Floral evolution by simplification in Monanthotaxis (Annonaceae) and hypotheses for pollination system shifts

Paul H Hoekstra,Lars W Chatrou,Erik Smets,Jan J Wieringa

doi:10.1038/s41598-018-30607-2

Paul H Hoekstra, Lars W Chatrou + Show 2 more

Open Access

https://doi.org/10.1038/s41598-018-30607-2

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Abstract

Simplification by reduction has occurred many times independently in the floral evolution of angiosperms. These reductions have often been attributed to changes in reproductive biology. In the angiosperm plant family Annonaceae, most species have flowers with six petals, and many stamens and carpels. In the genus Monanthotaxis several deviations from this pattern have been observed, including flowers that contain three petals and three stamens only. New DNA sequences were generated for 42 specimens of Monanthotaxis. Five chloroplast markers and two nuclear markers for 72 out of 94 species of Monanthotaxis were used to reconstruct a phylogeny of the genus, which revealed several well-supported, morphologically distinct clades. The evolution of four quantitative and two qualitative floral characters was mapped onto this phylogeny, demonstrating a reduction in flower size and number of flower parts in Monanthotaxis. A large variation in stamen forms and numbers, strong correlations between petal size, stamen and carpel number, combined with a non-gradual mode of evolution and the sympatric co-occurrence of Monanthotaxis species from different clades suggest that the high diversity in the African rainforest of this genus is caused by switches in pollination systems.

Highlights

The evolution of life shows a trend towards increasing complexity and synorganisation
The ancestral state of many other floral characters is uncertain for angiosperms, which is likely caused by the variability of many of those states in the early diverging angiosperms, complicating the inference of ancestral states[13]
The dataset used for the phylogenetic analyses comprised 6649 bp of sequence data that has been gathered for 88 specimens, including 80 specimens of Monanthotaxis representing 77% of the species of this genus

Summary

Introduction

The evolution of life shows a trend towards increasing complexity and synorganisation. Despite some uncertainty in the inference of ancestral floral characters at the crown node of angiosperms, e.g regarding the number of perianth and stamen whorls, it is evident that reductive trends are widespread in the evolution of angiosperms[5]. Some of these trends are linked to fundamental changes in reproductive biology, such as the change from bi- to unisexual flowers with a concomitant reduction in number, or entire disappearance, of either stamens or carpels[6]. Two perianth and stamen whorls[5] Both increases in size and complexity, as well as simplification occurred later in evolution and can be observed in extant angiosperms[12,13]. In the majority of species the flowers have a large number of stamens in multiple whorls, with the whorled pattern often becoming irregular with increasing numbers of stamens[16]

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