Repeated evolution of tricellular (and bicellular) pollen

Am J Bot. 2014 Apr;101(4):559-71. doi: 10.3732/ajb.1300423. Epub 2014 Mar 24.

Abstract

Premise of study: Male gametophytes of seed plants are sexually immature at the time they are dispersed as pollen, but approximately 30% of flowering plants have tricellular pollen containing fully formed sperm at anthesis. The classic study of Brewbaker (1967: American Journal of Botany 54: 1069-1083) provided a powerful confirmation of the long-standing hypothesis that tricellular pollen had many parallel and irreversible origins within angiosperms. We readdressed the main questions of that study with modern comparative phylogenetic methods.

Methods: We used our own and more recent reports to greatly expand the Brewbaker data set. We modeled trait evolution for 2511 species on a time-calibrated angiosperm phylogeny using (1) Binary State Speciation and Extinction (BiSSE), which accounts for the effect of species diversification rates on character transition rates and, (2) the hidden rates model (HRM), which incorporates variation in transition rates across a phylogeny.

Key results: Seventy percent of species had bicellular pollen. BiSSE found a 1.9-fold higher bicellular to tricellular transition rate than in the reverse direction, and bicellular lineages had a 1.8-fold higher diversification rate than tricellular lineages. HRM found heterogeneity in evolutionary rates, with bidirectional transition rates in three of four rate classes.

Conclusions: The tricellular condition is not irreversible. Pollen cell numbers are maintained at intermediate frequencies because lower net diversification rates of tricellular lineages are counterbalanced by slower state shifts to the bicellular condition. That tricellular lineages diversify slowly and give rise to bicellular lineages slowly reflects a linkage between the evolution of sporophyte lifestyles and the developmental lability of male gametophytes.

Keywords: Dollo’s law; cell cycle; constraint; diversification rate; evolution of development; gametogenesis; heterochrony; parallelism; pollen germination; trade-off.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Biological Evolution*
  • Magnoliopsida / cytology*
  • Magnoliopsida / genetics
  • Models, Biological
  • Phylogeny
  • Pollen / cytology*
  • Pollen / genetics
  • Species Specificity