What is the nature of petals in Caryophyllaceae? Developmental evidence clarifies their evolutionary origin

Floral development is a powerful tool to infer homologies of floral organs and to understand floral evolution. Caryophyllaceae is a major family of core Caryophyllales that possesses petal-like structures (petaloids) with a great diversity in shape. The main purpose of this study is to determine the nature of the second whorl of floral organs in Caryophyllaceae. Mainstream views consider ancestors of Caryophyllaceae as apetalous and interpret petals as centrifugally derived staminodial appendages. This hypothesis, based on morphological similarities of petals with stamens and previous ancestral state reconstruction, is tested here.

A floral developmental investigation of five species was carried out using scanning electron microscopy, combined with character optimization of the presence or absence of second-whorl petaloids.

The calyx is always well developed with a quincuncial aestivation. Petaloids either develop by fractionation of common stamen-petal primordia, as in Spergularia, or petaloid development is independent and precedes alternisepalous stamens in Saponaria and Sagina. In Sagina the petaloid whorl is always fully formed but alternisepalous stamens are often reduced or missing. Petaloids are absent in Gymnocarpos and the investigated Cerastium.

Developmental evidence and character mapping reject the hypothesis that petaloids represent a staminodial whorl and suggest that they are independent structures equivalent to second-whorl petals of most Pentapetalae and present in the basal Caryophyllaceae. Heterochronic shifts, including a delay in petal development and acceleration of androecial growth, are responsible for the amalgamation of petals with the androecium as common stamen-petal primordia and their appearance as stamen-derived appendages. Selective pollinator pressure in Caryophyllaceae led to variable petal expansion or reduction and loss. This trend corresponds largely with the general tendency in the core Caryophyllales for petal loss and perianth reorganization.