Publications

2011
Archetti M, Ubeda F, Fudenberg D, Green J, Pierce NE, Yu DW. Let the Right One In: A Microeconomic Approach to Partner Choice in Mutualisms. American Naturalist. 2011;177 :75-85.Abstract

One of the main problems impeding the evolution of cooperation is partner choice. When information is asymmetric (the quality of a potential partner is known only to himself), it may seem that partner choice is not possible without signaling. Many mutualisms, however, exist without signaling, and the mechanisms by which hosts might select the right partners are unclear. Here we propose a general mechanism of partner choice, "screening," that is similar to the economic theory of mechanism design. Imposing the appropriate costs and rewards may induce the informed individuals to screen themselves according to their types and therefore allow a noninformed individual to establish associations with the correct partners in the absence of signaling. Several types of biological symbioses are good candidates for screening, including bobtail squid, ant-plants, gut microbiomes, and many animal and plant species that produce reactive oxygen species. We describe a series of diagnostic tests for screening. Screening games can apply to the cases where by-products, partner fidelity feedback, or host sanctions do not apply, therefore explaining the evolution of mutualism in systems where it is impossible for potential symbionts to signal their cooperativeness beforehand and where the host does not punish symbiont misbehavior.

2011_archetti_et_al_let_the_right_one_in.pdf
Whiteman NK, Groen SC, Chevasco D, Bear A, Beckwith N, Gregory TR, Denoux C, Mammarella N, Ausubel FM, Pierce NE. Mining the plant-herbivore interface with a leafmining Drosophila of Arabidopsis. Molecular Ecology. 2011;20 :995-1014.Abstract

Experimental infections of Arabidopsis thaliana (Arabidopsis) with genomically characterized plant pathogens such as Pseudomonas syringae have facilitated the dissection of canonical eukaryotic defence pathways and parasite virulence factors. Plants are also attacked by herbivorous insects, and the development of an ecologically relevant genetic model herbivore that feeds on Arabidopsis will enable the parallel dissection of host defence and reciprocal resistance pathways such as those involved in xenobiotic metabolism. An ideal candidate is Scaptomyza flava, a drosophilid fly whose leafmining larvae are true herbivores that can be found in nature feeding on Arabidopsis and other crucifers. Here, we describe the life cycle of S. flava on Arabidopsis and use multiple approaches to characterize the response of Arabidopsis to S. flava attack. Oviposition choice tests and growth performance assays on different Arabidopsis ecotypes, defence-related mutants, and hormone and chitin-treated plants revealed significant differences in host preference and variation in larval performance across Arabidopsis accessions. The jasmonate and glucosinolate pathways in Arabidopsis are important in mediating quantitative resistance against S. flava, and priming with jasmonate or chitin resulted in increased resistance. Expression of xenobiotic detoxification genes was reduced in S. flava larvae reared on Arabidopsis jasmonate signalling mutants and increased in plants pretreated with chitin. These results and future research directions are discussed in the context of developing a genetic model system to analyse insect-plant interactions.

2011_whiteman_et_al_scaptomyza.pdf
Kronauer DJC, Pierce NE. Myrmecophiles. Current Biology. 2011;21 :R208-R209. 2011_kronauer_and_pierce.pdf
Kronauer DJC, Boomsma JJ, Pierce NE. Nine novel microsatellite markers for the army ant Simopelta pergandei (subfamily Ponerinae). Conservation Genetics Resources. 2011;3 :61-63.Abstract

Simopelta (subfamily Ponerinae) army ants are specialized predators of other ants in New World tropical forests. Although they show a striking convergence in overall life-history with the well known army ants of the subfamilies Aenictinae, Dorylinae, and Ecitoninae, the genus has been little studied. We developed and characterized nine novel microsatellite loci for S. pergandei with 2-8 observed alleles (mean: 5.2) and expected heterozygosities between 0.16 and 0.87 (mean: 0.68). Three of these loci reliably cross-amplified in a second species, S. pentadentata, with 4-8 alleles (mean: 8.0) and expected heterozygosities between 0.32 and 0.85 (mean: 0.65). These genetic markers will be useful in studying the sociobiology and molecular ecology of Simopelta army ants and in elucidating convergent evolutionary trajectories that have culminated in the army ant lifestyle.

kronauer2011_article_ninenovelmicrosatellitemarkers.pdf
Ugelvig LV, Vila R, Pierce NE, Nash DR. A phylogenetic revision of the Glaucopsyche section (Lepidoptera: Lycaenidae), with special focus on the Phengaris-Maculinea clade. Molecular Phylogenetics and Evolution. 2011;61 :237-243.Abstract

Despite much research on the socially parasitic large blue butterflies (genus Maculinea) in the past 40 years, their relationship to their closest relatives, Phengaris, is controversial and the relationships among the remaining genera in the Glaucopsyche section are largely unresolved. The evolutionary history of this butterfly section is particularly important to understand the evolution of life history diversity connected to food-plant and host-ant associations in the larval stage. In the present study, we use a combination of four nuclear and two mitochondrial genes to reconstruct the phylogeny of the Glaucopsyche section, and in particular, to study the relationships among and within the Phengaris-Maculinea species.We find a clear pattern between the clades recovered in the Glaucopsyche section phylogeny and their food-plant associations, with only the Phengaris-Maculinea clade utilising more than one plant family. Maculinea is, for the first time, recovered with strong support as a monophyletic group nested within Phengaris, with the closest relative being the rare genus Caerulea. The genus Glaucopsyche is polyphyletic, including the genera Sinia and lolana. Interestingly, we find evidence for additional potential cryptic species within the highly endangered Maculinea, which has long been suspected from morphological, ecological and molecular studies. (C) 2011 Elsevier Inc. All rights reserved.

ugelvig_lv_et_al._2011_glaucopsyche_mpe.pdf
Vila R, Bell CD, Macniven R, Goldman-Huertas B, Ree RH, Marshall CR, Balint Z, Johnson K, Benyamini D, Pierce NE. Phylogeny and palaeoecology of Polyommatus blue butterflies show Beringia was a climate-regulated gateway to the New World. Proceedings of the Royal Society B-Biological Sciences. 2011;278 :2737-2744.Abstract

Transcontinental dispersals by organisms usually represent improbable events that constitute a major challenge for biogeographers. By integrating molecular phylogeny, historical biogeography and palaeoecology, we test a bold hypothesis proposed by Vladimir Nabokov regarding the origin of Neotropical Polyommatus blue butterflies, and show that Beringia has served as a biological corridor for the dispersal of these insects from Asia into the New World. We present a novel method to estimate ancestral temperature tolerances using distribution range limits of extant organisms, and find that climatic conditions in Beringia acted as a decisive filter in determining which taxa crossed into the New World during five separate invasions over the past 11 Myr. Our results reveal a marked effect of the Miocene-Pleistocene global cooling, and demonstrate that palaeoclimatic conditions left a strong signal on the ecology of present-day taxa in the New World. The phylogenetic conservatism in thermal tolerances that we have identified may permit the reconstruction of the palaeoecology of ancestral organisms, especially mobile taxa that can easily escape from hostile environments rather than adapt to them.

vila_et_al._2011_evol_of_nabokovs_blues_esm_5.pdf vila_et_al._2011_evol_of_nabokovs_blues_ms.pdf
Weyl EG, Frederickson ME, Yu DW, Pierce NE. Reply to Kiers et al.: Economic and biological clarity in the theory of mutualism. Proceedings of the National Academy of Sciences of the United States of America. 2011;108 :E8-E8. 2011_weyl_et_al_reply.pdf
Kronauer DJC, O'Donnell S, Boomsma JJ, Pierce NE. Strict monandry in the ponerine army ant genus Simopelta suggests that colony size and complexity drive mating system evolution in social insects. Molecular Ecology. 2011;20 :420-428.Abstract

Altruism in social insects has evolved between closely related full-siblings. It is therefore of considerable interest why some groups have secondarily evolved low within-colony relatedness, which in turn affects the relatedness incentives of within-colony cooperation and conflict. The highest queen mating frequencies, and therefore among the lowest degrees of colony relatedness, occur in Apis honeybees and army ants of the subfamilies Aenictinae, Ecitoninae, and Dorylinae, suggesting that common life history features such as reproduction by colony fission and male biased numerical sex-ratios have convergently shaped these mating systems. Here we show that ponerine army ants of the genus Simopelta, which are distantly related but similar in general biology to other army ants, have strictly monandrous queens. Preliminary data suggest that workers reproduce in queenright colonies, which is in sharp contrast to other army ants. We hypothesize that differences in mature colony size and social complexity may explain these striking discrepancies.

kronauer_monandry.pdf
2010
Weyl EG, Frederickson ME, Yu DW, Pierce NE. Economic contract theory tests models of mutualism. Proceedings of the National Academy of Sciences. 2010;107 (36) :15712-15716.Abstract

Although mutualisms are common in all ecological communities and have played key roles in the diversification of life, our current understanding of the evolution of cooperation applies mostly to social behavior within a species. A central question is whether mutualisms persist because hosts have evolved costly punishment of cheaters. Here, we use the economic theory of employment contracts to formulate and distinguish between two mechanisms that have been proposed to prevent cheating in host–symbiont mutualisms, partner fidelity feedback (PFF) and host sanctions (HS). Under PFF, positive feedback between host fitness and symbiont fitness is sufficient to prevent cheating; in contrast, HS posits the necessity of costly punishment to maintain mutualism. A coevolutionary model of mutualism finds that HS are unlikely to evolve de novo, and published data on legume–rhizobia and yucca–moth mutualisms are consistent with PFF and not with HS. Thus, in systems considered to be textbook cases of HS, we find poor support for the theory that hosts have evolved to punish cheating symbionts; instead, we show that even horizontally transmitted mutualisms can be stabilized via PFF. PFF theory may place previously underappreciated constraints on the evolution of mutualism and explain why punishment is far from ubiquitous in nature.

pnas-2010-weyl-15712-6.pdf
Vila R, Lukhtanov VA, Talavera G, Gil F, Pierce NE. How common are dot-like distributions? Taxonomical oversplitting in western European Agrodiaetus (Lepidoptera: Lycaenidae) revealed by chromosomal and molecular markers. Biological Journal of the Linnean Society. 2010;101 :130-154.Abstract

Approximately 50 taxa of butterflies in Western Europe have been described as new species or elevated to the level of species during the last 40 years. Many, especially those belonging to the genus Agrodiaetus, have unusually localized, 'dot-like' distributional ranges. In the present study, we use a combination of chromosomal and molecular markers to re-evaluate the species status of Agrodiaetus distributed west of the 17th meridian. The results obtained do not support the current designations of Agrodiaetus galloi, Agrodiaetus exuberans, and Agrodiaetus agenjoi as endemic species with highly restricted distribution ranges, but indicate that these taxa are more likely to be local populations of a widely distributed species, Agrodiaetus ripartii. Agrodiaetus violetae is shown to be a polytypic species consisting of at least two subspecies, including Agrodiaetus violetae subbaeticus comb. nov. and Agrodiaetus violetae violetae. Agrodiaetus violetae is genetically (but not chromosomally) distinct from Agrodiaetus fabressei and has a wider distribution in southern Spain than previously believed. Agrodiaetus humedasae from northern Italy is supported as a highly localized species that is distinct from its nearest relatives. We propose a revision of the species lists for Agrodiaetus taking these new data into account. The results reported in the present study are relevant to animal conservation efforts in Europe because of their implications for IUCN Red List priorities. (C) 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 130-154.

vila_et_al._2010_dot_distrib.pdf
Sodhi NS, Lee TM, Sekercioglu CH, Webb EL, Prawiradilaga DM, Lohman DJ, Pierce NE, Diesmos AC, Rao M, Ehrlich PR. Local people value environmental services provided by forested parks. Biodiversity and Conservation. 2010;19 :1175-1188.Abstract

Garnering support from local people is critical for maintaining ecologically viable and functional protected areas. However, empirical data illustrating local people's awareness of the importance of nature's services is limited; hence possibly impeding effective ecosystem (environmental)-services based conservation efforts. Using data from five protected forests in four developing Southeast Asian countries, we provide evidence that local people living near parks value a wide range of environmental services, including cultural, provisioning, and regulating services, provided by the forests. Local people with longer residency valued environmental services more. Educated as well as poor people valued forest ecosystem services more. Conservation education has some influence on people's environmental awareness. For conservation endeavors to be successful, large-scale transmigration programs should be avoided and local people must be provided with alternative sustenance opportunities and basic education in addition to environmental outreach to reduce their reliance on protected forests and to enhance conservation support.

sodhi_ns_et_al._local_people_value_envir_serv_biodivers._conserv_2010.pdf
Ramirez SR, Nieh JC, Quental TB, Roubik DW, Imperatriz-Fonseca VL, Pierce NE. A molecular phylogeny of the stingless bee genus Melipona (Hymenoptera: Apidae). Molecular Phylogenetics and Evolution. 2010;56 :519-525.Abstract

Stingless bees (Meliponini) constitute a diverse group of highly eusocial insects that occur throughout tropical regions around the world. The meliponine genus Melipona is restricted to the New World tropics and has over 50 described species. Melipona, like Apis, possesses the remarkable ability to use representational communication to indicate the location of foraging patches. Although Melipona has been the subject of numerous behavioral, ecological, and genetic studies, the evolutionary history of this genus remains largely unexplored. Here, we implement a multigene phylogenetic approach based on nuclear, mitochondrial, and ribosomal loci, coupled with molecular clock methods, to elucidate the phylogenetic relationships and antiquity of subgenera and species of Melipona. Our phylogenetic analysis resolves the relationship among subgenera and tends to agree with morphology-based classification hypotheses. Our molecular clock analysis indicates that the genus Melipona shared a most recent common ancestor at least similar to 14-17 million years (My) ago. These results provide the groundwork for future comparative analyses aimed at understanding the evolution of complex communication mechanisms in eusocial Apidae. (C) 2010 Elsevier Inc. All rights reserved.

ramirez_stingless.pdf
Ramirez SR, Roubik DW, Skov C, Pierce NE. Phylogeny, diversification patterns and historical biogeography of euglossine orchid bees (Hymenoptera: Apidae). Biological Journal of the Linnean Society. 2010;100 :552-572.Abstract

The orchid bees constitute a clade of prominent insect pollinators distributed throughout the Neotropical region. Males of all species collect fragrances from natural sources, including flowers, decaying vegetation and fungi, and store them in specialized leg pockets to later expose during courtship display. In addition, orchid bees provide pollination services to a diverse array of Neotropical angiosperms when foraging for food and nesting materials. However, despite their ecological importance, little is known about the evolutionary history of orchid bees. Here, we present a comprehensive molecular phylogenetic analysis based on similar to 4.0 kb of DNA from four loci [cytochrome oxidase (CO1), elongation factor 1-alpha (EF1-alpha), arginine kinase (ArgK) and RNA polymerase II (Pol-II)] across the entire tribe Euglossini, including all five genera, eight subgenera and 126 of the approximately 200 known species. We investigated lineage diversification using fossil-calibrated molecular clocks and the evolution of morphological traits using disparity-through-time plots. In addition, we inferred past biogeographical events by implementing model-based likelihood methods. Our dataset supports a new view on generic relationships and indicates that the cleptoparasitic genus Exaerete is sister to the remaining orchid bee genera. Our divergence time estimates indicate that extant orchid bee lineages shared a most recent common ancestor at 27-42 Mya. In addition, our analysis of morphology shows that tongue length and body size experienced rapid disparity bursts that coincide with the origin of diverse genera (Euglossa and Eufriesea). Finally, our analysis of historical biogeography indicates that early diversification episodes shared a history on both sides of Mesoamerica, where orchid bees dispersed across the Caribbean, and through a Panamanian connection, thus reinforcing the hypothesis that recent geological events (e.g. the formation of the isthmus of Panama) contributed to the diversification of the rich Neotropical biota. (C) 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 552-572.

ramirez_et_al._euglossini_2010.pdf
2009
Russell JA, Moreau CS, Goldman-Huertas B, Fujiwara M, Lohman DJ, Pierce NE. Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proceedings of the National Academy of Sciences of the United States of America. 2009;106 :21236-21241.Abstract

Ants are a dominant feature of terrestrial ecosystems, yet we know little about the forces that drive their evolution. Recent findings illustrate that their diets range from herbivorous to predaceous, with "herbivores'' feeding primarily on exudates from plants and sap-feeding insects. Persistence on these nitrogen-poor food sources raises the question of how ants obtain sufficient nutrition. To investigate the potential role of symbiotic microbes, we have surveyed 283 species from 18 of the 21 ant subfamilies using molecular techniques. Our findings uncovered a wealth of bacteria from across the ants. Notable among the surveyed hosts were herbivorous "turtle ants'' from the related genera Cephalotes and Procryptocerus (tribe Cephalotini). These commonly harbored bacteria from ant-specific clades within the Burkholderiales, Pseudomonadales, Rhizobiales, Verrucomicrobiales, and Xanthomonadales, and studies of lab-reared Cephalotes varians characterized these microbes as symbiotic residents of ant guts. Although most of these symbionts were confined to turtle ants, bacteria from an ant-specific clade of Rhizobiales were more broadly distributed. Statistical analyses revealed a strong relationship between herbivory and the prevalence of Rhizobiales gut symbionts within ant genera. Furthermore, a consideration of the ant phylogeny identified at least five independent origins of symbioses between herbivorous ants and related Rhizobiales. Combined with previous findings and the potential for symbiotic nitrogen fixation, our results strongly support the hypothesis that bacteria have facilitated convergent evolution of herbivory across the ants, further implicating symbiosis as a major force in ant evolution.

2009_russell_et_al.pdf
Canfield MR, Chang S, Pierce NE. The double cloak of invisibility: phenotypic plasticity and larval decoration in a geometrid moth, Synchlora frondaria, across three diet treatments. Ecological Entomology. 2009;34 :412-414.Abstract

1. Crypsis is one of the main defences that insects use to avoid predators, and both the juveniles and adults of many geometrid moths are remarkable in their ability to blend into different host backgrounds. The larvae of Synchlora frondaria have two methods to achieve crypsis: phenotypic plasticity in colouration that enable them to hide more effectively on their host plants, and a self-decorating behaviour whereby the larvae camouflage themselves with materials from their host plants.2. Larvae of Synchlora frondaria reared on three different host plants showed systematic differences in relative growth rate, survivorship and larval colouration.3. Larval colouration varied across diet treatments in a way that was consistent with diet-induced phenotypic plasticity, and larvae also exhibited characteristic decorating behaviour on all three hosts.4. Larvae showed highest survivorship on Heterotheca subaxillaris (Asteraceae), and had significantly higher relative growth rates on H. subaxillaris (Asteraceae) and Lantana camara (Verbenaceae) than on Bejaria racemosa (Ericaceae).5. Synchlora frondaria provides an example of a species where both decorating behaviour and phenotypic plasticity in larval colouration produce a cryptic form that is remarkably responsive to its background.

canfield_et_al._2009.pdf
Russell JA, Goldman-Huertas B, Moreau CS, Baldo L, Stahlhut JK, Werren JH, Pierce NE. Specialization and Geographic Isolation among Wolbachia Symbionts from Ants and Lycaenid Butterflies. Evolution. 2009;63 :624-640.Abstract

Wolbachia are the most prevalent and influential bacteria described among the insects to date. But despite their significance, we lack an understanding of their evolutionary histories. To describe the evolution of symbioses between Wolbachia and their hosts, we surveyed global collections of two diverse families of insects, the ants and lycaenid butterflies. In total, 54 Wolbachia isolates were typed using a Multi Locus Sequence Typing (MLST) approach, in which five unlinked loci were sequenced and analyzed to decipher evolutionary patterns. AMOVA and phylogenetic analyses demonstrated that related Wolbachia commonly infect related hosts, revealing a pattern of host association that was strongest among strains from the ants. A review of the literature indicated that horizontal transfer is most successful when Wolbachia move between related hosts, suggesting that patterns of host association are driven by specialization on a common physiological background. Aside from providing the broadest and strongest evidence to date for Wolbachia specialization, our findings also reveal that strains from New World ants differ markedly from those in ants from other locations. We, therefore, conclude that both geographic and phylogenetic barriers have promoted evolutionary divergence among these influential symbionts.

russell_et_al._2009.pdf
2008
Canfield MR, Greene E, Moreau CS, Chen N, Pierce NE. Exploring phenotypic plasticity and biogeography in emerald moths: A phylogeny of the genus Nemoria (Lepidoptera: Geometridae). Molecular Phylogenetics and Evolution. 2008;49 :477-487.Abstract

The moth genus Nemoria (Lepidoptera: Geometridae) includes 134 described species whose larvae and adults display a considerable range of phenotypic plasticity in coloration and morphology. We reconstructed the phylogeny of 54 species of Nemoria and seven outgroups using characters from the mitochondrial genes, Cytochrome Oxidase I and II (COI and COII), and the nuclear gene, Elongation Factor-a (EF-1a). Maximum parsimony, maximum likelihood and Bayesian inference were used to infer the phylogeny. The 54 ingroup species represented 13 of the 15 recognized species groups of Nemoria [Ferguson, D.C., 1985. Fasc. 18.1, Geometroidea: Geometridae (in part). In: Dominick, R.B. (Ed.), The Moths of America North of Mexico, Fasc. 18.1. Wedge Entomological Research Foundation, Washington; Pitkin, L.M., 1993. Neotropical emerald moths of the genera Nemoria, Lissochlora and Chavarriella, with particular reference to the species of Costa Rica (Lepidoptera: Geometridae, Geometrinae). Bull. Br. Mus. Nat. Hist. 62, 39–159], and the seven outgroups came from four tribes of Geometrinae. These data support Nemoria as a monophyletic group and largely recover the species groupings proposed in previous taxonomic analyses using morphological characters. Phenotypic plasticity of larvae is not correlated with plasticity of adults among those species of Nemoria where life histories are known, and appears to be evolutionarily labile for both life history stages: Species exhibiting larval phenotypic plasticity, such as N. arizonaria and N. outina, are placed in several distinct clades, suggesting that this trait has evolved multiple times, and species displaying adult phenotypic plasticity are likewise distributed throughout the phylogeny. A comparative analysis of the biogeographic history of Nemoria supports a South American origin for the genus with multiple introductions into North America, and an application of published substitution rates to the phylogram provides an age estimate of 7.5 million years.

2008_canfield_et_al.pdf
Travassos MA, Devries PJ, Pierce NE. A novel organ and mechanism for larval sound production in butterfly caterpillars: Eurybia elvina(Lepidoptera: Riodinidae). Tropical Lepidoptera Research. 2008;18 :20-23.Abstract

Abstract – Eurybia elvina larvae produce substrate-borne vibrations by grating a cervical membrane studded with teeth against hemispherical protuberances scattered along the surface of the head.

2008_travassos_et_al.pdf
Mathew J, Travassos MA, Canfield M, Murawski D, Kitching RL, Pierce NE. The singing reaper: diet, morphology and vibrational signaling in the Nearctic species Feniseca tarquinius. Tropical Lepidoptera Research. 2008;18 :24-29.Abstract

Abstract – A survey at fourteen sites in Eastern North America of populations of the carnivorous lycaenid butterfly, Feniseca tarquinius, confirmed that the sole prey item on Alnus rugosa (Betulaceae) for this species in these regions was Paraprociphilus tessellatus (Homoptera: Aphidoidea: Pemphigidae). Overwhelmingly, these aphids were tended by ants in the subfamily Formicinae. These results are compiled with all earlier records of prey aphids, their host plants and attendant ants for this species. SEM examination of a 4th instar larva of F. tarquinius supported Cottrell’s (1984) observation that the dorsal nectary organ and tentacle organs are absent in the 4th instar of virtually all Miletinae. Larvae of F. tarquinius were found to produce substrate-borne vibrations that possess a long pulse length and narrow bandwidth when compared with other lycaenid calls. The possible function of these calls is briefly discussed.

2008_mathew_et_al.pdf
Whiteman NK, Pierce NE. Delicious poison: genetics of Drosophila host plant preference. Trends in Ecology & Evolution. 2008;23 :473-478.Abstract

Insects use chemical cues to identify host plants, which suggests that chemosensory perception could be a target of natural selection during host specialization. Five papers using data from the 12 recently sequenced Drosophila genomes examined chemosensory gene function and evolution across specialist and generalist species. A functional study identifies odorant binding proteins that mediate loss of toxin avoidance in a specialist, and targeted genomic studies indicate specialists and island endemics lose chemosensory genes more rapidly than generalist and mainland relatives. Together, these studies suggest a mode of chemoreceptor evolution dominated by birth/death dynamics, coupled with a low level of potential positive selection.

2008_whiteman_pierce.pdf

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