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

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.

Species limits in Diaporthe: molecular re-assessment of D. citri, D. cytosporella, D. foeniculina and D. rudis

“…Several modern studies aimed at epitypification of important pathogens in Diaporthe provide clarification and knowledge of the phylogeny and species boundaries within the genus (Castlebury et al 2003, van Niekerk et al 2005, Rensburg et al 2006, Diogo et al 2010, Udayanga et al 2012b, Gomes et al 2013). Application of genealogical concordance and/or gsi in combination with epitypification can provide critical insights into speciation processes, ecology and host associations (Sakalidis et al 2011, Gazis et al 2011, Mejia et al 2011, Silva et al 2012, Walker et al 2012). …”

Insights into the genus Diaporthe: phylogenetic species delimitation in the D. eres species complex

“…DNA-lyase genes have not traditionally been used as molecular markers in fungi; however, the association with mating type genes of fungi is known in relation to their structure. The Apn2 region has recently been used in conflicting genera like Colletotrichum (Crouch and Tomaso-Peterson 2012;Silva et al 2012b;Doyle et al 2013;Sharma et al 2013) and the Apn2 and Apn2/MAT-IGS (intergenic spacer between 3' end of the DNA lyase and mating type locus MAT1-2) genetic markers recommended as a better marker in disentangling the C. gloeosporioides species complex (Silva et al 2012a, b). Mating type genes of Diaporthe were amplified in several previous studies and utilised in phylogenetic analyses (Santos et al 2010(Santos et al , 2011.…”

Evolutionary history and variation in host range of three Stagonosporopsis species causing gummy stem blight of cucurbits

“…Thus, fungal pathogens can undergo speciation in geologically short time frames, particularly when driven by natural selection imposed by host specialization (Jones et al 2008;Stukenbrock & McDonald 2008;Giraud et al 2010). Host specialization to a new plant host through plant domestication was demonstrated by Silva et al (2012), who showed that a fungal pathogen of coffee, Colletrotrichum kahawae, diverged from its sibling species around 5600 YBP and underwent a population bottleneck upon specialization to coffee until approximately 2200 YBP. Specialization to coffee drove speciation of the coffee fungus from its ancestor that was not a pathogen of coffee.…”

“…Host-plant domestication is considered to be one type of force driving divergence and speciation of numerous plant pathogens (Couch et al 2005;Stukenbrock et al 2007;Frenkel et al 2009;Gladieux et al 2010;Silva et al 2012). Domestication and cultivation of crops have been documented to not only drive divergence and speciation in the crop species but can influence pathogens associated with the domesticated crop leading to the formation of species complexes (Couch et al 2005;Stukenbrock et al 2007).…”