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

Proceedings of the Royal Society B Biological Sciences, vol. 293

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.

Authors 5

1. Sreetama Bhadra corresponding

   German Centre for Integrative Biodiversity Research · Czech Academy of Sciences, Institute of Botany · Leipzig University

   Affiliation as printed

   German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, 1

   Institute of Botany of the Czech Academy of Sciences, 3

   Leipzig University, 2

2. Ilia J. Leitch

   Royal Botanic Gardens, Kew

   Affiliation as printed

   Royal Botanic Gardens, Kew, 4

3. Sidonie Bellot

   Royal Botanic Gardens, Kew

   Affiliation as printed

   Royal Botanic Gardens, Kew, 4

4. William J. Baker

   Aarhus University · Royal Botanic Gardens, Kew

   Affiliation as printed

   Aarhus Universitet, 5

   Royal Botanic Gardens, Kew, 4

5. Renske E. Onstein Aachen Naturalis Biodiversity Center

   Leiden University · Naturalis Biodiversity Center · German Centre for Integrative Biodiversity Research · Leipzig University

   Affiliation as printed

   German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, 1

   Leiden University, 7

   Leipzig University, 2

   Naturalis Biodiversity Center, 6