Evolution of syncarpy in angiosperms: theoretical and phylogenetic analyses of the effects of carpel fusion on offspring quantity and quality

Abstract

The repeated evolution of fused carpels (syncarpy) is one of the dominant features of angiosperm macroevolution. We present results of new phylogenetic and theoretical analyses to assess the frequency and nature of transitions to syncarpy, and the possible advantages of syncarpy over apocarpy under a variety of ecological conditions. Using a recent molecular estimate of angiosperm phylogeny, we ascertained that a minimum of 17 independent evolutionary transitions from apocarpy to syncarpy have occurred; about three‐quarters of these transitions allowed pollen tubes to cross between carpels and fertilize ovules that would otherwise be left unfertilized. Most of these transitions also intensified competition between pollen, potentially enhancing offspring fitness. The high proportion of evolutionary transitions promoting pollen competition and pollen‐tube access to all carpels supports the hypothesis that the main advantage of syncarpy is in increasing offspring quality and quantity. The potential advantages of syncarpy were more thoroughly evaluated by analytical and simulation studies. These showed that the advantage of syncarpy over apocarpy involving increased offspring‐quantity held under conditions of marginal pollination and declined with increasing pollination. The offspring‐quality advantage persisted over a wider range of conditions, including under quite high pollination rates.

Seed paternity in flowering plants: an evolutionary perspective

“…Syncarpy intensifies pollen competition and, thus, may increase the chances of obtaining pollen from the best male parent. In support of this idea, and consistent with an adaptive function, a recent phylogenetic analysis estimates that syncarpy has evolved independently 17-26 times in the flowering plants (Armbruster et al 2002).…”

Pollen tube growth in association with a dry‐type stigmatic transmitting tissue and extragynoecial compitum in the basal angiosperm Kadsura longipedunculata (Schisandraceae)

“…Error bars represent 95% confidence interval. compitum in angiosperms with syncarpy (Carr and Carr, 1961;Endress, 1982;Armbruster et al, 2002). Enhanced seed set via pollen tube growth in the extragynoecial compitum occurs because of the ability of pollen tubes from a pollinated carpel to enter the ovary of an unpollinated carpel (Williams et al, 1993;Wang et al, 2006).…”

“…The freely flowing exudates between the adjacent carpels have been posited to transmit pollen tubes from one carpel to another, thereby operating as a cryptic extragynoecial compitum (Endress and Igersheim, 2000). In syncarpous angiosperms, a compitum is a region of shared pollen tube transmitting tissue allowing pollen tubes full access to all ovules within a compound ovary (Carr and Carr, 1961;Armbruster et al, 2002). Although structural studies have provided insight into the distribution of gynoecial exudates, data confirming the spatial relationships of pollen tube transmission within and between carpels with respect to the ECM distribution are absent for the Schisandraceae as are data confirming the histo-and immunochemical nature of the ECM.…”

The flower anatomy of five species of Myrteae and its contribution to the taxonomy of Myrtaceae

“…Carr & Carr (1961) considered the compitum (eu-syncarpous ginoecium) as a connection between the carpels that allows pollen tubes from grains germinating on any stigma or part of the stigma to fertilize ovules belonging to more than one carpel. Armbruster et al (2002) found eu-syncarpous gynoecia for all species of Myrtaceae they analyzed, however, there is variation in the degree of development of the compitum.…”