The Case of the Missing Ancient Fungal Polyploids

Campbell, Matthew A.; Ganley, Austen R. D.; Gabaldón Estevan, Juan Antonio, 1973-; Cox, Murray P.

doi:http://dx.doi.org/10.5061/dryad.75dg8

The Case of the Missing Ancient Fungal Polyploids

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Campbell MA, Ganley ARD, Gabaldón Estevan JA, Cox MP. The Case of the Missing Ancient Fungal Polyploids. American Naturalist. 2016; 188(6): 602-614. DOI: 10.5061/dryad.75dg8

Abstract

Polyploidy—the increase in the number of whole chromosome sets—is an important evolutionary force in eukaryotes. Polyploidy is well recognized throughout the evolutionary history of plants and animals, where several ancient events have been hypothesized to be drivers of major evolutionary radiations. However, fungi provide a striking contrast: while numerous recent polyploids have been documented, ancient fungal polyploidy is virtually unknown. We present a survey of known fungal polyploids that confirms the absence of ancient fungal polyploidy events. Three hypotheses may explain this finding. First, ancient fungal polyploids are indeed rare, with unique aspects of fungal biology providing similar benefits without genome duplication. Second, fungal polyploids are not successful in the long term, leading to few extant species derived from ancient polyploidy events. Third, ancient fungal polyploids are difficult to detect, causing the real contribution of polyploidy to fungal evolution to be underappreciated. We consider each of these hypotheses in turn and propose that failure to detect ancient events is the most likely reason for the lack of observed ancient fungal polyploids. We examine whether existing data can provide evidence for previously unrecognized ancient fungal polyploidy events but discover that current resources are too limited. We contend that establishing whether unrecognized ancient fungal polyploidy events exist is important to ascertain whether polyploidy has played a key role in the evolution of the extensive complexity and diversity observed in fungi today and, thus, whether polyploidy is a driver of evolutionary diversifications across eukaryotes. Therefore, we conclude by suggesting ways to test the hypothesis that there are unrecognized polyploidy events in the deep evolutionary history of the fungi.