Pollination and mating traits underlie diverse reproductive strategies in flowering plants
Authors: Helmstetter Andrew J. , Méndez Marcos , Schönenberger Jürg , Burgarella Concetta , Anderson Bruce , von Balthazar Maria , Billiard Sylvain , de Boer Hugo , Cros Johanne , Delecroix Pierre-Alexandre , Dufay Mathilde , Pannell John R. , Bianchi Dessislava Savova , Schoen Daniel J. , Vallejo-Marin Mario , Zenil-Ferguson Rosana , Sauquet Hervé , Glémin Sylvain , Käfer Jos 
Published: February 2024

Reproductive and floral traits are strikingly diverse in angiosperms. However, general patterns in how these traits are associated and how these associations shape species diversity are still poorly known. To date, major trait associations, or plant ecological strategies, have largely been described using vegetative traits and are underpinned by size and growth. However, these do not consider traits relating to pollination, mating and sexual systems, which are critical to species’ reproductive success. Here, we characterize the strategies plants have evolved to achieve reproduction using 21 traits from an original set of 360 species sampled in 259 families across the angiosperm phylogeny. While outcrossing rates were associated with a well-known trait axis involving plant size and growth form, we revealed that pollination-related traits, including flower sex and floral reward, contribute to an equally important axis of variation. Surprisingly, this pollination axis clearly sets species with unisexual flowers apart from those with bisexual flowers, likely the result of selection for sexual specialisation at the flower and individual levels. Three angiosperm-scale reproductive strategies emerged, all containing considerable diversity that cannot be easily reduced, in contrast to strategies derived from vegetative traits. Our study demonstrates that often-overlooked, pollination-related traits represent an important dimension of plant trait variation that provides new insights into the ecology and evolution of mating and sexual systems. The reproductive strategies outlined here are the result of long-term evolutionary processes and ecological interactions between plants and pollinators, highlighting the importance of considering both fields when disentangling the origins of reproductive diversity.

Significance statement

Flowering plants (angiosperms) possess a spectacular diversity of flower morphologies, colours, modes of pollination and systems of reproduction. These traits are known to have evolved together through interactions with pollinators and have contributed to species diversification. However, we lack a general view of how these traits are associated across the angiosperm tree of life. To this end we sampled species representing all major angiosperm groups to uncover the main associations among reproductive and life-history traits. We described an important pollination-related axis of trait variation that is largely independent of a well-known size/lifespan axis, leading to the identification of three broad reproductive strategies. Our study provides a framework to explore how evolutionary history and ecology shape reproductive strategies at finer scales.