Phylogenomic analysis provides diagnostic tools for the identification of Anastrepha fraterculus (Diptera: Tephritidae) species complex

Carlos Congrains; Julian R. Dupuis; Erick J. Rodriguez; Allen L. Norrbom; Gary Steck; Bruce Sutton; Norma Nolazco; Reinaldo A. de Brito; Scott M. Geib

doi:10.1111/eva.13589

Phylogenomic analysis provides diagnostic tools for the identification of Anastrepha fraterculus (Diptera: Tephritidae) species complex

Carlos Congrains, Julian R. Dupuis, Erick J. Rodriguez, Allen L. Norrbom, Gary Steck, Bruce Sutton, Norma Nolazco, Reinaldo A. de Brito, Scott M. Geib

Producción científica: Article › revisión exhaustiva

12 Citas (Scopus)

Resumen

Insect pests cause tremendous impact to agriculture worldwide. Species identification is crucial for implementing appropriate measures of pest control but can be challenging in closely related species. True fruit flies of the genus Anastrepha Schiner (Diptera: Tephritidae) include some of the most serious agricultural pests in the Americas, with the Anastrepha fraterculus (Wiedemann) complex being one of the most important due to its extreme polyphagy and wide distribution across most of the New World tropics and subtropics. The eight morphotypes described for this complex as well as other closely related species are classified in the fraterculus species group, whose evolutionary relationships are unresolved due to incomplete lineage sorting and introgression. We performed multifaceted phylogenomic approaches using thousands of genes to unravel the evolutionary relationships within the A. fraterculus complex to provide a baseline for molecular diagnosis of these pests. We used a methodology that accommodates variable sources of data (transcriptome, genome, and whole-genome shotgun sequencing) and developed a tool to align and filter orthologs, generating reliable datasets for phylogenetic studies. We inferred 3031 gene trees that displayed high levels of discordance. Nevertheless, the topologies of the inferred coalescent species trees were consistent across methods and datasets, except for one lineage in the A. fraterculus complex. Furthermore, network analysis indicated introgression across lineages in the fraterculus group. We present a robust phylogeny of the group that provides insights into the intricate patterns of evolution of the A. fraterculus complex supporting the hypothesis that this complex is an assemblage of closely related cryptic lineages that have evolved under interspecific gene flow. Despite this complex evolutionary scenario, our subsampling analysis revealed that a set of as few as 80 loci has a similar phylogenetic resolution as the genome-scale dataset, offering a foundation to develop more efficient diagnostic tools in this species group.

Idioma original	English
Páginas (desde-hasta)	1598-1618
Número de páginas	21
Publicación	Evolutionary Applications
Volumen	16
N.º	9
DOI	https://doi.org/10.1111/eva.13589
Estado	Published - sept 2023

Nota bibliográfica

Publisher Copyright:
© 2023 The Authors. Evolutionary Applications published by Evolutionary Applications. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.

Financiación

Funding for this project was provided by the United States Department of Agriculture (USDA) Plant Protection Act 7721 and the USDA Agricultural Research Service (ARS). These funds were managed as an interagency agreement between the USDA Animal and Plant Health Inspection Service (APHIS) and USDA–ARS and a cooperative agreement with the University of Hawaii Manoa College of Tropical Agriculture and Human Resources. Similarly, Anastrepha collections were made possible through cooperative agreements between USDA–APHIS and the Florida Department of Agriculture and Consumer Services. Advanced computing resources were provided through the USDA SCINet scientific computing infrastructure. Specimens were collected in Peru with permission of the Ministerio de Agricultura, Dirección de Gestión Forestal de Fauna Silvestre (Resolución Directoral 209-2013-MINAGRI-DGFFS/DGEFFS and Resolución de Dirección General No. 022-2015-SERFOR-DGGSPFFS). We thank the Florida Department of Agriculture and Consumer Services – Division of Plant Industry for its support of this work. RAB has been supported by grants # 2018/06611-5 (FAPESP, Brazil), PVE 056/13 (CAPES) and 313504/2017-2 (CNPq). RAB is a CNPq fellow. The USDA is an equal opportunity employer. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA. Funding for this project was provided by the United States Department of Agriculture (USDA) Plant Protection Act 7721 and the USDA Agricultural Research Service (ARS). These funds were managed as an interagency agreement between the USDA Animal and Plant Health Inspection Service (APHIS) and USDA–ARS and a cooperative agreement with the University of Hawaii Manoa College of Tropical Agriculture and Human Resources. Similarly, collections were made possible through cooperative agreements between USDA–APHIS and the Florida Department of Agriculture and Consumer Services. Advanced computing resources were provided through the USDA SCINet scientific computing infrastructure. Specimens were collected in Peru with permission of the Ministerio de Agricultura, Dirección de Gestión Forestal de Fauna Silvestre (Resolución Directoral 209‐2013‐MINAGRI‐DGFFS/DGEFFS and Resolución de Dirección General No. 022‐2015‐SERFOR‐DGGSPFFS). We thank the Florida Department of Agriculture and Consumer Services – Division of Plant Industry for its support of this work. RAB has been supported by grants # 2018/06611‐5 (FAPESP, Brazil), PVE 056/13 (CAPES) and 313504/2017‐2 (CNPq). RAB is a CNPq fellow. The USDA is an equal opportunity employer. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA. Anastrepha

Financiadores	Número del financiador
USDA SCINet scientific computing infrastructure	022-2015-SERFOR-DGGSPFFS
University of Hawaii Manoa College of Tropical Agriculture and Human Resources
U.S. Department of Agriculture
USDA-Agricultural Research Service	2018/06611‐5
USDA-Agricultural Research Service
Animal and Plant Health Inspection Service
Florida Department of Agriculture and Consumer Services
Fundação de Amparo à Pesquisa do Estado de São Paulo	PVE 056/13
Fundação de Amparo à Pesquisa do Estado de São Paulo
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior	313504/2017‐2
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Conselho Nacional de Desenvolvimento Científico e Tecnológico

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Genetics
General Agricultural and Biological Sciences

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10.1111/eva.13589

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title = "Phylogenomic analysis provides diagnostic tools for the identification of Anastrepha fraterculus (Diptera: Tephritidae) species complex",

abstract = "Insect pests cause tremendous impact to agriculture worldwide. Species identification is crucial for implementing appropriate measures of pest control but can be challenging in closely related species. True fruit flies of the genus Anastrepha Schiner (Diptera: Tephritidae) include some of the most serious agricultural pests in the Americas, with the Anastrepha fraterculus (Wiedemann) complex being one of the most important due to its extreme polyphagy and wide distribution across most of the New World tropics and subtropics. The eight morphotypes described for this complex as well as other closely related species are classified in the fraterculus species group, whose evolutionary relationships are unresolved due to incomplete lineage sorting and introgression. We performed multifaceted phylogenomic approaches using thousands of genes to unravel the evolutionary relationships within the A. fraterculus complex to provide a baseline for molecular diagnosis of these pests. We used a methodology that accommodates variable sources of data (transcriptome, genome, and whole-genome shotgun sequencing) and developed a tool to align and filter orthologs, generating reliable datasets for phylogenetic studies. We inferred 3031 gene trees that displayed high levels of discordance. Nevertheless, the topologies of the inferred coalescent species trees were consistent across methods and datasets, except for one lineage in the A. fraterculus complex. Furthermore, network analysis indicated introgression across lineages in the fraterculus group. We present a robust phylogeny of the group that provides insights into the intricate patterns of evolution of the A. fraterculus complex supporting the hypothesis that this complex is an assemblage of closely related cryptic lineages that have evolved under interspecific gene flow. Despite this complex evolutionary scenario, our subsampling analysis revealed that a set of as few as 80 loci has a similar phylogenetic resolution as the genome-scale dataset, offering a foundation to develop more efficient diagnostic tools in this species group.",

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note = "Publisher Copyright: {\textcopyright} 2023 The Authors. Evolutionary Applications published by Evolutionary Applications. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.",

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AU - Congrains, Carlos

AU - Dupuis, Julian R.

AU - Rodriguez, Erick J.

AU - Norrbom, Allen L.

AU - Steck, Gary

AU - Sutton, Bruce

AU - Nolazco, Norma

AU - de Brito, Reinaldo A.

AU - Geib, Scott M.

N1 - Publisher Copyright: © 2023 The Authors. Evolutionary Applications published by Evolutionary Applications. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.

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N2 - Insect pests cause tremendous impact to agriculture worldwide. Species identification is crucial for implementing appropriate measures of pest control but can be challenging in closely related species. True fruit flies of the genus Anastrepha Schiner (Diptera: Tephritidae) include some of the most serious agricultural pests in the Americas, with the Anastrepha fraterculus (Wiedemann) complex being one of the most important due to its extreme polyphagy and wide distribution across most of the New World tropics and subtropics. The eight morphotypes described for this complex as well as other closely related species are classified in the fraterculus species group, whose evolutionary relationships are unresolved due to incomplete lineage sorting and introgression. We performed multifaceted phylogenomic approaches using thousands of genes to unravel the evolutionary relationships within the A. fraterculus complex to provide a baseline for molecular diagnosis of these pests. We used a methodology that accommodates variable sources of data (transcriptome, genome, and whole-genome shotgun sequencing) and developed a tool to align and filter orthologs, generating reliable datasets for phylogenetic studies. We inferred 3031 gene trees that displayed high levels of discordance. Nevertheless, the topologies of the inferred coalescent species trees were consistent across methods and datasets, except for one lineage in the A. fraterculus complex. Furthermore, network analysis indicated introgression across lineages in the fraterculus group. We present a robust phylogeny of the group that provides insights into the intricate patterns of evolution of the A. fraterculus complex supporting the hypothesis that this complex is an assemblage of closely related cryptic lineages that have evolved under interspecific gene flow. Despite this complex evolutionary scenario, our subsampling analysis revealed that a set of as few as 80 loci has a similar phylogenetic resolution as the genome-scale dataset, offering a foundation to develop more efficient diagnostic tools in this species group.

AB - Insect pests cause tremendous impact to agriculture worldwide. Species identification is crucial for implementing appropriate measures of pest control but can be challenging in closely related species. True fruit flies of the genus Anastrepha Schiner (Diptera: Tephritidae) include some of the most serious agricultural pests in the Americas, with the Anastrepha fraterculus (Wiedemann) complex being one of the most important due to its extreme polyphagy and wide distribution across most of the New World tropics and subtropics. The eight morphotypes described for this complex as well as other closely related species are classified in the fraterculus species group, whose evolutionary relationships are unresolved due to incomplete lineage sorting and introgression. We performed multifaceted phylogenomic approaches using thousands of genes to unravel the evolutionary relationships within the A. fraterculus complex to provide a baseline for molecular diagnosis of these pests. We used a methodology that accommodates variable sources of data (transcriptome, genome, and whole-genome shotgun sequencing) and developed a tool to align and filter orthologs, generating reliable datasets for phylogenetic studies. We inferred 3031 gene trees that displayed high levels of discordance. Nevertheless, the topologies of the inferred coalescent species trees were consistent across methods and datasets, except for one lineage in the A. fraterculus complex. Furthermore, network analysis indicated introgression across lineages in the fraterculus group. We present a robust phylogeny of the group that provides insights into the intricate patterns of evolution of the A. fraterculus complex supporting the hypothesis that this complex is an assemblage of closely related cryptic lineages that have evolved under interspecific gene flow. Despite this complex evolutionary scenario, our subsampling analysis revealed that a set of as few as 80 loci has a similar phylogenetic resolution as the genome-scale dataset, offering a foundation to develop more efficient diagnostic tools in this species group.

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Phylogenomic analysis provides diagnostic tools for the identification of Anastrepha fraterculus (Diptera: Tephritidae) species complex

Resumen

Nota bibliográfica

Financiación

ASJC Scopus subject areas

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