Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species.

BACKGROUND: Helicoverpa armigera and Helicoverpa zea are major caterpillar pests of Old and New World agriculture, respectively. Both, particularly H. armigera, are extremely polyphagous, and H. armigera has developed resistance to many insecticides. Here we use comparative genomics, transcriptomics and resequencing to elucidate the genetic basis for their properties as pests. RESULTS: We find that, prior to their divergence about 1.5 Mya, the H. armigera/H. zea lineage had accumulated up to more than 100 more members of specific detoxification and digestion gene families and more than 100 extra gustatory receptor genes, compared to other lepidopterans with narrower host ranges. The two genomes remain very similar in gene content and order, but H. armigera is more polymorphic overall, and H. zea has lost several detoxification genes, as well as about 50 gustatory receptor genes. It also lacks certain genes and alleles conferring insecticide resistance found in H. armigera. Non-synonymous sites in the expanded gene families above are rapidly diverging, both between paralogues and between orthologues in the two species. Whole genome transcriptomic analyses of H. armigera larvae show widely divergent responses to different host plants, including responses among many of the duplicated detoxification and digestion genes. CONCLUSIONS: The extreme polyphagy of the two heliothines is associated with extensive amplification and neofunctionalisation of genes involved in host finding and use, coupled with versatile transcriptional responses on different hosts. H. armigera's invasion of the Americas in recent years means that hybridisation could generate populations that are both locally adapted and insecticide resistant.

Population structure and gene flow in the global pest, Helicoverpa armigera.

Helicoverpa armigera is a major agricultural pest that is distributed across Europe, Asia, Africa and Australasia. This species is hypothesized to have spread to the Americas 1.5 million years ago, founding a population that is at present, a distinct species, Helicoverpa zea. In 2013, H. armigera was confirmed to have re-entered South America via Brazil and subsequently spread. The source of the recent incursion is unknown and population structure in H. armigera is poorly resolved, but a basic understanding would highlight potential biosecurity failures and determine the recent evolutionary history of region-specific lineages. Here, we integrate several end points derived from high-throughput sequencing to assess gene flow in H. armigera and H. zea from populations across six continents. We first assemble mitochondrial genomes to demonstrate the phylogenetic relationship of H. armigera with other Heliothine species and the lack of distinction between populations. We subsequently use de novo genotyping-by-sequencing and whole-genome sequences aligned to bacterial artificial chromosomes, to assess levels of admixture. Primarily, we find that Brazilian H. armigera are derived from diverse source populations, with strong signals of gene flow from European populations, as well as prevalent signals of Asian and African ancestry. We also demonstrate a potential field-caught hybrid between H. armigera and H. zea, and are able to provide genomic support for the presence of the H. armigera conferta subspecies in Australasia. While structure among the bulk of populations remains unresolved, we present distinctions that are pertinent to future investigations as well as to the biosecurity threat posed by H. armigera.

Temporal metabolic rate variation in a continental Antarctic springtail.

Terrestrial systems in Antarctica are characterized by substantial spatial and temporal variation. However, few studies have addressed the paucity of data on metabolic responses to the unpredictable Antarctic environment, particularly with regard to terrestrial biota. This study measured metabolic rate variation for individual springtails at a continental Antarctic site using a fiber-optic closed respirometry system incorporating a custom-made respiration chamber. Concurrent measures of (behavioural) activity were made via daily pitfall counts. Metabolic rate of Gomphiocephalus hodgsoni measured at constant temperature varied systematically with progression through the austral summer, and was greatest mid-season. This finding of clear intra-seasonal and temperature-independent variation in mass-specific metabolic rate in G. hodgsoni is one of very few such reports for a terrestrial invertebrate (and the only such study for Antarctica), and parallels physiological studies in the Antarctic marine environment linking metabolic rate elevation with biological function rather than temperature adaptation per se. However, response to temperature at relatively short time-scales is also likely to be an important part of the life history strategy of Antarctic terrestrial invertebrates such as G. hodgsoni, which appears capable of both physiologically and behaviourally 'tuning' in to short-term thermal variability to respond appropriately to the local unpredictable Antarctic habitat.

Temporal and spatial metabolic rate variation in the Antarctic springtail Gomphiocephalus hodgsoni.

Spatial and temporal environmental variation in terrestrial Antarctic ecosystems are known to impact species strongly at a local scale, but the ways in which organisms respond (e.g. physiologically, behaviourally) to such variation are poorly understood. Further, very few studies have attempted to assess inter-annual variability of such responses. Building on previous work demonstrating intra-seasonal variation in standard metabolic rate in the springtail Gomphiocephalushodgsoni, we investigated variation in metabolic activity of G. hodgsoni across two austral summer periods at Cape Bird, Ross Island. We also examined the influence of spatial variation by comparing metabolic rates of G. hodgsoni at Cape Bird with those from two other isolated continental locations within Victoria Land (Garwood and Taylor Valleys). We found significant differences between metabolic rates across the 2 years of measurement at Cape Bird. In addition, standard metabolic rates of G. hodgsoni obtained from Garwood and Taylor Valleys were significantly higher than those at Cape Bird where habitats are comparable, but environmental characteristics differ (e.g. microclimatic temperatures are higher). We discuss potential underlying causes of these metabolic rate variation patterns, including those related to differences among individuals (e.g. physiological and genetic differences), locations (e.g. habitat quality and microclimatic regime differences) and populations (e.g. acclimation differences among G. hodgsoni populations in the form of metabolic cold adaptation (MCA)).