Novel insight into lepidopteran phylogenetics from the mitochondrial genome of the apple fruit moth of the family Argyresthiidae

Abstract Background The order Lepidoptera has an abundance of species, including both agriculturally beneficial and detrimental insects. Molecular data has been used to investigate the phylogenetic relationships of major subdivisions in Lepidoptera, which has enhanced our understanding of the evolut...

Full description

Bibliographic Details
Main Authors: Abdelhameed Elameen, Simo N. Maduna, Melissa H. Mageroy, André van Eerde, Geir Knudsen, Snorre B. Hagen, Hans Geir Eiken
Format: Article
Language:English
Published: BMC 2024-01-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-023-09905-1
_version_ 1797363573323726848
author Abdelhameed Elameen
Simo N. Maduna
Melissa H. Mageroy
André van Eerde
Geir Knudsen
Snorre B. Hagen
Hans Geir Eiken
author_facet Abdelhameed Elameen
Simo N. Maduna
Melissa H. Mageroy
André van Eerde
Geir Knudsen
Snorre B. Hagen
Hans Geir Eiken
author_sort Abdelhameed Elameen
collection DOAJ
description Abstract Background The order Lepidoptera has an abundance of species, including both agriculturally beneficial and detrimental insects. Molecular data has been used to investigate the phylogenetic relationships of major subdivisions in Lepidoptera, which has enhanced our understanding of the evolutionary relationships at the family and superfamily levels. However, the phylogenetic placement of many superfamilies and/or families in this order is still unknown. In this study, we determine the systematic status of the family Argyresthiidae within Lepidoptera and explore its phylogenetic affinities and implications for the evolution of the order. We describe the first mitochondrial (mt) genome from a member of Argyresthiidae, the apple fruit moth Argyresthia conjugella. The insect is an important pest on apples in Fennoscandia, as it switches hosts when the main host fails to produce crops. Results The mt genome of A. conjugella contains 16,044 bp and encodes all 37 genes commonly found in insect mt genomes, including 13 protein-coding genes (PCGs), two ribosomal RNAs, 22 transfer RNAs, and a large control region (1101 bp). The nucleotide composition was extremely AT-rich (82%). All detected PCGs (13) began with an ATN codon and terminated with a TAA stop codon, except the start codon in cox1 is ATT. All 22 tRNAs had cloverleaf secondary structures, except trnS1, where one of the dihydrouridine (DHU) arms is missing, reflecting potential differences in gene expression. When compared to the mt genomes of 507 other Lepidoptera representing 18 superfamilies and 42 families, phylogenomic analyses found that A. conjugella had the closest relationship with the Plutellidae family (Yponomeutoidea-super family). We also detected a sister relationship between Yponomeutoidea and the superfamily Tineidae. Conclusions Our results underline the potential importance of mt genomes in comparative genomic analyses of Lepidoptera species and provide valuable evolutionary insight across the tree of Lepidoptera species.
first_indexed 2024-03-08T16:23:12Z
format Article
id doaj.art-3d646b6e10594c95ad984d96fab2c5b9
institution Directory Open Access Journal
issn 1471-2164
language English
last_indexed 2024-03-08T16:23:12Z
publishDate 2024-01-01
publisher BMC
record_format Article
series BMC Genomics
spelling doaj.art-3d646b6e10594c95ad984d96fab2c5b92024-01-07T12:12:20ZengBMCBMC Genomics1471-21642024-01-0125112010.1186/s12864-023-09905-1Novel insight into lepidopteran phylogenetics from the mitochondrial genome of the apple fruit moth of the family ArgyresthiidaeAbdelhameed Elameen0Simo N. Maduna1Melissa H. Mageroy2André van Eerde3Geir Knudsen4Snorre B. Hagen5Hans Geir Eiken6Division of Biotechnology and Plant Health, NIBIO, Norwegian Institute of Bioeconomy ResearchDivision of Environment and Natural Resources, NIBIO, Norwegian Institute of Bioeconomy ResearchDivision of Biotechnology and Plant Health, NIBIO, Norwegian Institute of Bioeconomy ResearchDivision of Biotechnology and Plant Health, NIBIO, Norwegian Institute of Bioeconomy ResearchDivision of Biotechnology and Plant Health, NIBIO, Norwegian Institute of Bioeconomy ResearchDivision of Environment and Natural Resources, NIBIO, Norwegian Institute of Bioeconomy ResearchDivision of Environment and Natural Resources, NIBIO, Norwegian Institute of Bioeconomy ResearchAbstract Background The order Lepidoptera has an abundance of species, including both agriculturally beneficial and detrimental insects. Molecular data has been used to investigate the phylogenetic relationships of major subdivisions in Lepidoptera, which has enhanced our understanding of the evolutionary relationships at the family and superfamily levels. However, the phylogenetic placement of many superfamilies and/or families in this order is still unknown. In this study, we determine the systematic status of the family Argyresthiidae within Lepidoptera and explore its phylogenetic affinities and implications for the evolution of the order. We describe the first mitochondrial (mt) genome from a member of Argyresthiidae, the apple fruit moth Argyresthia conjugella. The insect is an important pest on apples in Fennoscandia, as it switches hosts when the main host fails to produce crops. Results The mt genome of A. conjugella contains 16,044 bp and encodes all 37 genes commonly found in insect mt genomes, including 13 protein-coding genes (PCGs), two ribosomal RNAs, 22 transfer RNAs, and a large control region (1101 bp). The nucleotide composition was extremely AT-rich (82%). All detected PCGs (13) began with an ATN codon and terminated with a TAA stop codon, except the start codon in cox1 is ATT. All 22 tRNAs had cloverleaf secondary structures, except trnS1, where one of the dihydrouridine (DHU) arms is missing, reflecting potential differences in gene expression. When compared to the mt genomes of 507 other Lepidoptera representing 18 superfamilies and 42 families, phylogenomic analyses found that A. conjugella had the closest relationship with the Plutellidae family (Yponomeutoidea-super family). We also detected a sister relationship between Yponomeutoidea and the superfamily Tineidae. Conclusions Our results underline the potential importance of mt genomes in comparative genomic analyses of Lepidoptera species and provide valuable evolutionary insight across the tree of Lepidoptera species.https://doi.org/10.1186/s12864-023-09905-1Argyresthia conjugellaIllumina HiSeqLepidopteraMitochondrial genomeYponomeutoidea
spellingShingle Abdelhameed Elameen
Simo N. Maduna
Melissa H. Mageroy
André van Eerde
Geir Knudsen
Snorre B. Hagen
Hans Geir Eiken
Novel insight into lepidopteran phylogenetics from the mitochondrial genome of the apple fruit moth of the family Argyresthiidae
BMC Genomics
Argyresthia conjugella
Illumina HiSeq
Lepidoptera
Mitochondrial genome
Yponomeutoidea
title Novel insight into lepidopteran phylogenetics from the mitochondrial genome of the apple fruit moth of the family Argyresthiidae
title_full Novel insight into lepidopteran phylogenetics from the mitochondrial genome of the apple fruit moth of the family Argyresthiidae
title_fullStr Novel insight into lepidopteran phylogenetics from the mitochondrial genome of the apple fruit moth of the family Argyresthiidae
title_full_unstemmed Novel insight into lepidopteran phylogenetics from the mitochondrial genome of the apple fruit moth of the family Argyresthiidae
title_short Novel insight into lepidopteran phylogenetics from the mitochondrial genome of the apple fruit moth of the family Argyresthiidae
title_sort novel insight into lepidopteran phylogenetics from the mitochondrial genome of the apple fruit moth of the family argyresthiidae
topic Argyresthia conjugella
Illumina HiSeq
Lepidoptera
Mitochondrial genome
Yponomeutoidea
url https://doi.org/10.1186/s12864-023-09905-1
work_keys_str_mv AT abdelhameedelameen novelinsightintolepidopteranphylogeneticsfromthemitochondrialgenomeoftheapplefruitmothofthefamilyargyresthiidae
AT simonmaduna novelinsightintolepidopteranphylogeneticsfromthemitochondrialgenomeoftheapplefruitmothofthefamilyargyresthiidae
AT melissahmageroy novelinsightintolepidopteranphylogeneticsfromthemitochondrialgenomeoftheapplefruitmothofthefamilyargyresthiidae
AT andrevaneerde novelinsightintolepidopteranphylogeneticsfromthemitochondrialgenomeoftheapplefruitmothofthefamilyargyresthiidae
AT geirknudsen novelinsightintolepidopteranphylogeneticsfromthemitochondrialgenomeoftheapplefruitmothofthefamilyargyresthiidae
AT snorrebhagen novelinsightintolepidopteranphylogeneticsfromthemitochondrialgenomeoftheapplefruitmothofthefamilyargyresthiidae
AT hansgeireiken novelinsightintolepidopteranphylogeneticsfromthemitochondrialgenomeoftheapplefruitmothofthefamilyargyresthiidae