Adaptive Reduction of Male Gamete Number in a Selfing Species

Takashi Tsuchimatsu, Hiroyuki Kakui, Misako Yamazaki, Cindy Marona, Hiroki Tsutsui, Afif Hedhly, Dazhe Meng, Yutaka Sato, Thomas Städler, Ueli Grossniklaus, Masahiro M. Kanaoka, Michael Lenhard, Magnus Nordborg & Kentaro K. Shimizu

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Received: 9th February 18

The number of male gametes produced is critical for reproductive success and varies greatly between and within species1-3. Evolutionary reduction of male gamete production has been widely reported in plants as a hallmark of the selfing syndrome, as well as in humans. Such a reduction may simply represent deleterious decay4-7, but evolutionary theory predicts that breeding systems could act as a major selective force on male gamete number: while large numbers of sperm should be produced in highly promiscuous species because of male–male gamete competition1, reduced sperm numbers may be advantageous at lower outcrossing rates because of the cost of gamete production. Here we used genome-wide association study (GWAS) to show a signature of polygenic selection on pollen number in the predominantly selfing plant Arabidopsis thaliana. The top associations with pollen number were significantly more strongly enriched for signatures of selection than those for ovule number and 107 phenotypes analyzed previously, indicating polygenic selection8. Underlying the strongest association, responsible for 20% of total pollen number variation, we identified the gene REDUCED POLLEN NUMBER 1 affecting cell proliferation in the male germ line. We validated its subtle but causal allelic effects using a quantitative complementation test with CRISPR-Cas9-generated null mutants in a nonstandard wild accession. Our results support polygenic adaptation underlying reduced male gamete numbers.

Read in full at bioRxiv.

This is an abstract of a preprint hosted on an independent third party site. It has not been peer reviewed but is currently under consideration at Nature Communications.

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