Parental genetic distance and patterns in nonrandom mating and seed yield in predominately selfing Arabidopsis thaliana

Abstract

In this study, we ask two questions: (1) Is reproductive success independent of parental genetic distance in predominately selfing plants? (2) In the absence of early inbreeding depression, is there substantial maternal and/or paternal variation in reproductive success in natural populations? Seed yield in single pollinations and proportion of seeds sired in mixed pollinations were studied in genetically defined accessions of the predominately selfing plant Arabidopsis thaliana by conducting two diallel crosses. The first diallel was a standard, single pollination design that we used to examine variance in seed yield. The second diallel was a mixed pollination design that utilized a standard pollen competitor to examine variance in proportion of seeds sired. We found no correlation between reproductive success and parental genetic distance, and self-pollen does not systematically differ in reproductive success compared to outcross pollen, suggesting that Arabidopsis populations do not experience embryo lethality due to early-acting inbreeding or outbreeding depression. We used these data to partition the contributions to total phenotypic variation from six sources, including maternal contributions, paternal contributions and parental interactions. For seed yield in single pollinations, maternal effects accounted for the most significant source of variance (16.6 %). For proportion of seeds sired in mixed pollinations, the most significant source of variance was paternal effects (17.9 %). Thus, we show that population-level genetic similarities, including selfing, do not correlate with reproductive success, yet there is still significant paternal variance under competition. This suggests two things. First, since these differences are unlikely due to early-acting inbreeding depression or differential pollen viability, this implicates natural variation in pollen germination and tube growth dynamics. Second, this strongly supports a model of fixation of pollen performance genes in populations, offering a focus for future genetic studies in differential reproductive success.

New Arabidopsis Advanced Intercross Recombinant Inbred Lines Reveal Female Control of Nonrandom Mating

“…This would not be the case if the NPTII gene influenced nonrandom mating phenotypes. Second, our mixed pollinations of Col-NPTII and Col-0 pollen on virgin Col-0 and Col-4 pistils show no statistical difference in the siring success of the two pollen types and do not differ from the expected 1:1 ratio in progeny (Carlson et al, 2009(Carlson et al, , 2013. This demonstrates both that the NPTII gene does not change the competitive ability of the pollen and that we consistently deliver roughly equal amounts of pollen during mixed pollinations.…”

“…This aspect of nonrandom mating is less pronounced in predominantly selfing plants, likely because of reduced genetic load. In Arabidopsis, self pollen does not perform noticeably worse, and in some cases it performs better, than outcross pollen, and there is no correlation between reproductive success and genetic distances between pollen and maternal plants (Carlson et al, 2013). Thus, predominantly selfing plants provide the opportunity to examine aspects of nonrandom mating separable from the effects of inbreeding depression.…”

“…As outcrossing populations become increasingly self-fertilizing, they both lose heterozygosity, and their genetic load is purged Schemske and Lande, 1985;Lande et al, 1994;Byers and Waller, 1999;Crnokrak and Barrett, 2002). This is the case for Arabidopsis, whose tested populations show relatively low levels of heterozygosity and little evidence for the early-acting inbreeding depression that is indicative of genetic load (Bakker et al, 2006;Bomblies et al, 2010;Platt et al, 2010;Carlson et al, 2013). Thus, this system provides an excellent opportunity to identify and explore the genetic variation in differential reproduction that develops or persists in plant populations unrelated to inbreeding depression.…”

“…Despite this challenge, a number of experimental strategies have been devised to explore the role of the female in nonrandom mating. For example, a number of studies demonstrate that maternal identity influences nonrandom mating patterns Ellstrand, 1986, 1988;Snow and Mazer, 1988;Johnston, 1993;Marshall et al, 2000;Carlson et al, 2009Carlson et al, , 2013. Studies have also established that manipulation of watering or nutrient regimes of maternal plants changes the patterns and magnitude of nonrandom mating (Marshall and Diggle, 2001;Shaner and Marshall, 2003;Haileselassie et al, 2005;Marshall et al, 2007).…”

Can selection on a male mating character result in evolutionary change? A selection experiment on California wild radish, Raphanus sativus

“…Data from wild populations are more limited. In Oenothera organensis , modest clonal repeatability of in vitro pollen tube growth was demonstrated (Havens, 1994), and in Arabidopsis thaliana , substantial variation in proportion of seeds sired among lineages is due to paternal effects (Carlson et al, 2013). But Snow and Mazer (1988) found little evidence for heritability of pollen tube growth rate in Raphanus raphanistrum .…”