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Host-jump drives rapid and recent ecological speciation of the emergent fungal pathogen Colletotrichum kahawae

Authors

  • DIOGO N. SILVA,

    1. CIFC/IICT—Centro de Investigação das Ferrugens do Cafeeiro/Instituto de Investigação Científica Tropical, Quinta do Marquês, 2784-505 Oeiras, Portugal
    2. Computational Biology and Population Genomics Group, Centro de Biologia Ambiental, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal
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  • PEDRO TALHINHAS,

    1. CIFC/IICT—Centro de Investigação das Ferrugens do Cafeeiro/Instituto de Investigação Científica Tropical, Quinta do Marquês, 2784-505 Oeiras, Portugal
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  • LEI CAI,

    1. State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, No.10, North 4th Ring Road West, Beijing 100190, China
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  • LUZOLO MANUEL,

    1. Instituto Nacional do Café de Angola, Luanda, Angola
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  • ELIJAH K. GICHURU,

    1. Coffee Research Foundation, P.O. Box 4, 00232 Ruiru, Kenya
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  • ANDREIA LOUREIRO,

    1. CIFC/IICT—Centro de Investigação das Ferrugens do Cafeeiro/Instituto de Investigação Científica Tropical, Quinta do Marquês, 2784-505 Oeiras, Portugal
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  • VÍTOR VÁRZEA,

    1. CIFC/IICT—Centro de Investigação das Ferrugens do Cafeeiro/Instituto de Investigação Científica Tropical, Quinta do Marquês, 2784-505 Oeiras, Portugal
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  • OCTÁVIO S. PAULO,

    1. Computational Biology and Population Genomics Group, Centro de Biologia Ambiental, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal
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  • DORA BATISTA

    1. CIFC/IICT—Centro de Investigação das Ferrugens do Cafeeiro/Instituto de Investigação Científica Tropical, Quinta do Marquês, 2784-505 Oeiras, Portugal
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Diogo N. Silva, Fax: 00351 214 544 689; E-mail: o.diogo.silva@gmail.com

Abstract

Ecological speciation through host-shift has been proposed as a major route for the appearance of novel fungal pathogens. The growing awareness of their negative impact on global economies and public health created an enormous interest in identifying the factors that are most likely to promote their emergence in nature. In this work, a combination of pathological, molecular and geographical data was used to investigate the recent emergence of the fungus Colletotrichum kahawae. C. kahawae emerged as a specialist pathogen causing coffee berry disease in Coffea arabica, owing to its unparalleled adaptation of infecting green coffee berries. Contrary to current hypotheses, our results suggest that a recent host-jump underlay the speciation of C. kahawae from a generalist group of fungi seemingly harmless to coffee berries. We posit that immigrant inviability and a predominantly asexual behaviour could have been instrumental in driving speciation by creating pleiotropic interactions between local adaptation and reproductive patterns. Moreover, we estimate that C. kahawae began its diversification at <2200 bp leaving a very short time frame since the divergence from its sibling lineage (c. 5600 bp), during which a severe drop in C. kahawae’s effective population size occurred. This further supports a scenario of recent introduction and subsequent adaptation to C. arabica. Phylogeographical data revealed low levels of genetic polymorphism but provided the first geographically consistent population structure of C. kahawae, inferring the Angolan population as the most ancestral and the East African populations as the most recently derived. Altogether, these results highlight the significant role of host specialization and asexuality in the emergence of fungal pathogens through ecological speciation.

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