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.

This is a repository copy of The genetic consequences of habitat specificity for fig trees in southern African fragmented forests.

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.

Genetic considerations are rarely applied in forest conservation management strategies, but forest fragmentation can reduce pollen and seed dispersal both between and within isolated fragments. Gene flow and immigration rates determine the extent to which individual plants are related to each other at different distances from themselves. This gradation in relatedness is known as a population's fine scale spatial genetic structure (SGS). Specifically, reduced but clumped immigration from distant fragments reduces fine scale SGS, whereas reduced gene flow within fragments increases fine scale SGS. In addition, non-random mortality caused by post-dispersal ecological processes can also affect SGS. We studied the effects of fragmentation on the fine scale SGS of Ficus species with different habitat preferences and distributional ranges in an archipelago of South African forest patches. Significant fine scale SGS present in all three species suggests gene dispersal is restricted, even within forest fragments, probably due to localised seed dispersal. An endemic forest specialist, F. bizanae, has an unusually high fine scale SGS for a monoecious Ficus.This may be explained by several features that reduce pollen dispersal distances and are more typical of dioecious Ficus. A significant negative kinship coefficient in one F. bizanae population suggests that clumped long-distance immigration may have occurred in the past. Significant fine scale SGS in adult but not juvenile F. craterostoma suggests that recent population fragmentation has negatively affected long-distance immigration. Supplementation of F. craterostoma gene flow would maintain its genetic diversity. In contrast, the limited range of F. bizanae may result from its pollinator's behavior, rather than specific habitat requirements and ensuring its long-term survival may require artificial introductions to other forests.