Abstract
Microbes engage in numerous social behaviours that are critical for survival and reproduction, and that require individuals to act as a collective. Various mechanisms ensure that collectives are composed of related, cooperating cells, thus allowing for the evolution and stability of these traits, and for selection to favour traits beneficial to the collective. Since microbes are difficult to observe directly, sociality in natural populations can instead be investigated using evolutionary genetic signatures, as social loci can be evolutionary hotspots. The budding yeast has been studied for over a century, yet little is known about its social behaviour in nature. Flo11 is a highly regulated cell adhesin required for most laboratory social phenotypes; studies suggest it may function in cell recognition and its heterogeneous expression may be adaptive for collectives such as biofilms. We investigated this locus and found positive selection in the areas implicated in cell–cell interaction, suggesting selection for kin discrimination. We also found balancing selection at an upstream activation site, suggesting selection on the level of variegated gene expression. Our results suggest this model yeast is surprisingly social in natural environments and is probably engaging in various forms of sociality. By using genomic data, this research provides a glimpse of otherwise unobservable interactions.
Highlights
Microbes are capable of functioning as collectives to engage in social behaviours ranging from swarming and foraging to producing fruiting bodies and highly differentiated biofilms [1]
Social genes can be hotspots for evolution; they can be involved in a myriad of processes, including kin recognition, purging cheaters and modulating overall levels of sociality
We used patterns of genetic variation at this locus to determine whether there was any evidence of sociality in natural populations, and to our knowledge, performed the first evolutionary analysis of the FLO11
Summary
Microbes are capable of functioning as collectives to engage in social behaviours ranging from swarming and foraging to producing fruiting bodies and highly differentiated biofilms [1]. The highly repetitive middle domain of Flo11p pushes the extracellular domain away from the cell [21], and length variation has been associated with various social phenotypes [23] and yeast chronological ageing [24] These types of recognition proteins are found when discrimination among self/non-self is required. Our analysis uncovered the predicted pattern: positive selection in the regions of the gene responsible for cell–cell interactions, and a signature of balancing selection in a region previously shown to contribute to epigenetic silencing These results highlight the extent to which this important model organism is likely to be social in its natural environment, and further demonstrates the power of using evolutionary genetic signatures to infer microbial sociality. The data were analysed using an ANOVA approach in JMP v. 11.2.0
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