Increased above‐ground resource allocation is a likely precursor for independent evolutionary origins of annuality in the Pooideae grass subfamily

Abstract

Summary Semelparous annual plants flower a single time during their 1‐yr life cycle, investing much of their energy into rapid reproduction. By contrast, iteroparous perennial plants flower multiple times over several years, and partition their resources between reproduction and persistence. To which extent evolutionary transitions between life‐cycle strategies are internally constrained at the developmental, genetic and phylogenetic level is unknown. Here we study the evolution of life‐cycle strategies in the grass subfamily Pooideae and test if transitions between them are facilitated by evolutionary precursors. We integrate ecological, life‐cycle strategy and growth data in a phylogenetic framework. We investigate if growth traits are candidates for a precursor. Species in certain Pooideae clades are predisposed to evolve annuality from perenniality, potentially due to the shared inheritance of specific evolutionary precursors. Seasonal dry climates, which have been linked to annuality, were only able to select for transitions to annuality when the precursor was present. Allocation of more resources to above‐ground rather than below‐ground growth is a candidate for the precursor. Our findings support the hypothesis that only certain lineages can respond quickly to changing external conditions by switching their life‐cycle strategy, likely due to the presence of evolutionary precursors.

Understanding Past, and Predicting Future, Niche Transitions based on Grass Flowering Time Variation

“…This requires an understanding of the physiological and developmental basis of iteroparous perenniality in different environmental contexts, as well as an awareness of potential factors that might facilitate switches between annuality and perenniality in different clades. A recent study on Pooideae grasses inferred 51 independent shifts from the perennial to annual habit and demonstrated a link between the origin of annuality and an undefined precursor trait (Lindberg et al, 2020). Further investigation into the nodes of origin for the precursor trait(s) revealed that they correspond to an increase in belowground to aboveground biomass ratio, suggesting that changes in resource allocation are critical for the evolution of growth habit, and by extension in the engineering of more efficient crop grasses.…”

The morphogenesis of fast growth in plants

“…1), showing that fast RGR is not a prerequisite for the evolution of annual life history. Instead, annuals evolve at a faster rate in lineages with a larger investment in shoot relative to root mass (Lindberg et al, 2020). The faster growth of C 4 than C 3 grasses is manifested as gigantism in the size of shoot phytomers, but with no change in shoot branching.…”

“…1), showing that fast RGR is not a prerequisite for the evolution of annual life history. Instead, annuals evolve at a faster rate in lineages with a larger investment in shoot relative to root mass (Lindberg et al ., 2020).…”

QTL Map of Early- and Late-Stage Perennial Regrowth in Zea diploperennis

“…Some perennial species are seasonally dormant while others stay green year round. Evolutionary transitions between annual and perennial growth modes have occurred numerous times during land plant evolution ( Friedman and Rubin, 2015 ; Lindberg et al, 2020 ). Perenniality is usually the ancestral trait and the annual growth mode is derived ( Friedman and Rubin, 2015 ).…”