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Mongue, A. J.

Publications and source records attributed to Mongue, A. J..

At least 19 recordsLinked to original sources

A chromosome-level genome assembly of the chilli thrips Scirtothrips dorsalis Hood (Thysanoptera: Thripidae)

Thrips are known for being pests of many agricultural crops, as well as vectors of plant viruses. Yet despite their economic importance, genomic resources for this group remain limited, and no chromosome-level genome has been available for the genus Scirtothrips. One such species is the chilli thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae). This invasive and highly polyphagous pest is established across much of the world and transmits several tospoviruses. Genomic resources would provide a new means to understand the traits that make thrips difficult to manage. Here, we present a chromosome-level genome assembly for S. dorsalis. The assembly is 266.5 Mb, with 96.9% of the sequence anchored in 16 chromosome-scale scaffolds. It contains 20,557 genes, and repetitive elements account for 28.8% of the sequence, which is comparable to those of other sequenced Thripidae. A species tree based on 3,019 single copy orthologs placed S. dorsalis as sister to Scirtothrips hansoni, with Scirtothrips most closely related to Frankliniella, Megalurothrips, and Odontothrips. The mitochondrial genome is a single circular molecule of 15,207 bp in which the sequence of the published mini circle is integrated, in contrast to the bipartite mitogenome previously reported for the same cryptic species.

genomics↗

Genome report: Genome sequence of Phymata mystica (Evans), an ambush bug

Recent advances in sequencing technology have made the sequencing of non-model organisms significantly more streamlined and feasible. Using these technologies, we begin to address the lack of data on non-model organisms, by sequencing the genome of one such species, Phymata mystica (Evans 1931), an ambush bug (Hemiptera: Heteroptera: Reduviidae: Phymatinae) specialized for floral sit-and-wait style predation. Our genome assembly is 710 Mb, in which 99.7% of this sequence is assembled into 14 chromosomal scaffolds. We found that repetitive elements accounted for 58.85% of the sequence. We report 26,760 protein-coding genes in a preliminary annotation of the genome. Using these new resources, we explored both macrosynteny and gene conservation. Starting with chromosome structure, we found that P. mystica has a single X chromosome, unlike other well-assembled Reduviids in which the X apparently split into two linkage groups. Exploring this new annotation, we found a number of venom proteins conserved between P. mystica and the other venomous Heteroptera with reference genomes, primarily serine proteases, metallopeptidase and heteropteran venom family proteins. These results provide a new framework for the evolution of venom in this group of insects and further demonstrate the ease with which non-model species can be studied using modern genomic methods.

genomics↗

Leaving X: How scale insects evolved alternatives to chromosomal sex determination

Reproduction is a core feature of life, which makes understanding the reproductive diversity of organisms a fundamental goal of evolutionary biology. It is still unclear why sex determination systems are faithfully conserved for hundreds of millions of years in some taxa but repeatedly turn over in others. A prime example is the true bugs, Hemiptera. The vast majority of families employ a conserved X sex chromosomal system, but in scale insects (Coccomorpha), sex determination systems are far more varied. Different families may retain X chromosomes, employ a rare form of haplodiploidy known as paternal genome elimination (PGE), or forgo sexual reproduction in favor of simultaneous hermaphroditism. While these systems have been known for decades, only recently has non-model genomics enabled their study with modern bioinformatic methods. We collected and sequenced representatives of rare, early-diverging scale insects to study genomic changes that coincide with transitions between sex determination systems. Using ancillary expression data, we also explored sex-biased gene expression in a subset of scale insects on both sides of one transition. In a newly updated molecular phylogeny, we recovered two independent losses of X chromosomal sex determination, once in the family Monophlebidae and a second time at the base of the families that employ PGE. In the former, genomic rearrangements begin before the X is lost and any previously X-linked orthologs have been absorbed into one of two massive, shuffled autosomes in the hermaphrodites. In the latter, the X chromosome itself is faithfully preserved in early diverging PGE taxa; it appears to have merely lost its sex determination function. We analyze ortholog conservation across these transitions and find few genes lost, with only one orthogroup lost in both transitions, and a number of orthogroups gained, suggesting these large transitions did not require large changes to the gene content of the X chromosome. Expression data suggests that extreme sexual dimorphism of gene expression predates sex determination turnover and may have helped enable it. Together these new observations illustrate the multiple routes to sex determination turnover, help refine hypotheses for its causes, and provide a wealth of new resources for the modern genomic study of scale insects.

evolutionary biology↗

Insights from the lack of an enigmatic trait: monomorphic sperm in evergreen bagworm moths and the evolution of sperm dimorphism

Reproductive traits contain some of the most bizarre and unintuitive innovations seen across the tree of life. Chief among these is the sperm dimorphism of butterflies and moths (Lepidoptera). Males make two types of sperm: traditional fertilizing sperm (eupyrene) and a second, non-fertilizing type (apyrene) that lacks a nucleus entirely. Despite decades of study, the function and evolution of this second sperm type has remained unclear. Here we explore the sperm biology of the evergreen bagworm moth, Thyridopteryx ephemeraeformis (Lepidoptera: Tineoidea: Psychidae), and find no evidence for non-fertilizing sperm in this species. We generate genomic, transcriptomic, and proteomic resources to characterize the apparently monomorphic sperm of this species and compare it to that of other Lepidoptera. The fertilizing sperm of the evergreen bagworm shows key differences from other studied species, especially a lack of proteolytic enzymes used to break down sperm bundles in other species. Combining this and other evidence, we offer new hypotheses for the evolution and function of this enigmatic reproductive trait. Notably, early diverging moths appear to produce far less non-fertilizing sperm in general than later diverging Lepidoptera. We infer that non-fertilizing sperm are not necessary in these taxa, perhaps because less robust packaging of fertilizing sperm enables greater mobility than in later diverging moths.

evolutionary biology↗

Genome sequencing confirms cryptic diversity and potentially adaptive changes in gene content of Lepidoptera-infecting Apicomplexa

Apicomplexan parasites of insects represent a largely unexplored branch of the tree of life. Their small size and lack of informative phenotypic traits can obscure their diversity and many lineage-specific adaptations to different host species. To better understand how these parasites have evolved, we have sequenced and annotated the genome of a neogregarine parasite of moths including Helicoverpa armigera. This parasite, which we term Helicoverpa-infecting Ophryocystis, has a tiny 7 Megabase genome with only 2,200 protein-coding genes. Using phylogenomic methods, we place it as the closest currently sequenced relative to Ophryocystis elektroscirrha and its sister lineage, both of which infect milkweed butterflies. We then explore evolution of the ATPase gene family, which is known to be reduced in other Ophryocystis lineages. Helicoverpa-infecting Ophryocystis has more ATPase genes than other Ophryocystis, which may relate to the interactions of parasites with phytochemistry encountered in their insect hosts. These results demonstrate both the amount of uncertainty remaining in the insect-infecting Apicomplexa as well as the utility of applying modern genomic approaches to their study.

evolutionary biology↗

Genome report: Genome sequence of the hibiscus mealybug, Nipaecoccus viridis (Newstead), an invasive pest of citrus

Mealybugs are frequently known for being pest insects to both ornamental and large-scale agricultural crops. Yet despite their agricultural importance, the genomic resources for this group remain quite small. One such species is the hibiscus mealybug, Nipaecoccus viridis (Newstead) (Hemiptera: Coccomorpha: Pseudococcidae). This invasive mealybug species has recently expanded throughout Florida and has spread across the state. Genomic resources would provide a new means to better understand the invasive nature of this insect, and thus, we present the de novo genome assembly for Nipaecoccus viridis. Our genome assembly is 289 Mb, in which 91.2% of this sequence assembled into 5 chromosomal scaffolds. We report 15,370 genes to be present within our genome. We found that repetitive elements in the genome accounted for 32.40% of the sequence. These statistics follow similar trends to other previously sequenced pseudococcid species.

genomics↗

Gene family evolution reveals dietary adaptations in butterflies and moths

Butterflies and moths (Lepidoptera) are a hyperdiverse lineage of nearly 160,000 described species and their evolutionary success is postulated to be tightly correlated with the radiation of their primary host -- angiosperms. Previous studies found that a significant number of emergent gene families are specific to Lepidoptera, with many genes linked to odorant receptors and peptidases, suggesting that such genetic innovations may be linked to their diversification. Here, we use genomic resources to identify lineage-specific gene families in four nested lepidopteran clades (e.g. Lepidoptera, Glossata, Ditrysia, and Apoditrysia). Among nearly a hundred gene families specific to each group, a handful of gene families have specific and interpretable functions. We found that many digestion-related gene families emerged early in the evolution of Lepidoptera, followed by genes associated with detoxification and immunity. This result aligns with the evolutionary transition in ancient Lepidoptera diets to terrestrial plants, highlighting the emergence of detoxification mechanisms in the megadiverse Ditrysia as a critical adaptation driven by the proliferation of plant chemical defenses. We also found gene families originating from horizontal gene transfer (HGT) events, likely introduced from bacteria and fungi to the common ancestors of Lepidoptera and Ditrysia, respectively. These HGT-derived genes likely played a pivotal role in supporting the dietary transition from algae, diatoms, and aquatic plant debris to fungi and primitive terrestrial plants, ultimately enabling the adaptation to the most dominant angiosperm species.

evolutionary biology↗

Paternal genome elimination creates contrasting evolutionary trajectories in male and female citrus mealybugs

Most studies of sex-biased genes explore their evolution in familiar chromosomal sex determination systems, leaving the evolution of sex differences under alternative reproductive systems unknown. Here we explore the system of paternal genome elimination employed by mealybugs (Hempitera: Pseudococcidae) which have no sex chromosomes. Instead, all chromosomes are autosomal and inherited in two copies, but sex is determined by the ploidy of expression. Females express both parental alleles, but males reliably silence their paternally inherited chromosomes, creating genome-wide haploid expression in males and diploid expression in females. Additionally, sons do not express alleles directly inherited from their fathers, potentially disrupting the evolution of male-benefitting traits. To understand how these dynamics impact molecular evolution, we generated sex-specific RNAseq, a new gene annotation, and whole-genome population sequencing of the citrus mealybug, Planococcus citri. We found that genes expressed primarily in females hold more variation and evolve more quickly than those expressed in males or both sexes. Conversely, more adaptation occurs in genes expressed mainly in males than those expressed in females. Put together, paternal genome elimination appears to slow change on the male side but, by increasing selective scrutiny, increase the amount of adaptation in these genes. These results expand our understanding of evolution in a non-mendelian genetic system and the data we generated should prove useful for future research on this pest insect.

evolutionary biology↗

Genome report: Genome sequence of the tuliptree scale insect, Toumeyella liriodendri (Gmelin)

Scale insects are of interest both to basic researchers for their unique reproductive biology and to applied researchers for their pest status. In spite of this interest, there remain few genomic resources for this group of insects. To begin addressing this lack of data, we present the genome sequence of the tuliptree scale insect, Toumeyella liriodendri (Gmelin) (Hemiptera: Coccomorpha: Coccidae). The genome assembly spans 536Mb, with over 96% of sequence assembled into one of 17 chromosomal scaffolds. We characterize roughly 66% of this sequence as repetitive and annotate 16,508 protein coding genes. Then we use the reference genome to explore the phylogeny of soft scales (Coccidae) and evolution of karyotype within the family. We find that T. liriodendri is an early-diverging soft scale, less closely related to most sequenced soft scales than a species of the family Aclerdidae is. This molecular result bolsters a previous, character-based phylogenetic placement of Aclerdidae within Coccidae. In terms of genome structure, T. liriodendri has nearly twice as many chromosomes as the only other soft scale assembled to the chromosome level, Ericerus pela (Chavannes). In comparing the two, we find that chromosome number evolution can largely be explained by simple fissions rather than more complex rearrangements. These genomic natural history observations lay a foundation for further exploration of this unique group of insects.

genomics↗

Retention of an endosymbiont for the production of a single molecule

Sap-feeding insects often maintain multiple nutritional endosymbionts, which act in concert to produce compounds essential for insect survival. Many mealybugs have endosymbionts in a nested configuration: one or two bacterial species reside within the cytoplasm of another bacterium, and to-gether these bacteria have genomes which encode interdependent but complete sets of genes needed to produce key nutritional molecules. Here we show that the mealybug Pseudococcus viburni has three endosymbionts, one of which contributes only two genes that produce a single host nutrition-related molecule. All three bacterial endosymbionts have tiny genomes, suggesting that they have been co-evolving inside their insect host for millions of years. SignificanceNutritional endosymbionts synthesize (or contribute to the synthesis of) key metabolites such as essential amino acids and vitamins for their host organism. These nutrients are required by hosts because of their restricted diets, which in the case of mealybugs consists solely of plant phloem sap. Genome sequencing of insect endosymbionts has shown that their genomes can be very small, encoding few genes outside of core bacterial processes and nutrient provisioning. Here we highlight an example that has taken this reductive process to the extreme: a mealybug endosymbiont contributes only a single essential compound, chorismate, to the symbiosis.

evolutionary biology↗

Genetic drift drives faster-Z evolution in the salmon louse Lepeophtheirus salmonis

Sex chromosome evolution is a particularly complex sub-field of population genetics and there are still unresolved questions about how quickly and adaptively these chromosomes should evolve compared to autosomes. One key limitation to existing knowledge is an intense focus on only a handful of taxa in existing literature, resulting in uncertainty about whether observed patterns reflect general processes or are idiosyncratic to the more widely studied clades. In particular, the Z chromosomes of female heterogametic (ZW) systems tend to be quickly but not adaptively evolving in birds, while in butterflies and moths Z chromosomes tend to be evolving adaptively, but not always faster than autosomes. To understand how these two observations fit into broader evolutionary patterns, we explore, for the first time, patterns of Z chromosome evolution outside of these two well-studied clades. We utilize a publicly available high quality genome, gene expression, population, and outgroup data for the salmon louse Lepeophtheirus salmonis, an important aquacultural pest copepod. We find that the Z chromosome is faster evolving than the autosomes, but that this increased effect is driven by drift rather than adaptive evolution. This faster-Z effect seems to be a result of a very low effective population size of the Z chromosome, as well as high rates of female reproductive failure contributing to decreased efficiency of hemizygous selection acting on the Z. These results highlight the usefulness of organismal life history in calibrating population genetic expectations and demonstrate the usefulness of the ever-expanding wealth of modern publicly available genomic data to help resolve outstanding evolutionary questions.

evolutionary biology↗

Genome sequence of Ophryocystis elektroscirrha, an apicomplexan parasite of monarch butterflies: cryptic diversity and response to host-sequestered plant chemicals

Apicomplexa are ancient and diverse organisms which have been poorly characterized by modern genomics. To better understand the evolution and diversity of these single-celled eukaryotes, we sequenced the genome of Ophryocystis elektroscirrha, a parasite of monarch butterflies, Danaus plexippus. The genome is miniscule, totaling only 9 million bases and containing fewer than 3,000 genes. We then compared this new sequence to the two other sequenced invertebrate-infecting apicomplexans, Porospora gigantea and Gregarina niphandrodes, which have nearly twice the gene content and found that O. elektroscirrha shares different orthologs with each sequenced relative, suggesting the true set of universally conserved apicomplexan genes is very small indeed. We investigated sequenced reads from other potential hosts to explore the viability of in silico infection screening. We recovered a similarly sized parasite genome from another butterfly, Danaus chrysippus, that was highly diverged from the O. elektroscirrha reference, possibly representing a distinct species. Using these two new genomes, we investigated potential evolutionary response by parasites to toxic phytochemicals their hosts ingest and sequester. Monarch butterflies are well-known to tolerate toxic cardenolides thanks to changes in the sequence of their Type II ATPase sodium pumps. We show that Ophryocystis completely lacks Type II or Type 4 sodium pumps, and related proteins PMCA calcium pumps show extreme sequence divergence compared to other Apicomplexa, demonstrating new avenues of research opened by genome sequencing of non-model Apicomplexa. Author SummaryThere are many relatives of Plasmodium, the single-celled parasites responsible for malaria, and they infect a wide range of animals, including insects. These parasites have received less attention however, leaving much unknown about them. We sequenced the genome of one such parasite, Ophryocystis elektroscirrha (OE), to compare it to better-studied parasites and shed light on OEs interaction with its host, the monarch butterfly. We found that OE has a tiny genome with the fewest genes of any sequenced parasite in this group, lacking many genes found in its relatives. Using our new data, we also discovered evidence that infections of other butterfly species that have been attributed to OE may be caused by a previously undiscovered distinct parasite species. And finally, we explored the evolution of a family of genes that may be targeted by medicinal plant compounds in the monarch butterflys diet; OE has lost one of these genes and radically changed the sequence of another, setting a direction for future research.

genomics↗

Recent evolution of a maternally-acting sex-determining supergene in a fly with single-sex broods

Sex determination is a key developmental process, yet it is remarkably variable across the tree of life. The dipteran family Sciaridae exhibits one of the most unusual sex determination systems in which mothers control offspring sex through selective elimination of paternal X chromosomes. Whereas in some members of the family females produce mixed-sex broods, others such as the dark-winged fungus gnat Bradysia coprophila are monogenic, with females producing single-sex broods. Female-producing females were previously found to be heterozygous for a large X-linked paracentric inversion (X), which is maternally inherited and absent from male-producing females. Here we assembled and characterized the X sequence. As close sequence homology between the X and X made identification of the inversion challenging, we developed a k-mer-based approach to bin genomic reads before assembly. We confirmed that the inversion spans most of the X chromosome (approximately 55Mb) and encodes around 3500 genes. Analysis of the divergence between the inversion and the homologous region of the X revealed that it originated very recently (<0.5 mya). Surprisingly, we found that the X is more complex than previously thought and is likely to have undergone multiple rearrangements that have produced regions of varying ages, resembling a supergene composed of evolutionary strata. We found functional degradation of around 7.3% of genes within the region of recombination suppression, but no evidence of accumulation of repetitive elements. Our findings provide an indication that sex-linked inversions are driving turnover of the strange sex determination system in this family of flies.

evolutionary biology↗

The B chromosome of Pseudococcus viburni: a selfish chromosome that exploits whole-genome meiotic drive

Meiosis, the key process underlying sexual reproduction, is generally a fair process: each chromosome has a 50% chance of being included into each gamete. However in some organisms meiosis has become highly aberrant with some chromosomes having a higher chance of making it into gametes than others. Yet why and how such systems evolve remains unclear. Here we study the unusual reproductive genetics of mealybugs, in which only maternal-origin chromosomes are included into the gametes during male meiosis, while paternally-derived chromosomes degrade. This "whole genome meiotic drive" occurs in all males and is evolutionarily conserved. However one species - the obscure mealybug Pseudococcus viburni - has a segregating B chromosome that increases in frequency by escaping paternal genome elimination. Here we present whole-genome and gene expression data from laboratory lines with and without B chromosomes. These data allow us to identify B-linked sequences including >70 protein-coding genes as well as a B-specific satellite repeat that makes up a significant proportion of the chromosome. We also used these data to investigate the evolutionary origin of the B chromosome. The few paralogs between the B and the core genome are distributed throughout the genome, showing that it is unlikely that the B originated through a simple duplication of one of the autosomes. We also find that while many of the B-linked genes do not have paralogs within the P.viburni genome, but they do show orthology with genes in other hemipteran insects suggesting that the B might have originated from fission of one of the autosomes, possibly followed by further translocations of individual genes. Finally in order to understand the mechanisms by which the B is able to escape elimination when paternally-derived we generated gene expression data for males and females with and without B chromosomes. We find that at the developmental stage when meiosis is taking place only a small number of B-linked genes show significant expression. Only one gene was significantly over-expressed during male meiosis, which is when the drive occurs: a acetyltransferase involved in H3K56Ac, which has a putative role in meiosis and is therefore a promising candidate for further studies. Together, these results form a promising foundation for studying the mechanisms of meiotic drive in a system that is uniquely suited for this approach.

evolutionary biology↗

Testing impacts of goal-oriented outreach with the Girl Scouts: Can a single activity change attitudes towards insects?

Most people meet insects with fear and disgust but this reputation is largely unfounded, as few insects pose health risks. In fact, many are beneficial and their absence would adversely affect human life; thus insect conservation is important but unpopular. We have begun addressing these concerns as part of a broader effort to establish an ongoing outreach partnership between graduate students at the University of Kansas and the Girl Scouts of Northeast Kansas/Northwest Missouri. To explore ways to advocate for insect conservation, we held an insect collecting activity at a Girl Scout summer camp and surveyed changes in attitudes towards insects afterwards. This activity positively changed reactions to insect encounters and increased confidence in identifying harmful insects but did not strongly reduce fears or increase curiosity towards insects. Beyond these proximate results, this project highlights the potential of Girl Scout troops as targets for informal science education that can benefit both academics and the broader community.

scientific communication and education↗

Population differentiation and structural variation in the genome of Manduca sexta across the United States

Many species that are extensively studied in the laboratory are less well characterized in their natural habitat, and laboratory strains represent only a small fraction of the variation in a species genome. Here we investigate genomic variation in three natural North American populations of an agricultural pest and a model insect for many scientific disciplines, the tobacco hornworm (Manduca sexta). We show that hornworms from Arizona, Kansas, and North Carolina are genetically distinct, with Arizona being particularly differentiated from the other two populations using Illumina whole-genome resequencing. Peaks of differentiation exist across the genome, but here we focus in on the most striking regions. In particular, we identify two likely segregating inversions found in the Arizona population. One inversion on the Z chromosome may enhance adaptive evolution of the sex chromosome. The larger, autosomal inversion contains a pseudogene may be involved in the exploitation of a novel hostplant in Arizona, but functional genetic assays will be required to support this hypothesis. Nevertheless, our results reveal undiscovered natural variation and provide useful genomic data for both pest management and evolutionary genetics of this insect species.

evolutionary biology↗

Sex, males, and hermaphrodites in the scale insect Icerya purchasi

Androdioecy (the coexistence of males and hermaphrodites) is a rare mating system for which the evolutionary dynamics are poorly understood. Here we study the only presumed case of androdioecy in insects, found in the cottony cushion scale, Icerya purchasi. In this species, female-like hermaphrodites have been shown to produce sperm and self-fertilize. However, rare males are sometimes observed too. In a large population-genetic analysis, we show for the first time that although self-fertilization appears to be the primary mode of reproduction, rare outbreeding events between males and hermaphrodites do occur, and we thereby confirm androdioecy as the mating system of I. purchasi. Thus, this insect appears to have the colonization advantages of a selfing organism while also benefitting from periodic reintroduction of genetic variation through outbreeding with males.

evolutionary biology↗

ZZ Top: faster and more adaptive Z chromosome evolution in two Lepidoptera

The rate of divergence for Z or X chromosomes is theoretically predicted to be greater than autosomes, but the possible explanations for this pattern vary, as do empirical results from diverse taxa. Even among moths and butterflies (Lepidoptera), which generally share a single-origin Z chromosome, the handful of available studies give mixed support for faster or more adaptive evolution of the Z chromosome, depending on the species assayed. Here, we examine the molecular evolution of Z chromosomes in two additional lepidopteran species: the Carolina sphinx moth and the monarch butterfly, the latter of which possesses a recent chromosomal fusion yielding a segment of newly Z-linked DNA. We find evidence for both faster and more adaptive Z chromosome evolution in both species, though this effect is strongest in the neo-Z portion of the monarch sex chromosome. The neo-Z is less male-biased than expected of a Z chromosome, and unbiased and female-biased genes drive the signal for adaptive evolution here. Together these results suggest that male-biased gene accumulation and haploid selection have opposing effects on long-term rates of adaptation and may help explain the discrepancies in previous findings as well as the repeated evolution of neo-sex chromosomes in Lepidoptera.

evolutionary biology↗