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Mitochondrial genomes are widely used in insect taxonomy and phylogenetics, but their signals may conflict with morphology and nuclear genomic evidence because the mitochondrial genome represents a single maternally inherited locus. Here, we assembled complete mitochondrial genomes of four pygmy grasshoppers, Zhengitettix transpicula, Formosatettix sp., Gibbotettix parvipulvillus, and Bolivaritettix sp., using PacBio HiFi reads. The four mitogenomes ranged from 15,152 to 17,976 bp and contained the typical 37 mitochondrial genes. Mitochondrial phylogenies inferred by maximum likelihood and Bayesian methods were topologically identical and recovered several well-supported tetrigid relationships, including a close relationship between Formosatettix sp. and Bolivaritettix sp. However, Z. transpicula was unexpectedly placed near Macromotettixoides rather than close to other Zhengitettix representatives. In contrast, a morphology-based tree recovered Z. transpicula with Z. triangularis, and comparison with a published nuclear single-copy ortholog tree based on 1962 loci supported a non-mitochondrial placement of Zhengitettix inconsistent with the anomalous mitochondrial position of Z. transpicula. Independent assembly from the original HiFi reads, read-depth inspection, protein-coding gene checks, and nuclear-genome screening for NUMT-like sequences supported the authenticity of the assembled Z. transpicula mitogenome. These results document mito–nuclear and cyto-morphological discordance in Tetrigidae and highlight the need for integrative interpretation of mitochondrial phylogenies in taxonomically complex insect groups. Full article

The pygmy grasshopper, Zhengitettix transpicula, is a Chinese endemic species with an exceedingly limited distribution and fragile population structure, rendering it vulnerable to extinction. We present a high-continuity, chromosome-scale reference genome assembly to elucidate this species’ distinctive biology and inform conservation. Employing an integrated sequencing approach, we achieved a 970.40 Mb assembly with 96.32% coverage across seven pseudo-chromosomes and impressive continuity (N50 > 220 Mb). Genome annotation achieves identification with 99.2% BUSCO completeness, supporting quality. Comparative analyses with 14 genomes from Orthoptera-facilitated phylogenomics and revealed 549 significantly expanded gene families in Z. transpicula associated with metabolism, stress response, and development. However, genomic analysis exposed remarkably low heterozygosity (0.02%), implying a severe genetic bottleneck from small, fragmented populations, characteristic of species vulnerable to extinction from environmental disruptions. Elucidating the genetic basis of population dynamics and specialization provides an imperative guideline for habitat conservation and restoration of this rare organism. Moreover, divergent evolution analysis of the CYP305m2 gene regulating locust aggregation highlighted potential structural and hence functional variations between Acrididae and Tetrigidae. Our chromosomal genomic characterization of Z. transpicula advances Orthopteran resources, establishing a framework for evolutionary developmental explorations and applied conservation genomics, reversing the trajectory of this unique grasshopper lineage towards oblivion. Full article