Here we test whether genome size is a predictor of pollen size. If it were, inferences of ancient genome size would be possible using the abundant paleo-palynolgical record. We performed regression analyses across 464 species of pollen width and genome size. We found a significant positive trend. However, regression analysis using phylogentically independent contrasts did not support the correlated evolution of these traits. Instead, a large split between angiosperms and gymnosperms for both pollen width and genome size was revealed. Sister taxa were not more likely to show a positive contrast when compared to deeper nodes. However, significantly more congeneric species had a positive trend than expected by chance. These results may reflect the strong selection pressure for pollen to be small. Also, because pollen grains are not metabolically active when measured, their biology is different than other cells which have been shown to be strongly related to genome size, such as guard cells. Our findings contrast with previously published research. It was our hope that pollen size could be used as a proxy for inferring the genome size of ancient species. However, our results suggest pollen is not a good candidate for such endeavors. 1. Introduction Pollen range in size by over three orders of magnitude [1, 2] (Figure 1). The variation in pollen size may stem from strong selection pressures related to pollen dispersal strategies. For example, wind-pollinated species may achieve long-distance transport by having pollen that are (1) small, (2) light weighed, (3) dehydrated, and (4) that have shapes conducive to wind capture [1–3]. However, some gymnosperms have large pollen but are also wind pollinated (Pinaceae and Podocarpaceae) [4]. Two air-filled sacs (sacci) facilitate wind dispersal in these groups [3, 4]. Pollen of species that use insect facilitated dispersal can sometimes be quite large, but we are not aware of any study showing that pollen dispersed by insects is generally larger than pollen dispersed abiotically. However, there is greater interspecific variability for pollen grain size in species that use insect dispersal [5–7]. Understanding what controls pollen size from a developmental perspective will enhance our understanding of the ecological significance of variation in pollen size. Figure 1: Pollen varies considerably in size. (a) Images of pollen at the same scale and (b) (Inset on a): a histogram of pollen widths showing a log normal distribution. It has frequently been observed that pollen size is related to the length of the style (see
References
[1]
R. P. Wodehouse, Pollen Grains, McGraw-Hill, New York, NY, USA, 1935.
[2]
J. Muller, “Form and function in angiosperm pollen,” Annals of the Missouri Botanical Garden, vol. 66, pp. 594–632, 1979.
[3]
K. J. Niklas, “The aerodynamics of wind pollination,” The Botanical Review, vol. 51, no. 3, pp. 328–386, 1985.
[4]
P. B. Tomlinson, “Functional morphology of saccate pollen in conifers with special reference to Podocarpaceae,” International Journal of Plant Sciences, vol. 55, no. 6, pp. 699–715, 1994.
[5]
L. D. Harder, “Pollen-size comparisons among animal-pollinated angiosperms with different pollination characteristics,” Biological Journal of the Linnean Society, vol. 64, no. 4, pp. 513–525, 1998.
[6]
T. M. Culley, S. G. Weller, and A. K. Sakai, “The evolution of wind pollination in angiosperms,” Trends in Ecology and Evolution, vol. 17, no. 8, pp. 361–369, 2002.
[7]
J. Friedman and S. C. Barrett, “Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plants,” Annals of Botany, vol. 103, no. 9, pp. 1515–1527, 2009.
[8]
F. Delpino, “Sull'opera, la distribuzione dei sessi nelle piante e la legge che osta alla perennità della fecundazione consanguinea,” Atti de la Societa Italiana di Scienze Naturali, vol. 10, pp. 272–303, 1867.
[9]
R. W. Cruden, “Pollen grain size, stigma depth, and style length: the relationships revisited,” Plant Systematics and Evolution, vol. 278, no. 3-4, pp. 223–238, 2009.
[10]
C. Darwin, The Different Forms of Flowers on Plants of the Same Species, J. Murray, London, UK, 2nd edition, 1884.
[11]
B. A. Krizek, “Making bigger plants: key regulators of final organ size,” Current Opinion in Plant Biology, vol. 12, no. 1, pp. 17–22, 2009.
[12]
A. Linkles, K. Gaber, C. A. Knight, et al., “The evolution of seeds,” New Phytologist, vol. 186, pp. 817–831, 2010.
[13]
J. M. Beaulieu, I. J. Leitch, S. Patel, A. Pendharkar, and C. A. Knight, “Genome size is a strong predictor of cell size and stomatal density in angiosperms,” New Phytologist, vol. 179, no. 4, pp. 975–986, 2008.
[14]
F. W. Gould, “Pollen size as related to polyploidy and speciation in the Andropogon saccharoides-A. barbinodis complex,” Brittonia, vol. 9, no. 2, pp. 71–75, 1957.
[15]
G. Orjeda, R. Freyre, and M. Iwanaga, “Production of 2n pollen in diploid Ipomoea trifida, a putative wild ancestor of sweet potato,” Journal of Heredity, vol. 81, no. 6, pp. 462–467, 1990.
[16]
T. Altmann, B. Damm, W. B. Frommer, et al., “Easy determination of ploidy level in Arabidopsis thaliana plants by means of pollen size measurement,” Plant Cell Reports, vol. 13, no. 11, pp. 652–656, 1994.
[17]
M. D. Bennett, “Nuclear DNA content and minimum generation time in herbaceous plants,” Proceedings of the Royal Society of London B, vol. 181, no. 63, pp. 109–135, 1972.
[18]
M. D. Bennett and I. J. Leitch, “Plant DNA C-values database release 4.0,” October 2005, http://data.kew.org/cvalues/.
[19]
J. Greilhuber, J. Dole?el, M. A. Lysák, and M. D. Bennett, “The origin, evolution and proposed stabilization of the terms ‘genome size’ and ‘C-value’ to describe nuclear DNA contents,” Annals of Botany, vol. 95, no. 1, pp. 255–260, 2005.
[20]
G. C. S. Clarke, “Boraginaceae,” Review of Palaeobotany and Palynology, vol. 24, no. 2, pp. 59–101, 1977.
[21]
A. J. Kalis, “Papaveraceae,” Review of Palaeobotany and Palynology, vol. 28, no. 3-4, pp. 209–260, 1979.
[22]
Q. C. B. Cronk and G. C. S. Clarke, “Convolvulaceae,” Review of Palaeobotany and Palynology, vol. 33, no. 1, pp. 117–135, 1981.
[23]
P. Van Leeuwen, W. Punt, and P. P. Hoen, “Polygonaceae,” Review of Palaeobotany and Palynology, vol. 57, no. 1-2, pp. 81–151, 1988.
[24]
P. F. Stevens, “Angiosperm Phylogeny Website, version 9,” June 2008, http://www.mobot.org/MOBOT/research/APweb/.
[25]
N. Wikstr?m, V. Savolainen, and M. W. Chase, “Evolution of the angiosperms: calibrating the family tree,” Proceedings of the Royal Society of London B, vol. 268, no. 1482, pp. 2211–2220, 2001.
[26]
C. O. Webb, D. D. Ackerly, and S. W. Kembel, “Phylocom: software for the analysis of phylogenetic community structure and trait evolution,” Bioinformatics, vol. 24, no. 18, pp. 2098–2100, 2008.
[27]
J. Felsenstein, “Phylogenies and the comparative method,” American Naturalist, vol. 125, no. 1, pp. 1–15, 1985.
[28]
G. Theodore Jr., P. H. Harvey, and A. R. Ives, “Procedures for the analysis of comparative data using phylogenetically independent contrasts,” Systematic Biology, vol. 41, no. 1, pp. 18–32, 1992.
[29]
A. T. Moles, D. D. Ackerly, C. O. Webb, J. C. Twiddle, J. B. Dickie, and M. Westoby, “A brief history of seed size,” Science, vol. 307, no. 5709, pp. 576–580, 2005.
[30]
P. D. Cantino, J. A. Doyle, S. W. Graham, et al., “Towards a phylogenetic nomenclature of Tracheophyta,” Taxon, vol. 56, no. 3, pp. 822–846, 2007.
[31]
A. M. Timmons, E. T. O'Brien, Y. M. Charters, S. J. Dubbels, and M. J. Wilkinson, “Assessing the risks of wind pollination from fields of genetically modified Brassica napus ssp. oleifera,” Euphytica, vol. 85, no. 1–3, pp. 417–423, 1995.
[32]
J. E. Cresswell, “The influence of nectar and pollen availability on pollen transfer by individual flowers of oil-seed rape (Brassica napus) when pollinated by bumblebees (Bombus lapidarius),” Journal of Ecology, vol. 87, no. 4, pp. 670–677, 1999.
[33]
I. H. Williams, A. P. Martin, and R. P. White, “The pollination requirements of oil-seed rape (Brassica napus L.),” Journal of Agricultural Science, vol. 106, pp. 27–30, 1986.
[34]
K. E. Hayter and J. E. Cresswell, “The influence of pollinator abundance on the dynamics and efficiency of pollination in agricultural Brassica napus: implications for landscape-scale gene dispersal,” Journal of Applied Ecology, vol. 43, no. 6, pp. 1196–1202, 2006.
[35]
C. A. Knight and J. Raven, in preperation, Function and Cell Size.
[36]
J. A. Connolly, M. J. Oliver, J. M. Beaulieu, C. A. Knight, L. Tomanek, and M. A. Moline, “Correlated evolution of genome size and cell volume in diatoms (Bacillariophyceae),” Journal of Phycology, vol. 44, no. 1, pp. 124–131, 2008.
[37]
K. Faegri and P. Deuse, “Size variations in pollen grains with different treatment,” Pollen Spores, vol. 2, pp. 293–298, 1960.