Development differs between independently evolved staminode whorls in the same flower

Abstract

Premise Staminodes are commonly studied in hermaphroditic flowers, in which a fraction of the androecium evolves into infertile structures, but few studies have addressed the evolution of staminodes as they occur through the loss of stamen function in carpellate flowers. Plants of Paronychia (Caryophyllaceae) are monoecious with hermaphroditic flowers with one staminodial whorl, except for the dioecious P. chartacea and P. minima. Dioecious species have carpellate flowers that evolved an additional whorl of staminodes, providing an exceptional opportunity to study a second origin of staminodes in the same flower. Methods Using scanning electron microscopy, we observed the development of carpellate and staminate flowers to determine whether the developmental pathway of the staminodes in hermaphroditic flowers was co‐opted during the evolutionary transition to unisexual flowers. Results In carpellate flowers, antesepalous staminodes initiate as sterile anthers that develop similar to functioning stamens, but arrest before full development, leaving a rudimentary anther with lateral lobes that correspond to thecae. After antesepalous staminodes arrest, alternisepalous staminodes initiate as structures that correspond with filaments, as they do in staminate and hermaphroditic flowers. Conclusions The second origin of staminodes in carpellate flowers evolved using a different developmental pathway than what had previously evolved in the alternisepalous whorl. The two androecial whorls in the same flowers are serialogous as members of the androecium, but are paralogous as staminodes on the basis of structural and developmental differences.