Trait evolution drives speciation through complex interactions between genome size, adaptation and allometry

Abstract

Speciation shapes biodiversity, yet why some lineages diversify faster than others remains unclear. Theory predicts that traits promote ecological speciation through adaptation, but their evolvability (‘trait flexibility’) may be impacted by allometric and genomic constraints. Here we test this by integrating phylogenetic, trait and genome size data for palms (Arecaceae)—a large pantropical family (>2500 species) with 167-fold variation in certain traits (e.g. fruit size) and 60-fold genome size variation. Using structural equation modelling, we test three hypotheses: trait evolution promotes speciation (H1: trait flexibility hypothesis), and speciation and trait evolution rates are constrained by allometry (H2: allometric constraint hypothesis) and genome size (H3: large genome constraint hypothesis). We detected seven major speciation rate shifts during approximately 110-million-years of palm evolution. Tip-derived speciation rates increased with faster evolution in leaf size and plant height, supporting H1, whereas correlated evolution between all traits indirectly influenced speciation, supporting H2. Large genomes were associated with decreased plant height and stem diameter evolution rates supporting H3, but the genome size-speciation association was sensitive to phylogenetic autocorrelation. Our findings illustrate how the interplay between genome size, allometry and trait evolvability affect speciation, emphasizing the importance of holistic approaches for uncovering general mechanisms driving speciation throughout the Tree of Life.