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Featured researches published by Warren Booth.


Nature Communications | 2014

Molecular traces of alternative social organization in a termite genome

Nicolas Terrapon; Cai Li; Hugh M. Robertson; Lu Ji; Xuehong Meng; Warren Booth; Zhensheng Chen; Christopher P. Childers; Karl M. Glastad; Kaustubh Gokhale; Johannes Gowin; Wulfila Gronenberg; Russell A. Hermansen; Haofu Hu; Brendan G. Hunt; Ann Kathrin Huylmans; Sayed M.S. Khalil; Robert D. Mitchell; Monica Munoz-Torres; Julie A. Mustard; Hailin Pan; Justin T. Reese; Michael E. Scharf; Fengming Sun; Heiko Vogel; Jin Xiao; Wei Yang; Zhikai Yang; Zuoquan Yang; Jiajian Zhou

Although eusociality evolved independently within several orders of insects, research into the molecular underpinnings of the transition towards social complexity has been confined primarily to Hymenoptera (for example, ants and bees). Here we sequence the genome and stage-specific transcriptomes of the dampwood termite Zootermopsis nevadensis (Blattodea) and compare them with similar data for eusocial Hymenoptera, to better identify commonalities and differences in achieving this significant transition. We show an expansion of genes related to male fertility, with upregulated gene expression in male reproductive individuals reflecting the profound differences in mating biology relative to the Hymenoptera. For several chemoreceptor families, we show divergent numbers of genes, which may correspond to the more claustral lifestyle of these termites. We also show similarities in the number and expression of genes related to caste determination mechanisms. Finally, patterns of DNA methylation and alternative splicing support a hypothesized epigenetic regulation of caste differentiation.


Journal of Medical Entomology | 2012

Genetic Analysis of Bed Bug Populations Reveals Small Propagule Size Within Individual Infestations but High Genetic Diversity Across Infestations From the Eastern United States

Virna L. Saenz; Warren Booth; Coby Schal; Edward L. Vargo

ABSTRACT Bed bugs (Cimex lectularius L.) are a resurgent pest worldwide and infestations within the United States are increasing at a rapid rate. Because of the physical and psychological discomfort inflicted by their blood feeding habits, and allergies and secondary infections associated with bites, bed bugs are recognized as a significant public health problem. Although bed bug infestations are spreading and becoming more prevalent, we have a poor understanding of their dispersal patterns and sources of infestation. To help fill this gap, we conducted a genetic study of 21 bed bug infestations from the eastern United States, nearly all of which came from single rooms within residences. We genotyped samples comprised of 8–10 individuals per infestation at nine polymorphic microsatellite loci. Despite high genetic diversity across all infestations, with 5–17 alleles per locus (mean = 10.3 alleles per locus), we found low genetic diversity (1–4 alleles per locus) within all but one of the infestations. These results suggest that nearly all the studied infestations were started by a small propagule possibly consisting of a singly mated female and/or her progeny, or a female mated with multiple males that were highly related to her. All infestations were strongly genetically differentiated from each other (mean pairwise F ST between populations = 0.68) and we did not find strong evidence of a geographic pattern of genetic structure, indicating infestations located in closer proximity to each other were nearly as genetically differentiated as those located hundreds of kilometers away. The high level of genetic diversity across infestations from the eastern United States together with the lack of geographically organized structure is consistent with multiple introductions into the United States from foreign sources.


Biology Letters | 2012

Facultative parthenogenesis discovered in wild vertebrates

Warren Booth; Charles F. Smith; Pamela H. Eskridge; Shannon K. Hoss; Joseph R. Mendelson; Gordon W. Schuett

Facultative parthenogenesis (FP)—asexual reproduction by bisexual species—has been documented in a variety of multi-cellular organisms but only recently in snakes, varanid lizards, birds and sharks. Unlike the approximately 80 taxa of unisexual reptiles, amphibians and fishes that exist in nature, FP has yet to be documented in the wild. Based on captive documentation, it appears that FP is widespread in squamate reptiles (snakes, lizards and amphisbaenians), and its occurrence in nature seems inevitable, yet the task of detecting FP in wild individuals has been deemed formidable. Here we show, using microsatellite DNA genotyping and litter characteristics, the first cases of FP in wild-collected pregnant females and their offspring of two closely related species of North American pitviper snakes—the copperhead (Agkistrodon contortrix) and cottonmouth (Agkistrodon piscivorus). Our findings support the view that non-hybrid origins of parthenogenesis, such as FP, are more common in squamates than previously thought. With this confirmation, FP can no longer be viewed as a rare curiosity outside the mainstream of vertebrate evolution. Future research on FP in squamate reptiles related to proximate control of induction, reproductive competence of parthenogens and population genetics modelling is warranted.


Biology Letters | 2011

Evidence for viable, non-clonal but fatherless Boa constrictors

Warren Booth; Daniel H. Johnson; Sharon Moore; Coby Schal; Edward L. Vargo

Parthenogenesis in vertebrates is considered an evolutionary novelty. In snakes, all of which exhibit genetic sex determination with ZZ : ZW sex chromosomes, this rare form of asexual reproduction has failed to yield viable female WW offspring. Only through complex experimental manipulations have WW females been produced, and only in fish and amphibians. Through microsatellite DNA fingerprinting, we provide the first evidence of facultative parthenogenesis in a Boa constrictor, identifying multiple, viable, non-experimentally induced females for the first time in any vertebrate lineage. Although the elevated homozygosity of the offspring in relation to the mother suggests that the mechanism responsible may be terminal fusion automixis, no males were produced, potentially indicating maternal sex chromosome hemizygosity (WO). These findings provide the first evidence of parthenogenesis in the family Boidae (Boas), and suggest that WW females may be more common within basal reptilian lineages than previously assumed.


Nature Communications | 2016

Unique features of a global human ectoparasite identified through sequencing of the bed bug genome

Joshua B. Benoit; Zach N. Adelman; Klaus Reinhardt; Amanda Dolan; Monica Poelchau; Emily C. Jennings; Elise M. Szuter; Richard W. Hagan; Hemant Gujar; Jayendra Nath Shukla; Fang Zhu; M. Mohan; David R. Nelson; Andrew J. Rosendale; Christian Derst; Valentina Resnik; Sebastian Wernig; Pamela Menegazzi; Christian Wegener; Nicolai Peschel; Jacob M. Hendershot; Wolfgang Blenau; Reinhard Predel; Paul R. Johnston; Panagiotis Ioannidis; Robert M. Waterhouse; Ralf Nauen; Corinna Schorn; Mark Christoph Ott; Frank Maiwald

The bed bug, Cimex lectularius, has re-established itself as a ubiquitous human ectoparasite throughout much of the world during the past two decades. This global resurgence is likely linked to increased international travel and commerce in addition to widespread insecticide resistance. Analyses of the C. lectularius sequenced genome (650 Mb) and 14,220 predicted protein-coding genes provide a comprehensive representation of genes that are linked to traumatic insemination, a reduced chemosensory repertoire of genes related to obligate hematophagy, host–symbiont interactions, and several mechanisms of insecticide resistance. In addition, we document the presence of multiple putative lateral gene transfer events. Genome sequencing and annotation establish a solid foundation for future research on mechanisms of insecticide resistance, human–bed bug and symbiont–bed bug associations, and unique features of bed bug biology that contribute to the unprecedented success of C. lectularius as a human ectoparasite.


Journal of Medical Entomology | 2012

Molecular markers reveal infestation dynamics of the bed bug (Hemiptera: Cimicidae) within apartment buildings.

Warren Booth; Virna L. Saenz; Richard G. Santangelo; Changlu Wang; Coby Schal; Edward L. Vargo

ABSTRACT The bed bug, Cimex lectularius L. (Hemiptera: Cimicidae), has experienced an extraordinary global resurgence in recent years, the reasons for which remain poorly understood. Once considered a pest of lower socioeconomic classes, bed bugs are now found extensively across all residential settings, with widespread infestations established in multiapartment buildings. Within such buildings, understanding the population genetic structure and patterns of dispersal may prove critical to the development of effective control strategies. Here, we describe the development of 24 high-resolution microsatellite markers through next generation 454 pyrosequencing and their application to elucidate infestation dynamics within three multistory apartment buildings in the United States. Results reveal contrasting characteristics potentially representative of geographic or locale differences. In Raleigh, NC, an infestation within an apartment building seemed to have started from a single introduction followed by extensive spread. In Jersey City, NJ, two or more introductions followed by spread are evident in two buildings. Populations within single apartments in all buildings were characterized by high levels of relatedness and low levels of diversity, indicative of foundation from small, genetically depauperate propagules. Regardless of the number of unique introductions, genetic data indicate that spread within buildings is extensive, supporting both active and human-mediated dispersal within and between adjacent rooms or apartments spanning multiple floors.


Molecular Ecology Resources | 2011

Permanent Genetic Resources added to Molecular Ecology Resources Database 1 December 2010-31 January 2011: PERMANENT GENETIC RESOURCES NOTE

Kiyokazu Agata; Samer Alasaad; Vera Maria Fonseca Almeida-Val; J. A. Álvarez-Dios; F. Barbisan; Jon S. Beadell; J. F. Beltrán; M. Benítez; G. Bino; Colin Bleay; P. Bloor; Jörg Bohlmann; Warren Booth; E. Boscari; Adalgisa Caccone; Tatiana Campos; B. M. Carvalho; Gisele Torres Climaco; Jean Clobert; L. Congiu; Christina Cowger; G. Dias; I. Doadrio; Izeni P. Farias; N. Ferrand; Patrícia Domingues de Freitas; G. Fusco; Pedro Manoel Galetti; Cristian Gallardo-Escárate; Michael W. Gaunt

This article documents the addition of 238 microsatellite marker loci to the Molecular Ecology Resources Database. Loci were developed for the following species: Alytes dickhilleni, Arapaima gigas, Austropotamobius italicus, Blumeria graminis f. sp. tritici, Cobitis lutheri, Dendroctonus ponderosae, Glossina morsitans morsitans, Haplophilus subterraneus, Kirengeshoma palmata, Lysimachia japonica, Macrolophus pygmaeus, Microtus cabrerae, Mytilus galloprovincialis, Pallisentis (Neosentis) celatus, Pulmonaria officinalis, Salminus franciscanus, Thais chocolata and Zootoca vivipara. These loci were cross‐tested on the following species: Acanthina monodon, Alytes cisternasii, Alytes maurus, Alytes muletensis, Alytes obstetricans almogavarii, Alytes obstetricans boscai, Alytes obstetricans obstetricans, Alytes obstetricans pertinax, Cambarellus montezumae, Cambarellus zempoalensis, Chorus giganteus, Cobitis tetralineata, Glossina fuscipes fuscipes, Glossina pallidipes, Lysimachia japonica var. japonica, Lysimachia japonica var. minutissima, Orconectes virilis, Pacifastacus leniusculus, Procambarus clarkii, Salminus brasiliensis and Salminus hilarii.


Molecular Ecology | 2015

Host association drives genetic divergence in the bed bug, Cimex lectularius.

Warren Booth; Ondřej Balvín; Edward L. Vargo; Jitka Vilímová; Coby Schal

Genetic differentiation may exist among sympatric populations of a species due to long‐term associations with alternative hosts (i.e. host‐associated differentiation). While host‐associated differentiation has been documented in several phytophagus insects, there are far fewer cases known in animal parasites. The bed bug, Cimex lectularius, a wingless insect, represents a potential model organism for elucidating the processes involved in host‐associated differentiation in animal parasites with relatively limited mobility. In conjunction with the expansion of modern humans from Africa into Eurasia, it has been speculated that bed bugs extended their host range from bats to humans in their shared cave domiciles throughout Eurasia. C. lectularius that associate with humans have a cosmopolitan distribution, whereas those associated with bats occur across Europe, often in human‐built structures. We assessed genetic structure and gene flow within and among populations collected in association with each host using mtDNA, microsatellite loci and knock‐down resistance gene variants. Both nuclear and mitochondrial data support a lack of significant contemporary gene flow between host‐specific populations. Within locations human‐associated bed bug populations exhibit limited genetic diversity and elevated levels of inbreeding, likely due to human‐mediated movement, infrequent additional introduction events per infestation, and pest control. In contrast, populations within bat roosts exhibit higher genetic diversity and lower levels of relatedness, suggesting populations are stable with temporal fluctuations due to host dispersal and bug mortality. In concert with previously published evidence of morphological and behavioural differentiation, the genetic data presented here suggest C. lectularius is currently undergoing lineage divergence through host association.


PLOS ONE | 2010

Is It Easy to Be Urban? Convergent Success in Urban Habitats among Lineages of a Widespread Native Ant

Sean B. Menke; Warren Booth; Robert R. Dunn; Coby Schal; Edward L. Vargo; Jules Silverman

The most rapidly expanding habitat globally is the urban habitat, yet the origin and life histories of the populations of native species that inhabit this habitat remain poorly understood. We use DNA barcoding of the COI gene in the widespread native pest ant Tapinoma sessile to test two hypotheses regarding the origin of urban populations and traits associated with their success. First, we determine if urban samples of T. sessile have a single origin from natural populations by looking at patterns of haplotype clustering from across their range. Second, we examine whether polygynous colony structure – a trait associated with invasion success – is correlated with urban environments, by studying the lineage dependence of colony structure. Our phylogenetic analysis of 49 samples identified four well supported geographic clades. Within clades, Kimura-2 parameter pairwise genetic distances revealed <2.3% variation; however, between clade genetic distances were 7.5–10.0%, suggesting the possibility of the presence of cryptic species. Our results indicate that T. sessile has successfully colonized urban environments multiple times. Additionally, polygynous colony structure is a highly plastic trait across habitat, clade, and haplotype. In short, T. sessile has colonized urban habitats repeatedly and appears to do so using life history strategies already present in more natural populations. Whether similar results hold for other species found in urban habitats has scarcely begun to be considered.


Journal of Heredity | 2011

Population Genetic Structure in German Cockroaches (Blattella Germanica): Differentiated Islands in an Agricultural Landscape

Warren Booth; Richard G. Santangelo; Edward L. Vargo; D. V. Mukha; Coby Schal

Although a number of species live syanthropically with humans, few rely entirely on humans for their survival and distribution. Unlike other cosmopolitan human commensals, the German cockroach (Blattella germanica), an insect of both public and livestock health concern, is considered incapable of dispersal outside human dwellings. Patterns of genetic association are therefore constrained and may not be associated with distance. Analogies with other human-commensal species are therefore impossible to draw with any degree of accuracy. In the past 2 decades, B. germanica has become a prominent pest within the US swine production system. Swine production is mainly carried out through contracted producers, each associated with a management company. It has been hypothesized that cockroach populations will be genetically structured based on association to a specific management company. Here, we tested this hypothesis using microsatellite genotypes (8 polymorphic loci) from 626 individual cockroaches collected from 22 farms in southeastern North Carolina representing 3 management companies. Significant genetic differentiation was detected (F(ST) = 0.171), most of which was partitioned among the 22 farms rather than the 3 management groups. All pair-wise population comparisons yielded F(ST) values significantly greater than zero. Our results reveal that structure does not correspond to management company of origin, but instead it may be regional and influenced strongly by the unintentional movement of cockroaches by farm workers.

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Edward L. Vargo

North Carolina State University

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Coby Schal

North Carolina State University

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Richard G. Santangelo

North Carolina State University

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Todd A. Castoe

University of Texas at Arlington

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Paulo A. Prodöhl

Queen's University Belfast

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D. V. Mukha

Russian Academy of Sciences

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Ondřej Balvín

Czech University of Life Sciences Prague

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