A metabolic perspective on polyploid invasion and the emergence of life histories: insights from a mechanistic model

Abstract

Whole genome duplication (WGD, polyploidization), the fusion of unreduced gametes, has been identified as a driver of genetic and phenotypic novelty. Unreduced gamete formation is common in a wide range of species, but surprisingly, few polyploidization events have shown to be ecologically successful. Positive density dependence, by minority cytotype exclusion, and niche shifts are currently considered the most important drivers behind ecological failure or success. Genome doubling also results in increased cell sizes and metabolic expenses which, on their own may be sufficient to drive polyploid establishment in stable environments where their simple ancestors thrive. We developed a mechanistic model, motivated by data from natural plant polyploid species, to test whether realistic changes in size and metabolic efficiency allow polyploids to coexist with, or even invade, their original diploid population. Central to the model is metabolic efficiency, a functional trait that determines how energy gained from size-dependent photosynthetic metabolism is allocated to basal metabolism, somatic growth and reproductive growth. Polyploid invasion was observed across a wide range of metabolic efficiency differences between polyploids and their ancestors. Higher metabolic efficiency facilitates polyploid invasion, but even with minor deficits, establishment was facilitated by recurrent formation in these settings of high competition for nutrients. Interestingly, a long-term coexistence with the diploid ancestor was found to be possible only within a narrow range of this parameter space. Perenniality of the plants did not qualitatively affect these insights. Feedbacks between size-dependent metabolism and allocation of gained energy generated eventually size and age differences, resulting in intra- and intercytotype competition for nutrients as the major force for population dynamics. We thus demonstrate that changes in metabolic efficiency on their own are sufficient to impose establishment, but these advantages do not need to be substantial.