Phylogenomic resolution of the Ceratitis FARQ complex (Diptera: Tephritidae).

The Ceratitis FARQ complex (formerly FAR complex) includes four frugivorous tephritids, Ceratitis fasciventris, C. anonae, C. rosa and C. quilicii, the latter two causing important agricultural losses in Africa. Although FARQ species can be identified on the basis of subtle morphological differences, they cannot be resolved as monophyletic when trying phylogenetic tree reconstructions based on mitochondrial or nuclear gene fragments except for microsatellites. In this study, we used mitogenome and genome-wide SNPs to investigate the phylogenetic relationship within the complex as well as between all four Ceratitis subgenera. The analysis of 13 species supported the monophyly of the Ceratitis subgenera Ceratitis, Ceratalaspis, Pardalaspis, and recovered Pterandrus as paraphyletic but could not properly resolve species within the FARQ complex. Conversely, gene and species tree reconstructions based on 785,484 genome-wide SNPs could consistently resolve the FARQ taxa and provide insights into their phylogenetic relationships. Gene flow was detected by TreeMix analysis from C. quilicii to C. fasciventris, suggesting the existence of introgression events in the FARQ complex. Our results suggest that genome-wide SNPs represent a suitable tool for the molecular diagnosis of FARQ species and could possibly be used to develop rapid diagnostic methods or to trace the origins of intercepted samples.

Genomes of the cosmopolitan fruit pest Bactrocera dorsalis (Diptera: Tephritidae) reveal its global invasion history and thermal adaptation.

INTRODUCTION: The oriental fruit fly Bactrocera dorsalis is one of the most destructive agricultural pests worldwide, with highly debated species delimitation, origin, and global spread routes. OBJECTIVES: Our study intended to (i) resolve the taxonomic uncertainties between B. dorsalis and B. carambolae, (ii) reveal the population structure and global invasion routes of B. dorsalis across Asia, Africa, and Oceania, and (iii) identify genomic regions that are responsible for the thermal adaptation of B. dorsalis. METHODS: Based on a high-quality chromosome-level reference genome assembly, we explored the population relationship using a genome-scale single nucleotide polymorphism dataset generated from the resequencing data of 487 B. dorsalis genomes and 25 B. carambolae genomes. Genome-wide association studies and silencing using RNA interference were used to identify and verify the candidate genes associated with extreme thermal stress. RESULTS: We showed that B. dorsalis originates from the Southern India region with three independent invasion and spread routes worldwide: (i) from Northern India to Northern Southeast Asia, then to Southern Southeast Asia; (ii) from Northern India to Northern Southeast Asian, then to China and Hawaii; and (iii) from Southern India toward the African mainland, then to Madagascar, which is mainly facilitated by human activities including trade and immigration. Twenty-seven genes were identified by a genome-wide association study to be associated with 11 temperature bioclimatic variables. The Cyp6a9 gene may enhance the thermal adaptation of B. dorsalis and thus boost its invasion, which tended to be upregulated at a hardening temperature of 38 °C. Functional verification using RNA interference silencing against Cyp6a9, led to the specific decrease in Cyp6a9 expression, reducing the survival rate of dsRNA-feeding larvae exposed to extreme thermal stress of 45 °C after heat hardening treatments in B. dorsalis. CONCLUSION: This study provides insights into the evolutionary history and genetic basis of temperature adaptation in B. dorsalis.

Population structure of a global agricultural invasive pest, Bactrocera dorsalis (Diptera: Tephritidae).

Bactrocera dorsalis, the Oriental fruit fly, is one of the world's most destructive agricultural insect pests and a major impediment to international fresh commodity trade. The genetic structuring of the species across its entire geographic range has never been undertaken, because under a former taxonomy B. dorsalis was divided into four distinct taxonomic entities, each with their own, largely non-overlapping, distributions. Based on the extensive sampling of six a priori groups from 63 locations, genetic and geometric morphometric datasets were generated to detect macrogeographic population structure, and to determine prior and current invasion pathways of this species. Weak population structure and high genetic diversity were detected among Asian populations. Invasive populations in Africa and Hawaii are inferred to be the result of separate, single invasions from South Asia, while South Asia is also the likely source of other Asian populations. The current northward invasion of B. dorsalis into Central China is the result of multiple, repeated dispersal events, most likely related to fruit trade. Results are discussed in the context of global quarantine, trade, and management of this pest. The recent expansion of the fly into temperate China, with very few associated genetic changes, clearly demonstrates the threat posed by this pest to ecologically similar areas in Europe and North America.