang, Xingyu; Hoekstra, Hopi; Zhang, Guojie; Pierce, Naomi; Yu, Douglas WBackground: Taxa that harbor natural phenotypic variation are ideal for ecological genomic approaches aimed at understanding how the interplay between genetic and environmental factors can lead to the evolution of complex traits. Lasioglossum albipes is a polymorphic halictid bee that expresses variation in social behavior among populations, and common-garden experiments have suggested that this variation is likely to have a genetic component. Results: We present the L. albipes genome assembly to characterize the genetic and ecological factors associated with the evolution of social behavior. The de novo assembly is comparable to other published social insect genomes, with an N50 scaffold length of 602 kb. Gene families unique to L. albipes are associated with integrin-mediated signaling and DNA-binding domains, and several appear to be expanded in this species, including the glutathione-s-transferases and the inositol monophosphatases. L. albipes has an intact DNA methylation system, and in silico analyses suggest that methylation occurs primarily in exons. Comparisons to other insect genomes indicate that genes associated with metabolism and nucleotide binding undergo accelerated evolution in the halictid lineage. Whole-genome resequencing data from one solitary and one social L. albipes female identify six genes that appear to be rapidly diverging between social forms, including a putative odorant receptor and a cuticular protein. Conclusions: L. albipes represents a novel genetic model system for understanding the evolution of social behavior. It represents the first published genome sequence of a primitively social insect, thereby facilitating comparative genomic studies across the Hymenoptera as a whole.Publication Cross-continental comparisons of butterfly assemblages in tropical rainforests: implications for biological monitoring(Wiley-Blackwell, 2012) Basset, Yves; Eastwood, Rodney Gordon; Sam, Legi; Lohman, David; Novotny, Vojtech; Treuer, Tim; Miller, Scott E.; Weiblen, George D.; Pierce, Naomi; Bunyavejchewin, Sarayudh; Sakchoowong, Watana; Kongnoo, Pitoon; Osorio-Arenas, Miguel A.1. Standardised transect counts of butterflies in old-growth rainforests in different biogeographical regions are lacking. Such data are needed to mitigate the influence of methodological and environmental factors within and between sites and, ultimately, to discriminate between long-term trends and short-term stochastic changes in abundance and community composition. 2. We compared butterfly assemblages using standardised Pollard Walks in the understory of closed-canopy lowland tropical rainforests across three biogeographical regions: Barro Colorado Island (BCI), Panama; Khao Chong (KHC), Thailand; and Wanang (WAN), Papua New Guinea. 3. The length and duration of transects, their spatial autocorrelation, and number of surveys per year represented important methodological factors that strongly influenced estimates of butterfly abundance. Of these, the effect of spatial autocorrelation was most difficult to mitigate across study sites. 4. Butterfly abundance and faunal composition were best explained by air temperature, elevation, rainfall, wind velocity, and human disturbance at BCI and KHC. In the absence of weather data at WAN, duration of transects and number of forest gaps accounted for most of the explained variance, which was rather low in all cases (<33%). 5. Adequate monitoring of the abundance of common butterflies was achieved at the 50 ha BCI plot, with three observers walking each of 10 transects of 500 m for 30 min each, during each of four surveys per year. These datamay be standardised further after removing outliers of temperature and rainfall. Practical procedures are suggested to implement globalmonitoring of rainforest butterflies with Pollard Walks.