Dipterocarpoidae genomics reveal their demography and adaptations to Asian rainforests.

Dipterocarpoideae species form the emergent layer of Asian rainforests. They are the indicator species for Asian rainforest distribution, but they are severely threatened. Here, to understand their adaptation and population decline, we assemble high-quality genomes of seven Dipterocarpoideae species including two autotetraploid species. We estimate the divergence time between Dipterocarpoideae and Malvaceae and within Dipterocarpoideae to be 108.2 (97.8‒118.2) and 88.4 (77.7‒102.9) million years ago, and we identify a whole genome duplication event preceding dipterocarp lineage diversification. We find several genes that showed a signature of selection, likely associated with the adaptation to Asian rainforests. By resequencing of two endangered species, we detect an expansion of effective population size after the last glacial period and a recent sharp decline coinciding with the history of local human activities. Our findings contribute to understanding the diversification and adaptation of dipterocarps and highlight anthropogenic disturbances as a major factor in their endangered status.

Functional trait divergence associated with heteromorphic leaves in a climbing fig.

Introduction: Plants that display heteroblasty possess conspicuous variations in leaf morphology between their juvenile and adult phases, with certain species retaining juvenile-like leaves even in adulthood. Nevertheless, the ecological advantages of maintaining two or more distinct leaf types in heteroblastic plants at the adult stage remain unclear. Method: The aim of this study is to examine the adaptive significance of heteroblastic leaves sampled from branches with divergent functions (sterile and fertile branches) of mature Ficus pumila individuals by comparing their morphological, anatomical, and physiological characteristics. Result: Leaves on sterile branches (LSs) exhibited a significantly larger specific leaf area, thinner palisade and spongy tissues, lower chlorophyll contents, and lower light saturation points than leaves on fertile branches (LFs). These results demonstrate that LSs are better adapted to low light environments, while LFs are well equipped to take advantages of high light conditions. However, both LFs and LSs have a low light compensation point with no significant difference between them, indicating that they start to accumulate photosynthetic products under similar light conditions. Interestingly, significant higher net photosynthetic rate was detected in LFs, showing they have higher photosynthetic capacity. Furthermore, LFs produced significant more nutrients compared to LSs, which may associate to their ability of accumulating more photosynthetic products under full light conditions and higher photosynthetic capacity. Discussion: Overall, we observed a pattern of divergence in morphological features of leaves on two functional branches. Anatomical and physiological features indicate that LFs have an advantage in varied light conditions, providing amounts of photosynthetic products to support the sexual reproduction, while LSs adapt to low light environments. Our findings provide evidence that heteroblasty facilitates F. pumila to utilize varying light environments, likely associated with its growth form as a climbing plant. This strategy allows the plant to allocate resources more effectively and optimize its overall fitness.

Source-sink dynamics assists the maintenance of a pollinating wasp.

Dispersal that unites spatially subdivided populations into a metapopulation with source-sink dynamics is crucial for species persistence in fragmented landscapes. Understanding such dynamics for pollinators is particularly urgent owing to the ongoing global pollination crisis. Here, we investigated the population structure and source-sink dynamics of a pollinating wasp (Wiebesia sp. 3) of Ficus pumila in the Zhoushan Archipelago of China. We found significant asymmetry in the pairwise migrant numbers for 22 of 28 cases on the historical timescale, but only two on the contemporary timescale. Despite a small population size, the sole island not colonized by a superior competitor wasp (Wiebesia sp. 1) consistently behaved as a net exporter of migrants, supplying large sinks. Comparable levels of genetic diversity, with few private alleles and low genetic differentiation (total Fst : 0.03; pairwise Fst : 0.0005-0.0791), were revealed among all the islands. There was a significant isolation-by-distance pattern caused mainly by migration between the competition-free island and other islands, otherwise the pattern was negligible. The clustering analysis failed to detect multiple gene pools for the whole region. Thus, the sinks were most probably organized into a patchy population. Moreover, the estimates of effective population sizes were comparable between the two timescales. Thus the source-sink dynamics embedded within a well-connected population network may allow Wiebesia sp. 3 to persist at a competitive disadvantage. This study provides evidence that metapopulations in the real world may be complicated and changeable over time, highlighting the necessity to study such metapopulations in detail.

Sky islands as foci for divergence of fig trees and their pollinators in southwest China.

The dynamics of populations and their divergence over time have shaped current levels of biodiversity and in the case of the "sky islands" of mountainous southwest (SW) China have resulted in an area of exceptional botanical diversity. Ficus tikoua is a prostrate fig tree subendemic to the area that displays unique intraspecific diversity, producing figs typical of different pollination modes in different parts of its range. By combining climate models, genetic variation in populations of the tree's obligate fig wasp pollinators and distributions of the different plant phenotypes, we examined how this unusual situation may have developed. We identified three genetically distinct groups of a single Ceratosolen pollinator species that have largely parapatric distributions. The complex topography of the region contributed to genetic divergence among the pollinators by facilitating geographical isolation and providing refugia. Migration along elevations in response to climate oscillations further enhanced genetic differentiation of the three pollinator groups. Their distributions loosely correspond to the distributions of the functionally significant morphological differences in the male figs of their host plants, but postglacial expansion of one group has not been matched by spread of its associated plant phenotype, possibly due to a major river barrier. The results highlight how interplay between the complex topography of the "sky island" complex and climate change has shaped intraspecies differentiation and relationships between the plant and its pollinator. Similar processes may explain the exceptional botanical diversity of SW China.

Extremely high proportions of male flowers and geographic variation in floral ratios within male figs of Ficus tikoua despite pollinators displaying active pollen collection.

Most plants are pollinated passively, but active pollination has evolved among insects that depend on ovule fertilization for larval development. Anther-to-ovule ratios (A/O ratios, a coarse indicator of pollen-to-ovule ratios) are strong indicators of pollination mode in fig trees and are consistent within most species. However, unusually high values and high variation of A/O ratios (0.096-10.0) were detected among male plants from 41 natural populations of Ficus tikoua in China. Higher proportions of male (staminate) flowers were associated with a change in their distribution within the figs, from circum-ostiolar to scattered. Plants bearing figs with ostiolar or scattered male flowers were geographically separated, with scattered male flowers found mainly on the Yungui Plateau in the southwest of our sample area. The A/O ratios of most F. tikoua figs were indicative of passive pollination, but its Ceratosolen fig wasp pollinator actively loads pollen into its pollen pockets. Additional pollen was also carried on their body surface and pollinators emerging from scattered-flower figs had more surface pollen. Large amounts of pollen grains on the insects' body surface are usually indicative of a passive pollinator. This is the first recorded case of an actively pollinated Ficus species producing large amounts of pollen. Overall high A/O ratios, particularly in some populations, in combination with actively pollinating pollinators, may reflect a response by the plant to insufficient quantities of pollen transported in the wasps' pollen pockets, together with geographic variation in this pollen limitation. This suggests an unstable scenario that could lead to eventual loss of wasp active pollination behavior.