Phylogenetic analysis of the angiosperm-floricolous insect–yeast association: Have yeast and angiosperm lineages co-diversified?

Abstract

a b s t r a c tMetschnikowia (Saccharomycetales, Metschnikowiaceae/ Metschnikowia clade) is an ascomycetous yeast genus whose species are associated mostly with angiosperms and their insect pollinators over all continents. The wide distribution of the genus, its association with angiosperm flowers, and the fact that it includes some of the best-studied yeasts in terms of biogeography and ecology makeMetschnikowia an excellent group to investigate a possible co-radiation with angiosperm lineages. We performed phylogenetic analyses implementing Bayesian inference and likelihood methods, using a concatenated matrix (%2.6 Kbp) of nuclear DNA ( ACT1, 1st and 2nd codon positions of EF2, Mcm7, and RPB2) sequences. We included 77 species representing approximately 90% of the species in the family. Bayesian and parsimony methods were used to perform ancestral character reconstructions within Metschnikowia in three key morphological characters. Patterns of evolution of yeast habitats and divergence times were explored in the Metschnikowia clade lineages with the purpose of inferring the time of origin of angiosperm-associated habitats within Metschnikowiaceae. This paper presents the first phylogenetic hypothesis to include nearly all known species in the family. The polyphyletic nature of Clavispora was confirmed and Metschnikowia species (and their anamorphs) were shown to form two groups: one that includes mostly floricolous, insect-associated species distributed in mostly tropical areas (the large-spored Metschnikowia clade and relatives) and another that comprises more heterogeneous species in terms of habitat and geographical distribution. Reconstruction of character evolution suggests that sexual characters (ascospore length, number of ascospores, and ascus formation) evolved multiple times within Metschnikowia. Complex and dynamic habitat transitions seem to have punctuated the course of evolution of the Metschnikowiaceae with repeated and independent origins of angiosperm-associated habitats. The origin of the family is placed in the Late Cretaceous (71.7 Ma) with most extant species arising from the Early Eocene. Therefore, the Metschnikowiaceae likely radiated long after the Mid-Cretaceous radiations of angiosperms and their diversification seems to be driven by repeated radiation on a pre-existing diverse resource.

The impact of yeast presence in nectar on bumble bee behavior and fitness

“…Unlike many transient, opportunistic interactions between animals and microorganisms, the symbiosis between nectar-inhabiting yeasts and insects shows features that define it as biologically successful, persistent in an evolutionary context (Lachance et al 2003, Guzm an et al 2013), widespread (Brysch-Herzberg 2004, Herrera et al 2009a, b, Pozo et al 2012, Mittelbach and Vannette 2017, and having wide ecological implications. However, while it is clear that insects actively disperse yeasts and thus increase their mobility, little is known about how yeasts affect the fitness of flower-visiting insects.…”

Genetic basis of priority effects: insights from nectar yeast

“…To begin to test this hypothesis, we conducted competition experiments against one of the closest known relatives of M. reukaufii, Candida rancensis (Metschnikowiaceae) [40], commonly found in monkeyflower nectar [41]. Candida rancensis is one of the strongest competitors of M. reukaufii, likely due to resource-use overlap [10], but it is severely disadvantaged when M. reukaufii colonizes the nectar first [10].…”

Species coexistence in simple microbial communities: unravelling the phenotypic landscape of co‐occurring Metschnikowia species in floral nectar

“…The Metschnikowiaceae clade is thought to have originated in the Late Cretaceous (71.7 Ma) and its evolution appears to have been driven by complex and dynamic habitat transitions, with repeated and independent origins of angiosperm-associated habitats (Guzmán et al, 2013). Most species are terrestrial and form diverse mutualistic symbioses with a preponderance of associations with angiosperms and their associated insects (Lachance, 2011a,b).…”