Can genomic signatures guide the selection of host-specific agents for weed biological control?

Biological control of weeds involves deliberate introduction of host-specific natural enemies into invaded range to reduce the negative impacts of invasive species. Assessing the specificity is a crucial step, as introduction of generalist natural enemies into a new territory may pose risks to the recipient communities. A mechanistic understanding of host use can provide valuable insights for the selection of specialist natural enemies, bolster confidence in non-target risk assessment and potentially accelerate the host specificity testing process in biological control. We conducted a comprehensive analysis of studies on the genomics of host specialization with a view to examine if genomic signatures can help predict host specificity in insects. Focusing on phytophagous Lepidoptera, Coleoptera and Diptera, we compared chemosensory receptors and enzymes between "specialist" (insects with narrow host range) and "generalist" (insects with wide host range) insects. The availability of genomic data for biological control agents (natural enemies of weeds) is limited thus our analyses utilized data from pest insects and model organisms for which genomic data are available. Our findings revealed that specialists generally exhibit a lower number of chemosensory receptors and enzymes compared with their generalist counterparts. This pattern was more prominent in Coleoptera and Diptera relative to Lepidoptera. This information can be used to reject agents with large gene repertoires to potentially accelerate the risk assessment process. Similarly, confirming smaller gene repertoires in specialists could further strengthen the risk evaluation. Despite the distinctive signatures between specialists and generalists, challenges such as finite genomic data for biological control agents, ad hoc comparisons, and fewer comparative studies among congeners limit our ability to use genomic signatures to predict host specificity. A few studies have empirically compared phylogenetically closely related species, enhancing the resolution and the predictive power of genomics signatures thus suggesting the need for more targeted studies comparing congeneric specialists and generalists.

Gene technologies in weed management: a technical feasibility analysis.

With the advent of new genetic technologies such as gene silencing and gene drive, efforts to develop additional management tools for weed management is gaining significant momentum. These technologies promise novel ways to develop sustainable weed control options because gene silencing can switch-off genes mediating adaptation (e.g. growth, herbicide resistance), and gene drive can be used to spread modified traits and to engineer wild populations with reduced fitness. However, applying gene silencing and/or gene drive is expected to be inherently complex as their application is constrained by several methodological and technological difficulties. In this review we explore the challenges of these technologies, and discuss strategies and resources accessible to accelerate the development of gene-tech based tools for weed management. We also highlight how gene technologies can be integrated into existing management tactics such as classical biological control, and their possible interactions.

Gene drives in plants: opportunities and challenges for weed control and engineered resilience.

Plant species, populations and communities are under threat from climate change, invasive pathogens, weeds and habitat fragmentation. Despite considerable research effort invested in genome engineering for crop improvement, the development of genetic tools for the management of wild plant populations has rarely been given detailed consideration. Gene drive systems that allow direct genetic management of plant populations via the spread of fitness-altering genetic modifications could be of great utility. However, despite the rapid development of synthetic tools and their enormous promise, little explicit consideration has been given to their application in plants and, to date, they remain untested. This article considers the potential utility of gene drives for the management of wild plant populations, and examines the factors that might influence the design, spread and efficacy of synthetic drives. To gain insight into optimal ways to design and deploy synthetic drive systems, we investigate the diversity of mechanisms underlying natural gene drives and their dynamics within plant populations and species. We also review potential approaches for engineering gene drives and discuss their potential application to plant genomes. We highlight the importance of considering the impact of plant life-history and genetic architecture on the dynamics of drive, investigate the potential for different types of resistance evolution, and touch on the ethical, regulatory and social challenges ahead.

Global mismatch of policy and research on drivers of biodiversity loss.

The United Nations 2030 Agenda for Sustainable Development calls for urgent actions to reduce global biodiversity loss. Here, we synthesize >44,000 articles published in the past decade to assess the research focus on global drivers of loss. Relative research efforts on different drivers are not well aligned with their assessed impact, and multiple driver interactions are hardly considered. Research on drivers of biodiversity loss needs urgent realignment to match predicted severity and inform policy goals.

Plant-Mediated Female Transcriptomic Changes Post-Mating in a Tephritid Fruit Fly, Bactrocera tryoni.

Female post-mating behaviors are regulated by complex factors involving males, females, and the environment. In insects, plant secondary compounds that males actively forage for, may indirectly modify female behaviors by altering male behavior and physiology. In the tephritid fruit fly, Bactrocera tryoni, females mated with males previously fed on plant-derived phenylpropanoids (="lures" based on usage in tephritid literature), have longer mating refractoriness, greater fecundity, and reduced longevity than females mated with non-lure fed males. This system thus provides a model for studying transcriptional changes associated with those post-mating behaviors, as the genes regulating the phenotypic changes are likely to be expressed at a greater magnitude than in control females. We performed comparative transcriptome analyses using virgin B. tryoni females, females mated with control males (control-mated), and females mated with lure-fed males (lure-mated). We found 331 differentially expressed genes (DEGs) in control-mated females and 80 additional DEGs in lure-mated females. Although DEGs in control-mated females are mostly immune response genes and chorion proteins, as reported in Drosophila species, DEGs in lure-mated females are titin-like muscle proteins, histones, sperm, and testis expressed proteins which have not been previously reported. While transcripts regulating mating (e.g., lingerer) did not show differential expression in either of the mated female classes, the odorant binding protein Obp56a was down-regulated. The exclusively enriched or suppressed genes in lure-mated females, novel transcripts such as titin and histones, and several taxa-specific transcripts reported here can shed more light on post-mating transcriptional changes, and this can help understand factors possibly regulating female post-mating behaviors.

Sexual selection in true fruit flies (Diptera: Tephritidae): transcriptome and experimental evidences for phytochemicals increasing male competitive ability.

In male tephritid fruit flies of the genus Bactrocera, feeding on secondary plant compounds (sensu lato male lures = methyl eugenol, raspberry ketone and zingerone) increases male mating success. Ingested male lures alter the male pheromonal blend, normally making it more attractive to females and this is considered the primary mechanism for the enhanced mating success. However, the male lures raspberry ketone and zingerone are known, across a diverse range of other organisms, to be involved in increasing energy metabolism. If this also occurs in Bactrocera, then this may represent an additional benefit to males as courtship is metabolically expensive and lure feeding may increase a fly's short-term energy. We tested this hypothesis by performing comparative RNA-seq analysis between zingerone-fed and unfed males of Bactrocera tryoni. We also carried out behavioural assays with zingerone- and cuelure-fed males to test whether they became more active. RNA-seq analysis revealed, in zingerone-fed flies, up-regulation of 3183 genes with homologues transcripts to those known to regulate intermale aggression, pheromone synthesis, mating and accessory gland proteins, along with significant enrichment of several energy metabolic pathways and gene ontology terms. Behavioural assays show significant increases in locomotor activity, weight reduction and successful mating after mounting; all direct/indirect measures of increased activity. These results suggest that feeding on lures leads to complex physiological changes, which result in more competitive males. These results do not negate the pheromone effect, but do strongly suggest that the phytochemical-induced sexual selection is governed by both female preference and male competitive mechanisms.

Cuelure but not zingerone make the sex pheromone of male Bactrocera tryoni (Tephritidae: Diptera) more attractive to females.

In tephritid fruit flies of the genus Bactrocera Macquart, a group of plant derived compounds (sensu amplo 'male lures') enhance the mating success of males that have consumed them. For flies responding to the male lure methyl eugenol, this is due to the accumulation of chemicals derived from the male lure in the male rectal gland (site of pheromone synthesis) and the subsequent release of an attractive pheromone. Cuelure, raspberry ketone and zingerone are a second, related group of male lures to which many Bactrocera species respond. Raspberry ketone and cuelure are both known to accumulate in the rectal gland of males as raspberry ketone, but it is not known if the emitted male pheromone is subsequently altered in complexity or is more attractive to females. Using Bactrocera tryoni as our test insect, and cuelure and zingerone as our test chemicals, we assess: (i) lure accumulation in the rectal gland; (ii) if the lures are released exclusively in association with the male pheromone; and (iii) if the pheromone of lure-fed males is more attractive to females than the pheromone of lure-unfed males. As previously documented, we found cuelure was stored in its hydroxyl form of raspberry ketone, while zingerone was stored largely in an unaltered state. Small but consistent amounts of raspberry ketone and ß-(4-hydroxy-3-methoxyphenyl)-propionic acid were also detected in zingerone-fed flies. Males released the ingested lures or their analogues, along with endogenous pheromone chemicals, only during the dusk courtship period. More females responded to squashed rectal glands extracted from flies fed on cuelure than to glands from control flies, while more females responded to the pheromone of calling cuelure-fed males than to control males. The response to zingerone treatments in both cases was not different from the control. The results show that male B. tryoni release ingested lures as part of their pheromone blend and, at least for cuelure, this attracts more females.

Genomic resources notes accepted 1 December 2013-31 January 2014.

This article documents the public availability of (i) transcriptome sequence data, assembled and annotated contigs and unigenes, and BLAST hits from the Queensland fruit fly, Bactrocera tryoni; (ii) 75 single-nucleotide variants (SNVs) from 454 sequencing of reduced representation libraries for Phalangiidae harvestmen, Megabunus armatus, Megabunus vignai, Megabunus lesserti, and Rilaena triangularis; and (iii) expressed sequence tags from 454 sequencing of the lepidopterans Lymantria dispar and Lymantria monacha.