Antonio R. Castilla

Positive density-dependent reproduction regulated by local kinship and size in an understorey tropical tree

BACKGROUND AND AIMS Global pollinator declines and continued habitat fragmentation highlight the critical need to understand reproduction and gene flow across plant populations. Plant size, conspecific density and local kinship (i.e. neighbourhood genetic relatedness) have been proposed as important mechanisms influencing the reproductive success of flowering plants, but have rarely been simultaneously investigated. METHODS We conducted this study on a continuous population of the understorey tree Miconia affinis in the Forest Dynamics Plot on Barro Colorado Island in central Panama. We used spatial, reproductive and population genetic data to investigate the effects of tree size, conspecific neighbourhood density and local kinship on maternal and paternal reproductive success. We used a Bayesian framework to simultaneously model the effects of our explanatory variables on the mean and variance of maternal viable seed set and siring success. KEY RESULTS Our results reveal that large trees had lower proportions of viable seeds in their fruits but sired more seeds. We documented differential effects of neighbourhood density and local kinship on both maternal and paternal reproductive components. Trees in more dense neighbourhoods produced on average more viable seeds, although this positive density effect was influenced by variance-inflation with increasing local kinship. Neighbourhood density did not have significant effects on siring success. CONCLUSIONS This study is one of the first to reveal an interaction among tree size, conspecific density and local kinship as critical factors differentially influencing maternal and paternal reproductive success. We show that both maternal and paternal reproductive success should be evaluated to determine the population-level and individual traits most essential for plant reproduction. In addition to conserving large trees, we suggest the inclusion of small trees and the conservation of dense patches with low kinship as potential strategies for strengthening the reproductive status of tropical trees.

Sex-specific phenotypic selection and geographic variation in gender divergence in a gynodioecious shrub

In sexually polymorphic plant species the extent of gender divergence in floral morphology and phenology may be influenced by gender-specific selection patterns imposed by pollinators, which may change geographically. Distribution margins are areas where changes in the pollinator fauna, and thus variation in gender divergence of floral traits, are expected. We tested for pollination-driven geographic variation in the gender divergence in floral and phenological traits in the gynodioecious shrub Daphne laureola, in core and marginal areas differing in the identity of the main pollinator. Pollinators selected for longer corolla tubes in hermaphrodite individuals only in core populations, which in turn recorded higher fruit set. Consistent with these phenotypic selection patterns, gender divergence in flower corolla length was higher in core populations. Moreover, pollinators selected towards delayed flowering on hermaphrodite individuals only in marginal populations, where the two sexes differed more in flowering time. Our results support that a shift in main pollinators is able to contribute to geographic variation in the gender divergence of sexually polymorphic plant species.

Adding landscape genetics and individual traits to the ecosystem function paradigm reveals the importance of species functional breadth

Significance Pollinators mediate reproductive processes between plants; however, little is known about how plant and pollinator traits impact pollen dispersal and resulting genetic connectivity. Our study quantifies pollen-dispersal distances and pollination effectiveness for individual pollinator species. We demonstrate that seed set is positively driven by pollinator body size, but long-distance pollen dispersal is mediated by both large-bodied and small-bodied bees. We also reveal that individual plant and population attributes impact pollen-dispersal distances and seed production, respectively. Thus, we show that plant and pollinator traits mediate pollination function and that the entire pollinator community, large and small, plays an important role in the maintenance of genetic connectivity. Animal pollination mediates both reproduction and gene flow for the majority of plant species across the globe. However, past functional studies have focused largely on seed production; although useful, this focus on seed set does not provide information regarding species-specific contributions to pollen-mediated gene flow. Here we quantify pollen dispersal for individual pollinator species across more than 690 ha of tropical forest. Specifically, we examine visitation, seed production, and pollen-dispersal ability for the entire pollinator community of a common tropical tree using a series of individual-based pollinator-exclusion experiments followed by molecular-based fractional paternity analyses. We investigate the effects of pollinator body size, plant size (as a proxy of floral display), local plant density, and local plant kinship on seed production and pollen-dispersal distance. Our results show that while large-bodied pollinators set more seeds per visit, small-bodied bees visited flowers more frequently and were responsible for more than 49% of all long-distance (beyond 1 km) pollen-dispersal events. Thus, despite their size, small-bodied bees play a critical role in facilitating long-distance pollen-mediated gene flow. We also found that both plant size and local plant kinship negatively impact pollen dispersal and seed production. By incorporating genetic and trait-based data into the quantification of pollination services, we highlight the diversity in ecological function mediated by pollinators, the influential role that plant and population attributes play in driving service provision, and the unexpected importance of small-bodied pollinators in the recruitment of plant genetic diversity.

Elevation, Not Deforestation, Promotes Genetic Differentiation in a Pioneer Tropical Tree.

The regeneration of disturbed forest is an essential part of tropical forest ecology, both with respect to natural disturbance regimes and large-scale human-mediated logging, grazing, and agriculture. Pioneer tree species are critical for facilitating the transition from deforested land to secondary forest because they stabilize terrain and enhance connectivity between forest fragments by increasing matrix permeability and initiating disperser community assembly. Despite the ecological importance of early successional species, little is known about their ability to maintain gene flow across deforested landscapes. Utilizing highly polymorphic microsatellite markers, we examined patterns of genetic diversity and differentiation for the pioneer understory tree Miconia affinis across the Isthmus of Panama. Furthermore, we investigated the impact of geographic distance, forest cover, and elevation on genetic differentiation among populations using circuit theory and regression modeling within a landscape genetics framework. We report marked differences in historical and contemporary migration rates and moderately high levels of genetic differentiation in M. affinis populations across the Isthmus of Panama. Genetic differentiation increased significantly with elevation and geographic distance among populations; however, we did not find that forest cover enhanced or reduced genetic differentiation in the study region. Overall, our results reveal strong dispersal for M. affinis across human-altered landscapes, highlighting the potential use of this species for reforestation in tropical regions. Additionally, this study demonstrates the importance of considering topography when designing programs aimed at conserving genetic diversity within degraded tropical landscapes.

To be or not to be better pollinated: Differences between sex morphs in marginal gynodioecious populations

PREMISE OF THE STUDY Changes in the pollinator communities of marginal plant populations can affect their pollination quantity or quality. Geographic variation in pollination success can alter the reproductive advantage that female plants require to persist within gynodioecious populations. Particularly valuable is determining the pollination success at the prezygotic stage in self-compatible gynodioecious species whose females do not exhibit enhanced seed production. METHODS In core and marginal populations of Daphne laureola, we analyzed the differences between hermaphrodites and females in the proportion of flowers visited, the stigma pollen loads, and the quantity of pollen tubes in styles. We also examined the relationship between the number of pollen tubes in styles vs. the number of pollen grains on stigmas using piecewise regression and binomial generalized linear mixed models. KEY RESULTS Pollinators deposited larger pollen loads on flowers in marginal populations. In marginal populations, female flowers received more pollinator visits and more pollen grains on their stigmas, and they had more pollen tubes in their styles than did female flowers in core populations. Both piecewise regression and binomial GLMM analyses showed that females in marginal populations had a lower proportion of grains that developed tubes than females in the core populations, which suggests decreased pollination quality. CONCLUSIONS More efficient pollination services in marginal populations decreased the overall differences in the prezygotic pollination success between the sex morphs. Our results also suggest that pollination quality is lower in females of marginal populations, which could be counteracting the increased pollination in females in marginal populations.