Changes of effective gene dispersal distances by pollen and seeds across successive life stages in a tropical tree

Abstract

Pollen and seed dispersal are the two key processes in which plant genes move in space, mostly mediated by animal dispersal vectors in tropical forests. Due to the movement patterns of pollinators and seed dispersers and subsequent complex spatial patterns in the mortality of offspring, we have little knowledge of how pollinators and seed dispersers affect effective gene dispersal distances across successive recruitment stages. Using six highly polymorphic microsatellite loci and parentage analyses, we quantified pollen dispersal, seed dispersal, and effective paternal and maternal gene dispersal distances from pollen‐ and seed‐donors to offspring across four recruitment stages within a population of the monoecious tropical tree Prunus africana in western Kenya. In general, pollen‐dispersal and paternal gene dispersal distances were much longer than seed‐dispersal and maternal gene dispersal distances, with the long‐distance within‐population gene dispersal in P. africana being mostly mediated by pollinators. Seed dispersal, paternal and maternal gene dispersal distances increased significantly across recruitment stages, suggesting strong density‐ and distance‐dependent mortality near the parent trees. Pollen dispersal distances also varied significantly, but inconsistently across recruitment stages. The mean dispersal distance was initially much (23‐fold) farther for pollen than for seeds, yet the pollen‐to‐seed dispersal distance ratio diminished by an order of magnitude at later stages as maternal gene dispersal distances disproportionately increased. Our study elucidates the relative changes in the contribution of the two processes, pollen and seed dispersal, to effective gene dispersal across recruitment. Overall, complex sequential processes during recruitment contribute to the genetic make‐up of tree populations. This highlights the importance of a multistage perspective for a comprehensive understanding of the impact of animal‐mediated pollen and seed dispersal on small‐scale spatial genetic patterns of long‐lived tree species.

Fine-scale spatial genetic dynamics over the life cycle of the tropical tree Prunus africana

“…Usually, seed dispersal by frugivorous birds and large mammals should sustain gene flow across large distances, thereby leading to low levels of SGS. In fact, indirect estimations of gene dispersal distances (both pollen and seeds combined) from microsatellites revealed distances of 236-558 m. Further, also a direct assessment of contemporary pollen and seed dispersal distances using parentage analyses revealed seed dispersal distances of up to 700 m within our study population (Berens et al, 2013), with related individuals found even at far distances. However, direct estimates of pollen and seed dispersal revealed that the majority of seeds were dispersed across short distances, leading to a mean seed dispersal distance of only 5 m (Berens et al, 2013).…”

“…Our results suggested that seed dispersal was strongly distance restricted (mean distances of only 5 m), while pollen dispersal reached over 23-fold longer distances. Yet, strong nonrandom mortality led to a disproportionate increase of realized maternal gene flow distances at later life stages, as well as to strong variation in paternal gene flow distances (Berens et al, 2013). In this study, we used a multi-stage approach to determine whether the observed patterns of SGS are consistent with expectations deriving from the observed biological processes.…”

“…In fact, our analyses of spatial clustering revealed thinning of individuals from offspring clusters across life stages and support these results. Specifically, differing pollen and seed dispersal distances directly estimated at different recruitment stages by means of parentage analyses indicated a non-random density and distant-dependent mortality in our study population, which could be driving the observed patterns (Berens et al, 2013).…”

“…The significant autocorrelation in the first distance interval for adults indicates a close genetic relationship of reproductive nearby individuals. As a large proportion of pollination events normally occur within spatial clusters of conspecific trees (Berens et al, 2013), biparental inbreeding (that is, mating between relatives) may explain the observed heterozygosity deficit. Genetic diversity, in terms of allelic richness and heterozygosity, was similar throughout the life stages in P. africana.…”

“…They found stronger genetic differentiation among seedling populations than among adults, showing that genetic diversity and structure of the species is sensitive to processes reducing gene flow, such as forest fragmentation and local disturbance (Farwig et al, 2008). To better understand these patterns, we used parentage analyses to investigate the extent of gene flow across different life stages mediated by insect pollinators and vertebrate seed dispersers (Berens et al, 2013). Our results suggested that seed dispersal was strongly distance restricted (mean distances of only 5 m), while pollen dispersal reached over 23-fold longer distances.…”