Near-neighbour optimal outcrossing in the bird-pollinated Anigozanthos manglesii

Abstract

Background and aims: In plants, the spatial and genetic distance between mates can influence reproductive success and offspring fitness. Negative fitness consequences associated with the extremes of inbreeding and outbreeding suggest that there will be an intermediate optimal outcrossing distance (OOD), the scale and drivers of which remain poorly understood. In the bird-pollinated Anigozanthos manglesii (Haemodoraceae) we tested (1) for the presence of within-population OOD, (2) over what scale it occurs, and (3) for OOD under biologically realistic scenarios of multi-donor deposition associated with pollination by nectar-feeding birds.

Methods: We measured the impact of mate distance (spatial and genetic) on seed set, fruit size, seed mass, seed viability and germination success following hand pollination from (1) single donors across 0 m (self), <1 m, 1-3 m, 7-15 m and 50 m, and (2) a mix of eight donors. Microsatellite loci were used to quantify spatial genetic structure and test for the presence of an OOD by paternity assignment after multi-donor deposition.

Key results: Inter-mate distance had a significant impact on single-donor reproductive success, with selfed and nearest-neighbour (<1 m) pollination resulting in only ~50 seeds per fruit, lower overall germination success and slower germination. Seed set was greatest for inter-mate distance of 1-3 m (148 seeds per fruit), thereafter plateauing at ~100 seeds per fruit. Lower seed set following nearest-neighbour mating was associated with significant spatial genetic autocorrelation at this scale. Paternal success following pollination with multiple sires showed a significantly negative association with increasing distance between mates.

Conclusions: Collectively, single- and multi-donor pollinations indicated evidence for a near-neighbour OOD within A. manglesii. A survey of the literature suggests that within-population OOD may be more characteristic of plants pollinated by birds than those pollinated by insects.

Keywords: Anigozanthos manglesii; OCBIL; Optimal outcrossing; bird pollination; fitness; hand pollination; inbreeding.

Fig. 1.

Anigozanthos manglesii flowering head with a New Holland Honeyeater. Photograph by S. D. Hopper.

Fig. 2.

Correlogram showing the genetic correlation coefficient r as a function of distance for A. manglesii distance class sizes of 1, 5, 15 and 50 m. Grey lines show the 95 % confidence interval around the null hypothesis of a random distribution of genotypes. Error bars indicate the 95 % confidence of r as determined by bootstrapping.

Fig. 3.

Tukey’s boxplots showing the effect of distance between mates after single and multi-donor hand pollination on A. manglesii. (A) Fruit size. (B) Number of viable seeds per fruit. (C) Mass of viable seeds. (D) Percentage viability. (E) Total germination success. (F) Days to 50 % germination. Letters indicate Dunn test significance groupings (P < 0.05). The box represents the upper, median and lower quartiles and the whiskers indicate the 1.5× interquartile range; dots represent outliers.

Fig. 4.

Percentage of A. manglesii offspring fathered by each paternal donor after pollen from eight donors (D1–D8) was provided simultaneously. Paternal donors are ordered based on the average genetic distance between the donor and maternal plants. Error bars indicate standard error and letters show the grouping by Dunn test significance (P < 0.05). Individual pairwise genetic distances were calculated in Genalex 6.5 (Peakall and Smouse, 2006, 2012).

Fig. 5.

Effect of (A) spatial distance (r = 0.28, P = 0.026) and (B) pairwise genetic distance (r = −0.30, P = 0.023) between parents on the number of A. manglesii seeds fathered by each pollen donor after pollen from eight donors was provided simultaneously. Individual pairwise genetic distances were calculated in Genalex 6.5 (Peakall and Smouse, 2006, 2012).