Novelties of the flowering plant pollen tube underlie diversification of a key life history stage

Abstract

The origin and rapid diversification of flowering plants has puzzled evolutionary biologists, dating back to Charles Darwin. Since that time a number of key life history and morphological traits have been proposed as developmental correlates of the extraordinary diversity and ecological success of angiosperms. Here, I identify several innovations that were fundamental to the evolutionary lability of angiosperm reproduction, and hence to their diversification. In gymnosperms pollen reception must be near the egg largely because sperm swim or are transported by pollen tubes that grow at very slow rates (< Ϸ20 m/h). In contrast, pollen tube growth rates of taxa in ancient angiosperm lineages (Amborella, Nuphar, and Austrobaileya) range from Ϸ80 to 600 m/h. Comparative analyses point to accelerated pollen tube growth rate as a critical innovation that preceded the origin of the true closed carpel, long styles, multiseeded ovaries, and, in monocots and eudicots, much faster pollen tube growth rates. Ancient angiosperm pollen tubes all have callosic walls and callose plugs (in contrast, no gymnosperms have these features). The early association of the callose-walled growth pattern with accelerated pollen tube growth rate underlies a striking repeated pattern of faster and longer-distance pollen tube growth often within solid pathways in phylogenetically derived angiosperms. Pollen tube innovations are a key component of the spectacular diversification of carpel (flower and fruit) form and reproductive cycles in flowering plants.heterochrony ͉ key innovation ͉ modularity ͉ origin of angiosperms ͉ evo-devo

Fossil evidence for a herbaceous diversification of early eudicot angiosperms during the Early Cretaceous

“…This discovery contributes to an emerging pattern of early eudicots and eudicot-like plants as small herbs rather than woody plants as previously thought. An initially herbaceous radiation of eudicots that included the origin of the crown-group makes sense in the context of angiosperm reproductive innovations that promote short seed-to-seed time [66][67][68], because herbs tend to reach reproductive maturity earlier, have higher nucleotide substitution rates and have faster rates of climate niche evolution compared to their woody counterparts [69][70][71][72][73][74]. Therefore, the herbaceous habit may have been a key trait allowing eudicots to diversify in Early Cretaceous communities that were still dominated by gymnosperms and ferns.…”

Fossil evidence for low gas exchange capacities for Early Cretaceous angiosperm leaves

“…diagnose whether these fossil leaves came from plants adapted to wet (.2000 mm yr 21 rainfall) and forest understory habitats like those characterizing Amborella as well as most Austrobaileyales and Chloranthales (Feild et al 2004(Feild et al , 2009. Specifying the habitat context of austrobaileyoid/chloranthoids is critical for determining how functional trait diversity in extant basal lineages bears on how the first flowering plants functioned and the selective contexts responsible for diverse hypothesized key innovations of early angiosperm success (Hickey and Doyle 1977;Retallack and Dilcher 1981;Taylor and Hickey 1996;Feild and Arens 2007;Williams 2008;Feild et al 2009). Paleoenvironmental proxy records indicate high annual rainfalls (up to 4500 mm yr 21 ) and tropical to paratropical temperatures for all of the fossils sampled (Upchurch and Wolfe 1987;Upchurch and Dilcher 1990;Upchurch 1995;White et al 2001;Ufnar et al 2008).…”

Ancestral traits and specializations in the flowers of the basal grade of living angiosperms

“…- Williams (2008Williams ( , 2009) has shown that pollen tubes grow relatively slowly in the transmitting tract of the carpels in the ANITA grade as compared to other angiosperms, with a speed of growth intermediate between that in gymnosperms and Mesangiospermae. Pollen tube transmitting tracts are short because long styles are lacking (Endress, 2015).…”