Mitogenomic Comparison of the Mole Crickets Gryllotalpidae with the Phylogenetic Implications (Orthoptera: Ensifera)

SIMPLE SUMMARY: We sequenced the complete mitochondrial genomes (mitogenomes) of Gryllotalpa henana Cai & Niu, 1998 and the Chinese G. orientalis Burmeister, 1838 for the first time, and reconstructed the mitogenomic phylogeny of the infraorder Gryllidea. The results show that the two new mitogenomes are double-stranded circular molecules with a typical gene complement, gene arrangement and base composition, the same as those of other gryllotalpids and ancestral insects. Tandem repeats of the control region were discovered in Gryllotalpidae for the first time. Considering both the high nucleotide divergence and the elevated ratio of Ka/Ks, the genes nad2 and nad6 may be evaluated as potential markers for future phylogeny and species delimitation in Gryllotalpidae. The results of phylogenetic analyses provide supports for the mitogenomic and transcriptomic trees, but partially contradict those of the multilocus phylogenies. ABSTRACT: Owing to limited molecular data, the phylogenetic position of the family Gryllotalpidae is still controversial in the infraorder Gryllidea. Mitochondrial genome (mitogenome) plays a crucial role in reconstructing phylogenetic relationships and revealing the molecular evolution of insects. However, only four mitogenomes have been reported in Gryllotalpidae to date. Herein, we obtained the first mitogenomes of Gryllotalpa henana Cai & Niu, 1998 and the Chinese G. orientalis Burmeister, 1838, made a detailed comparison of all mitogenomes available in Gryllotalpidae and reconstructed the phylogeny of Gryllidea based on mitogenomes using Bayesian inference (BI) and maximum likelihood (ML) methods. The results show that the complete mitogenome sequences of G. henana (15,504 bp) and G. orientalis (15,497 bp) are conserved, both exhibiting the double-stranded circular structure, typical gene content and the ancestral insect gene arrangement. The complete mitogenome of G. henana exhibits the lowest average AT content ever detected in Gryllotalpidae, and even Gryllidea. The gene nad2 of both species has atypical initiation codon GTG. All tRNAs exhibit typical clover-leaf structure, except for trnS1 lacking the dihydrouridine (DHU) arm. A potential stem–loop structure, containing a (T)(n)(TC)(2)(T)(n) sequence, is detected in the control region of all gryllotalpids investigated and is likely related to the replication initiation of the minority strand. The phylogenetic analyses recover the six families of Gryllidea as Gryllotalpidae + (Myrmecophilidae + (Mogoplistidae + (Trigonidiidae + (Phalangopsidae + Gryllidae)))), similar to the trees based on transcriptomic and mitogenomic data. However, the trees are slightly different from the multilocus phylogenies, which show the sister-group relationship of Gryllotalpidae and Myrmecophilidae. The contradictions between mitogenomic and multilocus trees are briefly discussed.