Understanding polyploid establishment: temporary persistence or stable coexistence?

Abstract

Polyploidy, resulting from whole‐genome duplication (WGD), is ubiquitous in nature and reportedly associated with extreme environments and biological invasions. However, WGD usually comes with great costs, raising questions about the establishment chance of newly formed polyploids. The surprisingly high number of polyploid and mixed‐ploidy species observed in nature may be a consequence of their continuous emergence or may reflect stable polyploid persistence and even coexistence with the ancestral ploidy under certain circumstances. However, empirical studies on contemporary polyploid establishment often neglect the cost–benefit balances of polyploid characteristics, tradeoffs between phenotypic characteristics, intercytotype interactions, recurrent polyploid formation, and stochastic processes. Here, we advocate for considering population‐level success, combining the aforementioned factors that affect polyploid establishment and long‐term coexistence with their ancestors. We approach the paradox of polyploid establishment despite high costs from a modern coexistence theory perspective and give an overview of the diversity of mechanisms and their timing that may potentially enable stable rather than transient persistence.

Whole-genome duplication in the Multicellularity Long Term Evolution Experiment

“…First, we show that nascent polyploidy is not necessarily transient, even prior to the evolution of genome-stabilizing mechanisms. WGD is long known to bring immediate phenotypic changes, many stemming from increased cell size (a universal feature of polyploid cells and central to evolved polyploid isolates in the MuLTEE), which can confer fitness benefits under novel environments 12,17,18,20,21 . Here, we experimentally demonstrate that selection favoring the immediate phenotypic effects of WGD is sufficient to drive both its origin and maintenance, despite the intrinsic instability of polyploid genomes.…”

“…This costly and transient nature of nascent polyploidy raises the question of how polyploidy can rise in a diploid population and be maintained over long-term evolution. A central hypothesis is that the immediate phenotypic effects of polyploidy, often stemming from the increased size of polyploid cells, can confer fitness advantages under novel, often stressful, environments 12,17–20 . This has been suggested to contribute to many ancient WGDs that rose during periods of drastic climate change 21 .…”