Disentangling the components of pollen limitation in a widespread herb with gametophytic self‐incompatibility

Abstract

Premise Seed production is frequently limited by the receipt of insufficient or low‐quality pollen, collectively termed “pollen limitation” (PL). In taxa with gametophytic self‐incompatibility (GSI), incompatible pollen can germinate on stigmas but pollen tubes are arrested in styles. This allows for estimates of pollen performance before, during, and after self‐recognition, as well as insight into the factors underlying pollen quality limitation in GSI taxa. Methods We scored pollen performance following self and outcross pollinations in Argentina anserina to identify the location of self‐recognition and establish the relationship between pollen tubes and seed production. We then estimated quantity and quality components of PL from >3300 field‐collected styles. We combined our results with other studies to test the prediction that low pollen quality, but not quantity, drives higher PL in self‐incompatible (SI) taxa than in self‐compatible taxa (SC). Results Self and outcross pollen germinated readily on stigmas, but 96% of germinated self‐pollen was arrested during early tube elongation. Reproduction in the field was more limited by pollen quality than by quantity, and pollen failure near the location of self‐recognition was a stronger barrier to fertilization than pollen germination. Across 26 taxa, SI species experienced stronger pollen quality, but not quantity, limitation than SC species. Conclusions Evaluating pollen performance at multiple points within pistils can elucidate potential causes of pollen quality limitation. The receipt of incompatible pollen inhibits fertilization success more than insufficient pollen receipt or poor pollen germination in A. anserina. Likewise, pollen quality limitation drives high overall PL in other SI taxa.

Effective population size mediates the impact of pollination services on pollen limitation

“…For each flower, we averaged the number of stigmatic pollen grains, and pollen tube number across the 5 styles scored. Previous work using a subset of the samples presented here showed that results from analyses of style-level and flower-level average data were similar [36].…”

“…To quantify components of pollen quality and quality limitation in A. anserina populations, we assessed prezygotic stages of fertilization success from open-pollinated flowers collected in the field [29,36,[40][41][42][43][44]. We collected styles from senesced flowers in 13 populations of A. anserina during peak flowering in July of 2019, 2020 and 2021.…”

“…was determined by collecting fresh flowers from the field in 2021, storing them in 70% EtOH, and counting ovules under a dissecting microscope [36]. The number of flowers scored per population ranged from 6 to 42 (mean = 12.4 per population).…”

“…To estimate a pre-fertilization metric of pollen quality, we used the piece-wise regression approach of Alonso et al [29] within each population [36,[41][42][43][44]. For each population, we modelled the number of pollen tubes at the base of styles as a function of pollen grains adhered to stigmas using a segmented regression (segmented package [48]).…”

Drivers of strong isolation and small effective population size at a leading range edge of a widespread plant

“…(Rosaceae) is a perennial herb, with a cosmopolitan global distribution in temperate environments. It reproduces both sexually via self-incompatible flowers (Cisternas-Fuentes et al 2023 ), and vegetatively via runners (Eriksson 1988 ). Flowers of anserina are predominately pollinated by small solitary bees and flies (Koski and Ashman 2015 ).…”