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Biology subjects

Sword, G. A.

Publications and source records attributed to Sword, G. A..

8 recordsLinked to original sources

Multiple roads to swarming: divergent molecular machineries drive the repeated evolution of locusts

Locust swarming, one of nature's most spectacular examples of a repeated emergent polyphenism, has long been suspected to rely on conserved "swarming genes" or shared genomic features. By applying a model-clade approach comparing six species that vary in their degrees of plasticity and collective behavior, we show that the evolution of swarming locusts is not driven by shared genomic features or a universal set of swarming genes. In contrast, we find that this phenomenon evolved through flexible regulatory architectures, in which the degree of behavioral plasticity directly correlates with the total scale of density-responsive gene expression. While different locust species recruit largely non-overlapping gene sets to achieve the same syndrome, these divergent molecular machineries converge on similar higher-level biological functions. Thus, multiple molecular pathways achieve locust swarming, challenging the preconceived notion about the genetic prerequisites to transition from solitary to collective states. Further, we establish that a complex syndrome such as locust swarming emerges through modular regulatory systems that can be amplified, modified, or attenuated across the tree of life.

evolutionary biology↗

Rearing, dissection, and temporal transcriptomic profiling protocols to study density-dependent phenotypic plasticity in Schistocerca (Insecta: Orthoptera)

This protocol generates gregarious and solitarious density-dependent phenotypes in multiple Schistocerca species under controlled environmental conditions. It describes cage setup, feeding, animal handling, and sterile dissection workflows to isolate nervous, chemosensory, gut, fat body, and female reproductive tissues from nymphs and adults. It emphasizes rapid tissue stabilization and RNase-control practices for downstream single-tissue DNA and RNA analyses. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=136 SRC="FIGDIR/small/705994v1_ufig1.gif" ALT="Figure 1"> View larger version (43K): org.highwire.dtl.DTLVardef@59afdaorg.highwire.dtl.DTLVardef@283b72org.highwire.dtl.DTLVardef@156fa13org.highwire.dtl.DTLVardef@13bf71b_HPS_FORMAT_FIGEXP M_FIG C_FIG

zoology↗

Identification of a novel resistance gene which provides insight into Vip3Aa mode of action in Helicoverpa armigera

The global reliance on Bacillus thuringiensis (Bt) proteins for controlling lepidopteran pests in cotton, corn, and soybean crops underscores the critical need to understand resistance mechanisms. Vip3Aa, one of the most widely deployed and currently effective Bt proteins in genetically modified crops, plays a pivotal role in pest management. This study identifies the molecular basis of Vip3Aa resistance in Australian Helicoverpa armigera through genetic crosses, and integrated genomic and transcriptomic analyses. We identified a previously uncharacterized gene, LOC110373801 (designated HaVipR1), as a crucial determinant of Vip3Aa resistance in two field-derived resistant lines. Functional validation using CRISPR-Cas9 knockout in susceptible lines confirmed the genes role in conferring resistance. Despite extensive laboratory selection of Vip3Aa-resistant colonies in Lepidoptera, the biochemical mechanisms underlying resistance have remained elusive. Our research demonstrates that HaVipR1-mediated resistance operates independently of known resistance genes, including midgut-specific chitin synthase and the transcription factor SfMyb. The identification of HaVipR1 offers further insights into the Vip3Aa mechanism of action. This discovery is vital for devising strategies to counteract resistance and sustain the efficacy of Bt crops. Future research should focus on elucidating the biochemical pathways involving HaVipR1 and investigating its interactions with other resistance mechanisms. Our findings underscore the utility of analysing field-derived resistant lines in providing biologically relevant insights and stress the necessity for comprehensive management strategies to maintain agricultural productivity. Significance StatementThis is the first identification of a specific gene in Helicoverpa armigera which mediates resistance to the Bacillus thuringiensis (Bt) protein Vip3Aa. We identify that this gene is disrupted in two different ways in separate field-derived resistant lines, one being a large transposable element insertion in the first intron of the HaVipR1 gene, confirmed using long-read sequencing. Disruption of this gene using CRISPR-Cas9 knockout in a susceptible H. armigera line confers Vip3A resistance. The identification of a specific gene is important for molecular monitoring and management of H. armigera as well as other global pests of concern like Spodoptera frugiperda. These findings also offer insights for researchers aiming to understand how Vip3Aa functions, as the action pathway remains unclear.

genomics↗

Anisotropic interaction and motion states of locusts in a hopper band

Swarming locusts present a quintessential example of animal collective motion. Juvenile locusts march and hop across the ground in coordinated groups called hopper bands. Composed of up to millions of insects, hopper bands exhibit aligned motion and various collective structures. These groups are well-documented in the field, but the individual insects themselves are typically studied in much smaller groups in laboratory experiments. We present the first trajectory data that detail the movement of individual locusts within a hopper band in a natural setting. Using automated video tracking, we derive our data from footage of four distinct hopper bands of the Australian plague locust, Chortoicetes terminifera. We reconstruct nearly twenty-thousand individual trajectories composed of over 3.3 million locust positions. We classify these data into three motion states: stationary, walking, and hopping. Distributions of relative neighbor positions reveal anisotropies that depend on motion state. Stationary locusts have high-density areas distributed around them apparently at random. Walking locusts have a low-density area in front of them. Hopping locusts have low-density areas in front and behind them. Our results suggest novel insect interactions, namely that locusts change their motion to avoid colliding with neighbors in front of them.

animal behavior and cognition↗

The impact of dietary protein and carbohydrates on gene expression in a generalist insect herbivore

Nutrition fuels all of the physiological processes that animals rely on for survival and reproduction. Of all the nutrients that are required, dietary protein (p) and carbohydrates (c) have a primary role. Insect herbivores are capable of detecting amino acid and sugar concentrations in plant tissue via chemoreception and regulate their intake of these two macronutrients to reach an optimal protein:carbohydrate, or p:c, ratio, termed an intake target. A multitude of studies have shown that the two nutritional factors that have the strongest impact on insect survival and performance are dietary p:c ratio and total macronutrient content, which is the proportion of the diet made up by p and c and a proxy for energy content. Variations in these two dietary traits have strong unique and interactive effects on many insect life history traits, yet the mechanisms that mediate these effects are not well understood. While many studies have documented the effect of host plant usage on gene expression, differences in plant secondary compounds between plant species and tissue types have confounded efforts to understand nutritional contributions to transcriptional changes. This study is the first to document the transcriptional effects of dietary p:c ratio and total macronutrient content in a phytophagous insect, the polyphagous moth species Helicoverpa zea. Our results show that changes in dietary p:c ratio produced a rather limited transcriptional response, while total macronutrient content had more dramatic effects on gene expression. The invariable expression of many metabolic genes across diets also suggests that H. zea larvae employ a strategy of constitutive expression to deal with nutritional imbalances rather than diet-associated changes in expression. We also observed many similarities in the transcriptional response to diets that varied from the intake target diet in different ways (c-biased, p-biased, increased energy content). This indicates that similar mechanisms are used to deal with nutritional imbalances regardless of the direction of the imbalance, and further supports the importance of nutrient regulation. HIGHLIGHTSO_LIVariations in plant macronutrients can have strong impacts on herbivore fitness C_LIO_LIDespite a wealth of studies documenting the physiological effects of macronutrient nutrition, underlying mechanisms are still ambiguous C_LIO_LIDiet protein-to-carbohydrate ratio had an unexpectedly small impact on overall transcription, while total macronutrient content had a stronger effect C_LIO_LIThe transcriptional response to dietary variations away from an optimal diet was similar across diets that varied in different ways (carbohydrate-biased, protein-biased, more concentrated) C_LIO_LIMaintaining consistent consumption and constitutive expression of digestive enzymes across diets that varied in macronutrient profiles led to compensation for the most limiting dietary macronutrient C_LI

physiology↗

Gene-by-environment interactions in agricultural pest management: population effects on diet-Bt interactions in a caterpillar

Given that plant nutrient content is both spatially and temporally dynamic (Lenhart et al., 2015; Deans et al., 2016, 2018), insect herbivores are exposed to an incredible amount of nutritional variability. This variability can constrain insects to feeding on sub-optimal resources, but it can also provide an opportunity for insects to regulate their intake of specific nutrients to obtain an optimal balance. Nutrient regulation has implications for pest control strategies in agricultural systems, as the nutritional state of pest species may impact their susceptibility to insecticides. Deans et al. (2017) showed that diet macronutrient balance has significant effects on the susceptibility of Helicoverpa zea larvae to Cry1Ac, an endotoxin expressed in transgenic Bt crops. This was demonstrated using a highly inbred laboratory strain of H. zea, limiting the applicability of these results to field populations that encompass greater genetic diversity. In this study, we assessed the impact of field-relevant macronutrient variability on the efficacy of two Bt endotoxins, Cry1Ab and Cry1Ac, using three field populations collected from different geographic regions. This was done to further understand the impact of nutritional variability on Bt susceptibility and also to determine the relevance of these effects in the field. While we saw limited differences in Cry susceptibility across populations, dietary effects were highly variable. Across populations there were distinct population-level differences in the interactions between Cry concentration and diet, the type of Cry toxin impacted by diet, and the treatment diet that produced optimal survival and performance. These results show that nutrition can have strong impacts on Bt susceptibility but also that these impacts are strongly affected by genetic background in H. zea. To accurately assess Bt susceptibility in the field, including resistance monitoring, bioassay methods should incorporate the appropriate nutritional parameters and be as localized as possible.

ecology↗

Whole genome comparisons reveal panmixia among fall armyworm (Spodoptera frugiperda) from diverse locations

The fall armyworm (Spodoptera frugiperda (J.E. Smith)) is a highly polyphagous agricultural pest with long-distance migratory behavior threatening food security worldwide. This pest has a host range of >80 plant species, but two host strains are recognized based on their association with corn (C-strain) or rice and smaller grasses (R-strain). In this study, the population structure and genetic diversity in 55 S. frugiperda samples from Argentina, Brazil, Kenya, Puerto Rico and the United States (USA) were surveyed to further our understanding of whole genome nuclear diversity. Comparisons at the genomic level suggest panmixia in this population, other than a minor reduction in gene flow between the two overwintering populations in the continental USA that also corresponded to genetically distinct host strains. Two maternal lines were detected from analysis of mitochondrial genomes. We found members from the Eastern Hemisphere interspersed within both continental USA overwintering subpopulations, suggesting multiple individuals were likely introduced to Africa. Comparisons between laboratory-reared and field collected S. frugiperda support similar genomic diversity, validating the experimental use of laboratory strains. Our research is the largest diverse collection of United States S. frugiperda whole genome sequences characterized to date, covering eight continental states and a USA territory (Puerto Rico). The genomic resources presented provide foundational information to understand gene flow at the whole genome level among S. frugiperda populations.

genomics↗

Geomagnetic field absence influences adult body weight of a migratory insect, potentially through appetite regulation

The geomagnetic field (GMF) is well documented for its essential role as a cue used in animal orientation or navigation. Recent evidence indicates that the absence of GMF can trigger stress-like responses such as reduced body weight, as we have previously shown in newly emerged adults of the brown planthopper, Nilaparvata lugens. To test the hypothesis that reduced feeding in the absence of the GMF leads to a decrease of N. lugens body weight, we compared magnetic responses in feeding behavior, glucose levels, and expression of magnetoreception- and appetite-related genes in brown planthopper nymphs exposed to either a near-zero magnetic field (NZMF, i.e., GMF absence) or typical GMF conditions. In addition to observing the expected responses in the expression of the potential magnetosensor cryptochromes, the food intake of 5th instar nymphs was significantly reduced in insects reared in the absence of GMF. Insects that exhibited reduced feeding reared in the absence of the GMF also had higher glucose levels which is associated with food aversion. Expression patterns of appetite-related neuropeptide genes were also altered in the absence of GMF in a manner consistent with diminishing appetite. These findings support the hypothesis that strong changes in GMF intensity can affect insect feeding behavior and underlying regulatory processes. Our results provide further evidence that magnetoreception and regulatory responses to GMF changes can affect a wide variety of biological processes.

animal behavior and cognition↗