Uncoupled evolution of male and female cone sizes in an ancient conifer lineage

Abstract

Sexual functions in gymnosperms are mostly performed by separate reproductive structures, which largely reduces sexual interference and sets the scene for morphological and functional sexual specialization. The evolutionary trajectories followed by traits related to the male and female functions are therefore expected to be uncoupled. Studies on the fossil record of the conifer family Araucariaceae revealed important morphological changes occurring in reproductive cones. Here, we explored the pattern of evolution of male and female cone sizes in Araucariaceae, with a special focus on Araucaria-the most variable and widespread genus in the family. We gathered data on male and female cone sizes from fossils and extant Araucariaceae species. Focusing on Araucaria, we analyzed whether cone sizes are phylogenetically structured. Furthermore, we compared the evolutionary trajectories of male and female cone sizes by evaluating the goodness of fit of different evolutionary models. Finally, we evaluated whether different selective regimes across the phylogeny could have shaped cone morphology. Size changes in Araucariaceae occurred in both male and female cones, with the largest cones appearing in extant Araucaria. In this genus, different evolutionary models best described cone size changes, with male cone evolution best described by a model not influenced by phylogeny and female cone evolution by a stabilizing selection model with two optima. This resulted in contrasting phylogenetic signals, with female cone size being more phylogenetically structured than male cone size. Changes in cone size in Araucariaceae occurred in both male and female cones. The largest male and female cones appeared in Araucaria through uncoupled evolutionary pathways, both involving a natural selection component as a driver of evolutionary change. A contrasting pattern of phylogenetic signal in male and female cone size reflected the uncoupled evolutionary trajectories followed by these sexual structures.