A fitness landscape instability governs the morphological diversity of tip-growing cells

Abstract

Cellular morphology affects many aspects of cellular and organismal physiology. This makes it challenging to understand the evolutionary basis for specific morphologies since the various facets of cellular physiology may exert competing selective pressures on this trait. The influence of these pressures, moreover, will depend on the mechanisms of cellular morphogenesis. To address this problem, we combined experimental cell biology with mechanics-based theory to analyze the morphological diversity of tip-growing cells from across the tree of life. We discovered that an instability in the convergent mechanism of "inflationary" growth shared by these cells leads directly to a bifurcation in their fitness landscape, which imposes a strong global constraint on their morphologies. Additionally, we found that co-selection for cell size and elongation rate explains variation among observable morphologies. This analysis rationalizes the morphology - and provides quantitative insight into the ecology - of an enormous diversity of important fungal, plant, protistan, and bacterial systems. Additionally, our study elucidates a fundamental principle of evolutionary-developmental biology that would be difficult to rigorously demonstrate in more complex systems.