Economy, efficiency, and the evolution of pollen tube growth rates

Am J Bot. 2016 Mar;103(3):471-83. doi: 10.3732/ajb.1500264. Epub 2016 Mar 2.

Abstract

Premise: Pollen tube growth rate (PTGR) is an important aspect of male gametophyte performance because of its central role in the fertilization process. Theory suggests that under intense competition, PTGRs should evolve to be faster, especially if PTGR accurately reflects gametophyte quality. Oddly, we know remarkably little about how effectively the work of tube construction is translated to elongation (growth and growth rate). Here we test the prediction that pollen tubes grow equally efficiently by comparing the scaling of wall production rate (WPR) to PTGR in three water lilies that flower concurrently: Nymphaea odorata, Nuphar advena and Brasenia schreberi.

Methods: Single-donor pollinations on flower or carpel pairs were fixed just after pollen germination (time A) and 45 min later (time B). Mean PTGR was calculated as the average increase in tube length over that growth period. Tube circumferences (C) and wall thicknesses (W) were measured at time B. For each donor, WPR = mean (C × W) × mean PTGR.

Key results: Within species, pollen tubes maintained a constant WPR to PTGR ratio, but species had significantly different ratios. N. odorata and N. advena had similar PTGRs, but for any given PTGR, they had the lowest and highest WPRs, respectively.

Conclusions: We showed that growth rate efficiencies evolved by changes in the volume of wall material used for growth and in how that material was partitioned between lateral and length dimensions. The economics of pollen tube growth are determined by tube design, which is consequent on trade-offs between efficient growth and other pollen tube functions.

Keywords: Nymphaeales; callose; cell wall synthesis; developmental constraint; efficiency; evolution of development; functional trait; pollen competition; progamic phase.

Publication types

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

MeSH terms

  • Biological Evolution*
  • Cell Wall / metabolism
  • Models, Biological
  • Nymphaeaceae / growth & development*
  • Pollen Tube / anatomy & histology
  • Pollen Tube / growth & development*
  • Regression Analysis
  • Species Specificity
  • Temperature