Genetic structure and symbiotic profile of worldwide natural populations of the Mediterranean fruit fly, Ceratitis capitata

Abstract Background The Mediterranean fruit fly, Ceratitis capitata, is a cosmopolitan agricultural pest of worldwide economic importance and a model for the development of the Sterile Insect Technique (SIT) for fruit flies of the Tephritidae family (Diptera). SIT relies on the effective mating of l...

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Main Authors: Katerina Nikolouli, Antonios A. Augustinos, Panagiota Stathopoulou, Elias Asimakis, Anastasios Mintzas, Kostas Bourtzis, George Tsiamis
Format: Article
Language:English
Published: BMC 2020-12-01
Series:BMC Genetics
Subjects:
Online Access:https://doi.org/10.1186/s12863-020-00946-z
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author Katerina Nikolouli
Antonios A. Augustinos
Panagiota Stathopoulou
Elias Asimakis
Anastasios Mintzas
Kostas Bourtzis
George Tsiamis
author_facet Katerina Nikolouli
Antonios A. Augustinos
Panagiota Stathopoulou
Elias Asimakis
Anastasios Mintzas
Kostas Bourtzis
George Tsiamis
author_sort Katerina Nikolouli
collection DOAJ
description Abstract Background The Mediterranean fruit fly, Ceratitis capitata, is a cosmopolitan agricultural pest of worldwide economic importance and a model for the development of the Sterile Insect Technique (SIT) for fruit flies of the Tephritidae family (Diptera). SIT relies on the effective mating of laboratory-reared strains and natural populations, and therefore requires an efficient mass-rearing system that will allow for the production of high-quality males. Adaptation of wild flies to an artificial laboratory environment can be accompanied by negative effects on several life history traits through changes in their genetic diversity and symbiotic communities. Such changes may lead to reduced biological quality and mating competitiveness in respect to the wild populations. Profiling wild populations can help understand, and maybe reverse, deleterious effects accompanying laboratory domestication thus providing insects that can efficiently and effectively support SIT application. Results In the present study, we analyzed both the genetic structure and gut symbiotic communities of natural medfly populations of worldwide distribution, including Europe, Africa, Australia, and the Americas. The genetic structure of 408 individuals from 15 distinct populations was analyzed with a set of commonly used microsatellite markers. The symbiotic communities of a subset of 265 individuals from 11 populations were analyzed using the 16S rRNA gene-based amplicon sequencing of single individuals (adults). Genetic differentiation was detected among geographically distant populations while adults originated from neighboring areas were genetically closer. Alpha and beta diversity of bacterial communities pointed to an overall reduced symbiotic diversity and the influence of the geographic location on the bacterial profile. Conclusions Our analysis revealed differences both in the genetic profile and the structure of gut symbiotic communities of medfly natural populations. The genetic analysis expanded our knowledge to populations not analyzed before and our results were in accordance with the existing scenarios regarding this species expansion and colonization pathways. At the same time, the bacterial communities from different natural medfly populations have been characterized, thus broadening our knowledge on the microbiota of the species across its range. Genetic and symbiotic differences between natural and laboratory populations must be considered when designing AW-IPM approaches with a SIT component, since they may impact mating compatibility and mating competitiveness of the laboratory-reared males. In parallel, enrichment from wild populations and/or symbiotic supplementation could increase rearing productivity, biological quality, and mating competitiveness of SIT-important laboratory strains.
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spelling doaj.art-a1d47ae1183d426196cc72789bea7da02022-12-22T02:22:47ZengBMCBMC Genetics1471-21562020-12-0121S211310.1186/s12863-020-00946-zGenetic structure and symbiotic profile of worldwide natural populations of the Mediterranean fruit fly, Ceratitis capitataKaterina Nikolouli0Antonios A. Augustinos1Panagiota Stathopoulou2Elias Asimakis3Anastasios Mintzas4Kostas Bourtzis5George Tsiamis6Insect Pest Control Laboratory, Joint FAO/IAEA Programme of Nuclear Techniques in Food and AgricultureInsect Pest Control Laboratory, Joint FAO/IAEA Programme of Nuclear Techniques in Food and AgricultureDepartment of Environmental Engineering, University of PatrasDepartment of Environmental Engineering, University of PatrasDepartment of Biology, University of PatrasInsect Pest Control Laboratory, Joint FAO/IAEA Programme of Nuclear Techniques in Food and AgricultureDepartment of Environmental Engineering, University of PatrasAbstract Background The Mediterranean fruit fly, Ceratitis capitata, is a cosmopolitan agricultural pest of worldwide economic importance and a model for the development of the Sterile Insect Technique (SIT) for fruit flies of the Tephritidae family (Diptera). SIT relies on the effective mating of laboratory-reared strains and natural populations, and therefore requires an efficient mass-rearing system that will allow for the production of high-quality males. Adaptation of wild flies to an artificial laboratory environment can be accompanied by negative effects on several life history traits through changes in their genetic diversity and symbiotic communities. Such changes may lead to reduced biological quality and mating competitiveness in respect to the wild populations. Profiling wild populations can help understand, and maybe reverse, deleterious effects accompanying laboratory domestication thus providing insects that can efficiently and effectively support SIT application. Results In the present study, we analyzed both the genetic structure and gut symbiotic communities of natural medfly populations of worldwide distribution, including Europe, Africa, Australia, and the Americas. The genetic structure of 408 individuals from 15 distinct populations was analyzed with a set of commonly used microsatellite markers. The symbiotic communities of a subset of 265 individuals from 11 populations were analyzed using the 16S rRNA gene-based amplicon sequencing of single individuals (adults). Genetic differentiation was detected among geographically distant populations while adults originated from neighboring areas were genetically closer. Alpha and beta diversity of bacterial communities pointed to an overall reduced symbiotic diversity and the influence of the geographic location on the bacterial profile. Conclusions Our analysis revealed differences both in the genetic profile and the structure of gut symbiotic communities of medfly natural populations. The genetic analysis expanded our knowledge to populations not analyzed before and our results were in accordance with the existing scenarios regarding this species expansion and colonization pathways. At the same time, the bacterial communities from different natural medfly populations have been characterized, thus broadening our knowledge on the microbiota of the species across its range. Genetic and symbiotic differences between natural and laboratory populations must be considered when designing AW-IPM approaches with a SIT component, since they may impact mating compatibility and mating competitiveness of the laboratory-reared males. In parallel, enrichment from wild populations and/or symbiotic supplementation could increase rearing productivity, biological quality, and mating competitiveness of SIT-important laboratory strains.https://doi.org/10.1186/s12863-020-00946-zMedflyMicrobiotaBacterial communitiesMicrosatellites16S rRNAIllumina sequencing
spellingShingle Katerina Nikolouli
Antonios A. Augustinos
Panagiota Stathopoulou
Elias Asimakis
Anastasios Mintzas
Kostas Bourtzis
George Tsiamis
Genetic structure and symbiotic profile of worldwide natural populations of the Mediterranean fruit fly, Ceratitis capitata
BMC Genetics
Medfly
Microbiota
Bacterial communities
Microsatellites
16S rRNA
Illumina sequencing
title Genetic structure and symbiotic profile of worldwide natural populations of the Mediterranean fruit fly, Ceratitis capitata
title_full Genetic structure and symbiotic profile of worldwide natural populations of the Mediterranean fruit fly, Ceratitis capitata
title_fullStr Genetic structure and symbiotic profile of worldwide natural populations of the Mediterranean fruit fly, Ceratitis capitata
title_full_unstemmed Genetic structure and symbiotic profile of worldwide natural populations of the Mediterranean fruit fly, Ceratitis capitata
title_short Genetic structure and symbiotic profile of worldwide natural populations of the Mediterranean fruit fly, Ceratitis capitata
title_sort genetic structure and symbiotic profile of worldwide natural populations of the mediterranean fruit fly ceratitis capitata
topic Medfly
Microbiota
Bacterial communities
Microsatellites
16S rRNA
Illumina sequencing
url https://doi.org/10.1186/s12863-020-00946-z
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