Abstract
Angiosperm flowers have diversified in adaptation to pollinators, but are also shaped by developmental and genetic histories. The relative importance of these factors in structuring floral diversity remains unknown. We assess the effects of development, function and evolutionary history by testing competing hypotheses on floral modularity and shape evolution in Merianieae (Melastomataceae). Merianieae are characterized by different pollinator selection regimes and a developmental constraint: tubular anthers adapted to specialized buzz-pollination. Our analyses of tomography-based 3-dimensional flower models show that pollinators selected for functional modules across developmental units and that patterns of floral modularity changed during pollinator shifts. Further, we show that modularity was crucial for Merianieae to overcome the constraint of their tubular anthers through increased rates of evolution in other flower parts. We conclude that modularity may be key to the adaptive success of functionally specialized pollination systems by making flowers flexible (evolvable) for adaptation to changing selection regimes.
Highlights
Flowers represent ideal systems to test hypotheses on modularity
We present a novel approach to the study of flower shape evolution through the integration of advanced imaging techniques (High-Resolution X-ray Computed Tomography22,23), state-of-the-art landmark-based geometric morphometrics, and phylogenetic comparative methods[24]
This setup allows us to evaluate whether developmental modules persist in Merianieae flowers or whether these flowers were shaped by functional adaptation to different pollinator selection regimes and converge into distinct areas of multivariate trait space[21]
Summary
Flowers represent ideal systems to test hypotheses on modularity. They comprise different organ types, which arise through different developmental pathways[18,20], and may show strong developmental modularity. 300) Merianieae species included in this study represent two independent shifts from buzz-bee pollination to a mixed-vertebrate pollination syndrome and two independent shifts to a passerine pollination syndrome, respectively This setup allows us to evaluate whether developmental modules persist in Merianieae flowers or whether these flowers were shaped by functional adaptation to different pollinator selection regimes and converge into distinct areas of multivariate trait space[21]. Hypothesis 1 (developmental modularity) proposes that flowers are structured by development rather than by pollinator-mediated selection (Fig. 118,20,29) and we do not expect to find differences in developmental modularity between the different Merianieae pollination syndromes. We conclude that the strong ancestral modularity has allowed Merianieae to overcome the structural constraint of tubular anther dehiscence through increased rates of evolution in other flower parts and to flexibly adapt to changes in pollinator selection regimes
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