The role of endosymbionts in the evolution of haploid-male genetic systems in scale insects (Coccoidea)

There is an extraordinary diversity in genetic systems across species, but this variation remains poorly understood. In part, this is because the mechanisms responsible for transitions between systems are often unknown. A recent hypothesis has suggested that conflict between hosts and endosymbiotic microorganisms over transmission could drive the transition from diplodiploidy to systems with male haploidy (haplodiploidy, including arrhenotoky and paternal genome elimination [PGE]). Here, we present the first formal test of this idea with a comparative analysis across scale insects (Hemiptera: Coccoidea). Scale insects are renowned for their large variation in genetic systems, and multiple transitions between diplodiploidy and haplodiploidy have taken place within this group. Additionally, most species rely on endosymbiotic microorganisms to provide them with essential nutrients lacking in their diet. We show that species harboring endosymbionts are indeed more likely to have a genetic system with male haploidy, which supports the hypothesis that endosymbionts might have played a role in the transition to haplodiploidy. We also extend our analysis to consider the relationship between endosymbiont presence and transitions to parthenogenesis. Although in scale insects there is no such overall association, species harboring eukaryote endosymbionts were more likely to be parthenogenetic than those with bacterial symbionts. These results support the idea that intergenomic conflict can drive the evolution of novel genetic systems and affect host reproduction.Peer reviewe

NEW SINGLE-COPY NUCLEAR GENES FOR USE IN SCALE INSECT SYSTEMATICS

Despite the advent of next-generation sequencing, the polymerase chain reaction (PCR) and Sanger sequencing remain useful tools for molecular identification and systematics. To date, molecular systematics of scale insects has been constrained by the paucity of loci that researchers have been able to amplify with available PCR primers. Due to the rapid molecular evolution of scale insects, “universal” primers, and even primers developed for their sister taxon the Aphidoidea, typically fail. We used transcriptome data for two diaspidids, Acutaspis umbonifera (Newstead) and Chrysomphalus aonidum (Linnaeus), together with a published aphid genome, to design novel PCR primer sets for scale insects. Our primers amplify fragments of eight single-copy genes: ATP-dependent RNA helicase (DHX8), translation initiation factor5 (IF5X1), DNA replication licensing factor (Mcm2), double-strand break repair protein (MRE11A), serine/threonine- protein phosphatase (PPP1CB), DNA-directed RNA polymerase II (RNApII), ribonucleoside-diphosphate reductase (RRM1), signal recognition particle receptor (SRPα), neuronal PAS domain-containing protein 4 (NPAS4), and cleft lip and palate transmembrane protein 1 (TP1). Here we report the results of tests of amplification success and phylogenetic utility of these primer sets across the Diaspididae and nine other families of Coccomorpha

Gene expression plasticity across hosts of an invasive scale insect species

For plant-eating insects, we still have only a nascent understanding of the genetic basis of host-use promiscuity. Here, to improve that situation, we investigated host-induced gene expression plasticity in the invasive lobate lac scale insect, Paratachardina pseudolobata (Hemiptera: Keriidae). We were particularly interested in the differential expression of detoxification and effector genes, which are thought to be critical for overcoming a plant's chemical defenses. We collected RNA samples from P. pseudolobata on three different host plant species, assembled transcriptomes de novo, and identified transcripts with significant host-induced gene expression changes. Gene expression plasticity was pervasive, but the expression of most detoxification and effector genes was insensitive to the host environment. Nevertheless, some types of detoxification genes were more differentially expressed than expected by chance. Moreover, we found evidence of a trade-off between expression of genes involved in primary and secondary metabolism; hosts that induced lower expression of genes for detoxification induced higher expression of genes for growth. Our findings are largely consonant with those of several recently published studies of other plant-eating insect species. Thus, across plant-eating insect species, there may be a common set of gene expression changes that enable host-use promiscuity

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

Funding: This work was supported by a number of fellowships, namely a University Research Fellowship from Royal Society of London (to AG) and a Junior Research Fellowship from Balliol College, Oxford to AG. Funding came from Independent Research Fellowships from Natural Environment Research Council (grant no. NE/K009524/1 to AG and NE/K009516/1 to LR), a Consolidator Grant from European Research Council (grant no. 771387 to AG), a European Research Countil Starting Grant (PGErepro to LR), and a Royal Society Newton fellowship (to LR).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.Publisher PDFPeer reviewe

The Strange Case of the Armored Scale Insect and Its Bacteriome

Armored scale insects are unusual in that a part of their bodies is genetically distinct from the rest. This extraordinary phenomenon challenges the notion of identit

Extending our scientific reach in arboreal ecosystems for research and management

The arboreal ecosystem is vitally important to global and local biogeochemical processes, the maintenance of biodiversity in natural systems, and human health in urban environments. The ability to collect samples, observations, and data to conduct meaningful scientific research is similarly vital. The primary methods and modes of access remain limited and difficult. In an online survey, canopy researchers (n = 219) reported a range of challenges in obtaining adequate samples, including ∼10% who found it impossible to procure what they needed. Currently, these samples are collected using a combination of four primary methods: (1) sampling from the ground; (2) tree climbing; (3) constructing fixed infrastructure; and (4) using mobile aerial platforms, primarily rotorcraft drones. An important distinction between instantaneous and continuous sampling was identified, allowing more targeted engineering and development strategies. The combination of methods for sampling the arboreal ecosystem provides a range of possibilities and opportunities, particularly in the context of the rapid development of robotics and other engineering advances. In this study, we aim to identify the strategies that would provide the benefits to a broad range of scientists, arborists, and professional climbers and facilitate basic discovery and applied management. Priorities for advancing these efforts are (1) to expand participation, both geographically and professionally; (2) to define 2–3 common needs across the community; (3) to form and motivate focal teams of biologists, tree professionals, and engineers in the development of solutions to these needs; and (4) to establish multidisciplinary communication platforms to share information about innovations and opportunities for studying arboreal ecosystems

Schematic Diagram of the Genetic System of a Diaspidid Scale Insect

<p>Zygote 1 is the fertilized ovum from which all organismal tissues except the bacteriome develop (black arrows). The bacteriome develops from zygote 2 (green arrows). Each haploid genome is represented by an N. A haploid genome may come from the oocyte (pink), sperm (blue), or polar bodies (black). The blue and pink arrows emphasize that the maternal versus paternal identity of a haploid genome is reset (imprinted) in each generation; thus, a male transmits only his maternal genome, but in his offspring the same chromosomes behave as a paternal genome (schematically, the pink N is converted to blue during spermatogenesis).</p