Comparative Analysis of Mitochondrial Genomes in Gryllidea (Insecta: Orthoptera): Implications for Adaptive Evolution in Ant-Loving Crickets

Author:

Sanno Ryuto1,Kataoka Kosuke2ORCID,Hayakawa Shota1,Ide Keigo134,Nguyen Chuong N56,Nguyen Thao P56,Le Binh T N7,Kim Oanh T P7,Mineta Katsuhiko8ORCID,Takeyama Haruko123910,Takeda Makio11,Sato Toshiyuki12,Suzuki Takeshi13,Yura Kei1314,Asahi Toru12910

Affiliation:

1. Graduate School of Advanced Science and Engineering, Waseda University, Tokyo, Japan

2. Comprehensive Research Organization, Waseda University, Tokyo, Japan

3. Computational Bio Big-Data Open Innovation Laboratory (CBBD-OIL), National Institute of Advanced Industrial Science and Technology, Tokyo, Japan

4. Department of Health Data Science Research, Healthy Aging Innovation Center, Tokyo Metropolitan Geriatric Medical Center, Tokyo, Japan

5. Applied Biotechnology for Crop Development Research Unit, School of Biotechnology, International University, Ho Chi Minh City, Vietnam

6. Vietnam National University, Ho Chi Minh City, Vietnam

7. Institute of Genome Research, Vietnam Academy of Science and Technology, Cau Giay, Hanoi, Vietnam

8. Computational Bioscience Research Center, King Abdullah University of Science and Technology, Thuwal, Kingdom of Saudi Arabia

9. Institute for Advanced Research of Biosystem Dynamics, Waseda Research Institute for Science and Engineering, Waseda University, Tokyo, Japan

10. Research Organization for Nano & Life Innovation, Waseda University, Tokyo, Japan

11. Department of Agrobioscience, Graduate School of Agricultural Science, Kobe University, Hyogo, Japan

12. Faculty of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Japan

13. Graduate School of Bio-Applications and Systems Engineering, Tokyo University of Agriculture and Technology, Japan

14. Graduate School of Humanities and Sciences, Ochanomizu University, Tokyo, Japan

Abstract

Abstract Species of infraorder Gryllidea, or crickets, are useful invertebrate models for studying developmental biology and neuroscience. They have also attracted attention as alternative protein sources for human food and animal feed. Mitochondrial genomic information on related invertebrates, such as katydids, and locusts, has recently become available in attempt to clarify the controversial classification schemes, although robust phylogenetic relationships with emphasis on crickets remain elusive. Here, we report newly sequenced complete mitochondrial genomes of crickets to study their phylogeny, genomic rearrangements, and adaptive evolution. First, we conducted de novo assembly of mitochondrial genomes from eight cricket species and annotated protein-coding genes and transfer and ribosomal RNAs using automatic annotations and manual curation. Next, by combining newly described protein-coding genes with public data of the complete Gryllidea genomes and gene annotations, we performed phylogenetic analysis and found gene order rearrangements in several branches. We further analyzed genetic signatures of selection in ant-loving crickets (Myrmecophilidae), which are small wingless crickets that inhabit ant nests. Three distinct approaches revealed two positively selected sites in the cox1 gene in these crickets. Protein 3D structural analyses suggested that these selected sites could influence the interaction of respiratory complex proteins, conferring benefits to ant-loving crickets with a unique ecological niche and morphology. These findings enhance our understanding of the genetic basis of cricket evolution without relying on estimates based on a limited number of molecular markers.

Publisher

Oxford University Press (OUP)

Subject

Genetics,Ecology, Evolution, Behavior and Systematics

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