Chromosome-scale genome of the polyphagous pest Anastrepha ludens (Diptera: Tephritidae) provides insights on sex chromosome evolution in Anastrepha

Authors: CONGRAINS, CARLOS - University Of Hawaii; Sim, Sheina; PAULO, DANIEL - University Of Hawaii; Corpuz, Renee; Kauwe, Angela; SIMMONDS, TYLER - Oak Ridge Institute For Science And Education (ORISE); Simpson, Sheron; Scheffler, Brian; Geib, Scott

Submitted to: G3: Genes, Genomes, Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/18/2024
Publication Date: 10/4/2024
Citation: Congrains, C., Sim, S.B., Paulo, D.F., Corpuz, R.L., Kauwe, A.N., Simmonds, T.J., Simpson, S.A., Scheffler, B.E., Geib, S.M. 2024. Chromosome-scale genome of the polyphagous pest Anastrepha ludens (Diptera: Tephritidae) provides insights on sex chromosome evolution in Anastrepha. G3: Genes, genomics, genetics. 14(12). Article jkae239. https://doi.org/10.1093/g3journal/jkae239.
DOI: https://doi.org/10.1093/g3journal/jkae239

Interpretive Summary: The Mexican fruit fly, Anastrepha ludens, is a polyphagous true fruit fly considered one of the most serious insect pest to fruits in Central and North America. Despite its agricultural relevance, a high-quality genome assembly has not been reported, which limits the capacity of incorporate cutting edge technologies such genome editing (e.g., CRISPR-based approaches) and molecular taxonomy (e.g., using a multilocus approach to discriminate members of species complexes) into the pest control strategies. This study produced the first high-quality chromosome-level for this pest using a combination of powerful approaches PacBio high fidelity (HiFi) long-reads and chromatin conformation capture (Hi-C) sequencing data. The final genome was highly contiguous with seven scaffolds (fragments of the genome) comprising 98.9% of the final assembly. The quality of the sequenced genome is comparable to a genome of a species model such as Drosophila melanogaster. We were also able to identify and characterize the sex chromosomes (X and Y), which have been a challenge to characterize due to the high levels of repetitive DNA, particularly elevated in the Y chromosome. This genome offers a new range of possibilities to find highly phylogenetically informative regions (i.e., useful for species identification) and new potential targets for genome editing (e.g., new phenotypic markers, and genes related to female viability and male fertility) that may be valuable to improve pest control strategies for this important agricultural pest.

Technical Abstract: The Mexican fruit fly, Anastrepha ludens, is a polyphagous true fruit fly considered one of the most serious insect pest to various economically relevant fruits, particularly citrus and mango, in Central and North America. Despite its agricultural relevance, a high-quality genome assembly has not been reported. Here, we generated and described a high-quality chromosome-level genome for the Mexican fruit fly using a combination of PacBio high fidelity (HiFi) long-reads and chromatin conformation capture (Hi-C) sequencing data. The final genome was assembled into 140 scaffolds with a total length of 821 Mbp (N50 = 131 Mbp), containing 98.9% complete single-copied of the 3,285 Benchmarking Universal Single-Copy Orthologs for Diptera. Chromosome-level assembly recovered seven scaffolds comprising 98.9% of the final assembly. We identified the sex chromosomes using three strategies: 1) visual inspection of Hi-C contact map, 2) synteny with Drosophila melanogaster, and 3) the difference in the average read depth of autosomal versus sex chromosomal scaffolds (AD-ratio approach). The X chromosome was found in one scaffold (~100 Mbp) and the Y chromosome was recovered in one large scaffold (4.2 Mbp) and 39 smaller scaffolds, totalizing 10.3 Mbp. A comparison of the sex chromosomes with autosomes revealed considerable differences in terms of TE and gene content. Moreover, we inferred orthologous genes between Anastrepha obliqua and A. ludens to calculate evolutionary rates. This analysis evidenced higher evolutionary rates (Ka and Ka/Ks) of X-linked genes compared to autosome-linked genes, consistent with the pattern expected for the faster-X effect. Our study has generated a high-quality chromone-level genome assembly and revealed new insights about sex chromosomes evolution in this group of fruit flies. In addition, this genome assembly provides a valuable resource that may be used to improve pest control strategies for this important agricultural pest.