Timing of evolutionary innovation: scenarios of evolutionary diversification in a species-rich fungal clade, Boletales.

ABSTRACT

Acquisition of mutualistic symbiosis could provide hosts and/or symbionts with novel ecological opportunities for evolutionary diversification. Such a mechanism is one of the major components of coevolutionary diversification. However, whether the origin of mycorrhizal symbiosis promotes diversification in fungi still requires clarification. Here, we aimed to reveal evolutionary diversification in a clade comprising ectomycorrhizal (ECM) fungi. Based on a phylogenic tree inferred from the sequences of 87 single-copy genes, we reconstructed the origins of ECM symbiosis in a species-rich basidiomycetous order, Boletales. High-resolution phylogeny of Boletales revealed that ECM symbiosis independently evolved from non-ECM states at least four times in the group. Among them, only the second most recent event, occurring in the clade of Boletaceae, was inferred to involve an almost synchronous rapid diversification and rapid transition from non-ECM to ECM symbiosis. Our results contradict the hypothesis of evolutionary priority effect, which postulates the greatest ecological opportunities in the oldest lineages. Therefore, the novel resources that had not been pre-empted by the old ECM fungal lineages - supposedly the coevolving angiosperm hosts - could be available for the young ECM fungal lineages, which resulted in evolutionary diversification occurring only in the young ECM fungal lineages.