Complex pollination of a tropical Asian rainforest canopy tree by flower-feeding thrips and thrips-feeding predators.

PREMISE OF THE STUDY: In tropical rainforests of Southeast Asia, a highly fecund thrips (Thrips spp.) responds rapidly to the mass flowering at multiple-year intervals characteristic of certain species such as the canopy tree studied here, Shorea acuminata, by feeding on flower resources. However, past DNA analyses of pollen adherent to thrips bodies revealed that the thrips promoted a very high level of self-pollination. Here, we identified the pollinator that contributes to cross-pollination and discuss ways that the pollination system has adapted to mass flowering. METHODS: By comparing the patterns of floral visitation and levels of genetic diversity in adherent pollen loads among floral visitors, we evaluated the contribution of each flower visitor to pollination. KEY RESULTS: The big-eyed bug, Geocoris sp., a major thrips predator, was an inadvertent pollinator, and importantly contributed to cross-pollination. The total outcross pollen adhering to thrips was approximately 30% that on the big-eyed bugs. Similarly, 63% of alleles examined in S. acuminata seeds and seedlings occurred in pollen adhering to big-eyed bugs; about 30% was shared with pollen from thrips. CONCLUSIONS: During mass flowering, big-eyed bugs likely travel among flowering S. acuminata trees, attracted by the abundant thrips. Floral visitation patterns of big-eyed bugs vs. other insects suggest that these bugs can maintain their population size between flowering by preying upon another thrips (Haplothrips sp.) that inhabits stipules of S. acuminata throughout the year and quickly respond to mass flowering. Thus, thrips and big-eyed bugs are essential components in the pollination of S. acuminata.

Mixed Mating System Are Regulated by Fecundity in Shorea curtisii (Dipterocarpaceae) as Revealed by Comparison under Different Pollen Limited Conditions.

The maintenance of mixed mating was studied in Shorea curtisii, a dominant and widely distributed dipterocarp species in Southeast Asia. Paternity and hierarchical Bayesian analyses were used to estimate the parameters of pollen dispersal kernel, male fecundity and self-pollen affinity. We hypothesized that partial self incompatibility and/or inbreeding depression reduce the number of selfed seeds if the mother trees receive sufficient pollen, whereas reproductive assurance increases the numbers of selfed seeds under low amounts of pollen. Comparison of estimated parameters of self-pollen affinity between high density undisturbed and low density selectively logged forests indicated that self-pollen was selectively excluded from mating in the former, probably due to partial self incompatibility or inbreeding depression until seed maturation. By estimating the self-pollen affinity of each mother tree in both forests, mother trees with higher amount of self-pollen indicated significance of self-pollen affinity with negative estimated value. The exclusion of self-fertilization and/or inbreeding depression during seed maturation occurred in the mother trees with large female fecundity, whereas reproductive assurance increased self-fertilization in the mother trees with lower female fecundity.

Non-density dependent pollen dispersal of Shorea maxwelliana (Dipterocarpaceae) revealed by a Bayesian mating model based on paternity analysis in two synchronized flowering seasons.

Pollinator syndrome is one of the most important determinants regulating pollen dispersal in tropical tree species. It has been widely accepted that the reproduction of tropical forest species, especially dipterocarps that rely on insects with weak flight for their pollination, is positively density-dependent. However differences in pollinator syndrome should affect pollen dispersal patterns and, consequently, influence genetic diversity via the mating process. We examined the pollen dispersal pattern and mating system of Shorea maxwelliana, the flowers of which are larger than those of Shorea species belonging to section Mutica which are thought to be pollinated by thrips (weak flyers). A Bayesian mating model based on the paternity of seeds collected from mother trees during sporadic and mass flowering events revealed that the estimated pollen dispersal kernel and average pollen dispersal distance were similar for both flowering events. This evidence suggests that the putative pollinators - small beetles and weevils - effectively contribute to pollen dispersal and help to maintain a high outcrossing rate even during sporadic flowering events. However, the reduction in pollen donors during a sporadic event results in a reduction in effective pollen donors, which should lead to lower genetic diversity in the next generation derived from seeds produced during such an event. Although sporadic flowering has been considered less effective for outcrossing in Shorea species that depend on thrips for their pollination, effective pollen dispersal by the small beetles and weevils ensures outcrossing during periods of low flowering tree density, as occurs in a sporadic flowering event.

Effects of flowering tree density on the mating system and gene flow in Shorea leprosula (Dipterocarpaceae) in Peninsular Malaysia.

Pristine tropical rainforests in Southeast Asia have rich species diversity and are important habitats for many plant species. However, the extent of these forests has declined in recent decades and they have become fragmented due to human activities. These developments may reduce the genetic diversity of species within them and, consequently, the species' ability to adapt to environmental changes. Our objective in the study presented here was to clarify the effect of tree density on the genetic diversity and gene flow patterns of Shorea leprosula Miq. populations in Peninsular Malaysia. For this purpose, we related genetic diversity and pollen flow parameters of seedling populations in study plots to the density of mature trees in their vicinity. The results show that gene diversity and allelic richness were not significantly correlated to the mature tree density. However, the number of rare alleles among the seedlings and the selfing rates of the mother trees were negatively correlated with the density of the adult trees. Furthermore, in a population with high mature tree density pollination distances were frequently <200 m, but in populations with low adult tree density the distances were longer. These findings suggest that the density of flowering trees affects selfing rates, gene flow and, thus, the genetic diversity of S. leprosula populations. We also found an individual S. leprosula tree with a unique reproductive system, probably apomictic, mating system.

Genetic diversity of Eurycoma longifolia inferred from single nucleotide polymorphisms.

Eurycoma longifolia Jack. is a treelet that grows in the forests of Southeast Asia and is widely used throughout the region because of its reported medicinal properties. Widespread harvesting of wild-grown trees has led to rapid thinning of natural populations, causing a potential decrease in genetic diversity among E. longifolia. Suitable genetic markers would be very useful for propagation and breeding programs to support conservation of this species, although no such markers currently exist. To meet this need, we have applied a genome complexity reduction strategy to identify a series of single nucleotide polymorphisms (SNPs) within the genomes of several E. longifolia accessions. We have found that the occurrence of these SNPs reflects the geographic origins of individual plants and can distinguish different natural populations. This work demonstrates the rapid development of molecular genetic markers in species for which little or no genomic sequence information is available. The SNP markers that we have developed in this study will also be useful for identifying genetic fingerprints that correlate with other properties of E. longifolia, such as high regenerability or the appearance of bioactive metabolites.