Interspecific gene flow obscures phylogenetic relationships in an important insect pest species complex

Michael San Jose, Camiel Doorenweerd, Scott Geib, Norman Barr, Julian R. Dupuis, Luc Leblanc, Angela Kauwe, Kimberley Y. Morris, Daniel Rubinoff

Research output: Contribution to journalArticlepeer-review

15 Scopus citations

Abstract

As genomic data proliferates, the prevalence of post-speciation gene flow is making species boundaries and relationships increasingly ambiguous. Although current approaches inferring fully bifurcating phylogenies based on concatenated datasets provide simple and robust answers to many species relationships, they may be inaccurate because the models ignore inter-specific gene flow and incomplete lineage sorting. To examine the potential error resulting from ignoring gene flow, we generated both a RAD-seq and a 500 protein-coding loci highly multiplexed amplicon (HiMAP) dataset for a monophyletic group of 12 species defined as the Bactrocera dorsalis sensu lato clade. With some of the world's worst agricultural pests, the taxonomy of the B. dorsalis s.l. clade is important for trade and quarantines. However, taxonomic confusion confounds resolution due to intra- and interspecific phenotypic variation and convergence, mitochondrial introgression across half of the species, and viable hybrids. We compared the topological convergence of our datasets using concatenated phylogenetic and various multispecies coalescent approaches, some of which account for gene flow. All analyses agreed on species delimitation, but there was incongruence between species relationships. Under concatenation, both datasets suggest identical species relationships with mostly high statistical support. However, multispecies coalescent and multispecies network approaches suggest markedly different hypotheses and detected significant gene flow. We suggest that the network approaches are likely more accurate because gene flow violates the assumptions of the concatenated phylogenetic analyses, but the data-reductive requirements of network approaches resulted in reduced statistical support and could not unambiguously resolve gene flow directions. Our study highlights the importance of testing for gene flow, particularly with phylogenomic datasets, even when concatenated approaches receive high statistical support.

Original languageEnglish
Article number107892
JournalMolecular Phylogenetics and Evolution
Volume188
DOIs
StatePublished - Nov 2023

Bibliographical note

Publisher Copyright:
© 2023 Elsevier Inc.

Funding

This project was supported by the United States Department of Agriculture (USDA) Plant Protection Act 7721. These funds were managed as interagency or cooperative agreements between USDA Animal and Plant Health Inspection Service and USDA-ARS (8130–0893-IA), and the University of Hawaii's College of Tropical Agriculture and Human Resources (8130–0565-CA). This material was made possible, in part, by a Cooperative Agreement from the United States Department of Agriculture's Animal and Plant Health Inspection Service (APHIS). It may not necessarily express APHIS' views. Additional funding was provided by the USDA Cooperative State Research, Education and Extension (CSREES) project HAW00942-H administered by the College of Tropical Agriculture and Human Resources, University of Hawaii. We greatly appreciate the help of Chi-Yeh Chien (Thai Royal Project Foundation), Thongsavanh Taipangnavong (United Nations Food and Agriculture Organization Insect pest management Laos), Vornthalom Chanthavong (United Nations Food and Agriculture Organization Insect pest management Laos), Lira Chea (United Nations Food and Agriculture Organization Insect pest management Cambodia), Ajay Markanday (United Nations Food and Agriculture Organization Insect pest management Cambodia), Johannes Ketelaar (United Nations Food and Agriculture Organization Insect pest management - Regional Office for Asia and the Pacific), Prabhat Kumar (Asian Institute of Technology), Po-Yung Lai (University of Hawaii Manoa CTAHR), Hong Thai Pham (Vietnam National Museum of Nature), Yuchi Lin, Chia-lung Huang and Yu-Feng Tsu (National Taiwan Normal University), U.G.A.I. Sirisena (Rajarata University of Sri Lanka), M. Aftab Hossain, and Shakil Ahmed Khan (Bangladesh Atomic Energy Commission) for help with permits and logistics during our fieldwork. We thank A. Ota, A. Y. Kawahara, B. Bharndari, D. Haymer, E. Fiegalan, E. J. Rodriguez, F. Huda, H. Y. Huang, J. Niogret, J.B. Reil, K. Badji, K.-H. Wang, R. Messing, R. Putoa, S. Ouedraogo, S. Tam, T. Stark, N. Pierce, T. Xian, U. Freitas, W. P. Haines and Y. Xia for contributing specimens to the UHIM collections that we could use for this project. We thank the Sabah Biodiversity Centre for providing collection permits (ref. JKM/MBS.1000-2/3 JLD.3 (88)) and A. Chung and A. Mariani-Mustapeng for their support with collecting in Sabah, Malaysia. We greatly appreciate help from Daniel Nitta with the molecular wet-lab work and the Cornell Institute of Biotechnology for the initial GBS optimization, library preparation and sequencing. Scientific illustrations of the flies were created by Cody Anderson Studios. The technical support and advanced computing resources from University of Hawaii Information Technology Services – Cyberinfrastructure and the USDA SCINet scientific computing infrastructure are gratefully acknowledged. The USDA is an equal opportunity/affirmative action employer and all agency services are available without discrimination. 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.

FundersFunder number
Ajay Markanday
College of Tropical Agriculture and Human Resources
Cornell Institute of Biotechnology
Lira Chea
Shakil Ahmed Khan
Thongsavanh Taipangnavong
UHIM
USDA Cooperative State Research, Education and Extension
United Nations Food and Agriculture Organization Insect
United Nations Food and Agriculture Organization Insect
United Nations Food and Agriculture Organization Insect pest management - Regional Office for Asia
United Nations Food and Agriculture Organization Insect pest management Cambodia
Vornthalom Chanthavong
U.S. Department of Agriculture
Cooperative State Research, Education, and Extension Service
Hawai'i Pacific University
Animal and Plant Health Inspection Service
Asian Institute of Technology
National Taiwan Normal University
Rajarata University of Sri Lanka
Sabah Biodiversity CentreJKM/MBS.1000-2/3 JLD.3 (88)
Sabah Biodiversity Centre

    Keywords

    • Amplicons
    • Gene Flow
    • Multispecies Coalescent
    • Multispecies Network
    • Phylogenomics
    • RAD-seq

    ASJC Scopus subject areas

    • Ecology, Evolution, Behavior and Systematics
    • Molecular Biology
    • Genetics

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