Higher levels of multiple paternities increase seedling survival in the long-lived tree Eucalyptus gracilis.

Martin F Breed,Andrew J Lowe,Matthew J Christmas

doi:10.1371/journal.pone.0090478

Abstract

Studying associations between mating system parameters and fitness in natural populations of trees advances our understanding of how local environments affect seed quality, and thereby helps to predict when inbreeding or multiple paternities should impact on fitness. Indeed, for species that demonstrate inbreeding avoidance, multiple paternities (i.e. the number of male parents per half-sib family) should still vary and regulate fitness more than inbreeding – named here as the ‘constrained inbreeding hypothesis’. We test this hypothesis in Eucalyptus gracilis, a predominantly insect-pollinated tree. Fifty-eight open-pollinated progeny arrays were collected from trees in three populations. Progeny were planted in a reciprocal transplant trial. Fitness was measured by family establishment rates. We genotyped all trees and their progeny at eight microsatellite loci. Planting site had a strong effect on fitness, but seed provenance and seed provenance × planting site did not. Populations had comparable mating system parameters and were generally outcrossed, experienced low biparental inbreeding and high levels of multiple paternity. As predicted, seed families that had more multiple paternities also had higher fitness, and no fitness-inbreeding correlations were detected. Demonstrating that fitness was most affected by multiple paternities rather than inbreeding, we provide evidence supporting the constrained inbreeding hypothesis; i.e. that multiple paternity may impact on fitness over and above that of inbreeding, particularly for preferentially outcrossing trees at life stages beyond seed development.

Highlights

The realised inbreeding rate of monoecious trees, when estimated from mature seeds or seedlings, is usually constrained below their actual inbreeding rate [1]
We explored the variance of estimated family-level mating system parameters further because of possible problems of estimating these parameters from a limited progeny array sample size
We explored whether inbreeding avoidance in monoecious trees constrains inbreeding-fitness correlations at life stages beyond seed development [18], and whether within such systems and life stages, levels of multiple paternities had a greater influence on offspring fitness than inbreeding - the constrained inbreeding hypothesis

Summary

Introduction

The realised inbreeding rate of monoecious trees, when estimated from mature seeds or seedlings, is usually constrained below their actual inbreeding rate [1]. This occurs because inbreeding usually imposes fitness costs at early stages of reproduction [1,2,3,4], via expression of deleterious recessive alleles [5,6,7], leading to the abortion of these inbred offspring. Monoecious trees routinely exhibit multiple paternities because they receive great amounts of pollen from a large diversity of donors [8,9,10]. Fertilisation success is filtered by the availability of receptive flowers (i.e. tree phenology) and the genetic compatibility of pollen-ovule combinations

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Results

Conclusion