Studies investigating the evolution of flowering plants have long focused on isolating mechanisms such as pollinator specificity. Some recent studies have proposed a role for introgressive hybridization between species, recognizing that isolating processes such as pollinator specialization may not be complete barriers to hybridization. Occasional hybridization may therefore lead to distinct yet reproductively connected lineages. We investigate the balance between introgression and reproductive isolation in a diverse clade using a densely sampled phylogenomic study of fig trees (Ficus, Moraceae). Codiversification with specialized pollinating wasps (Agaonidae) is recognized as a major engine of fig diversity, leading to about 850 species. Nevertheless, some studies have focused on the importance of hybridization inFicus, highlighting the consequences of pollinator sharing. Here, we employ dense taxon sampling (520 species) throughout Moraceae and 1,751 loci to investigate phylogenetic relationships and the prevalence of introgression among species throughout the history ofFicus. We present a well-resolved phylogenomic backbone forFicus, providing a solid foundation for an updated classification. Our results paint a picture of phylogenetically stable evolution within lineages punctuated by occasional local introgression events likely mediated by local pollinator sharing, illustrated by clear cases of cytoplasmic introgression that have been nearly drowned out of the nuclear genome through subsequent lineage fidelity. The phylogenetic history of figs thus highlights that while hybridization is an important process in plant evolution, the mere ability of species to hybridize locally does not necessarily translate into ongoing introgression between distant lineages, particularly in the presence of obligate plant–pollinator relationships.

As the largest genus in Moraceae, Ficus is widely distributed across tropical and subtropical regions and exhibits a high degree of adaptability to different environments. At present, however, the phylogenetic relationships of this genus are not well resolved, and chloroplast evolution in Ficus remains poorly understood. Here, we sequenced, assembled, and annotated the chloroplast genomes of 10 species of Ficus, downloaded and assembled 13 additional species based on next-generation sequencing data, and compared them to 46 previously published chloroplast genomes. We found a highly conserved genomic structure across the genus, with plastid genome sizes ranging from 159,929 bp (Ficus langkokensis) to 160,657 bp (Ficus religiosa). Most chloroplasts encoded 113 unique genes, including a set of 78 protein-coding genes, 30 transfer RNA (tRNA) genes, four ribosomal RNA (rRNA) genes, and one pseudogene (infA). The number of simple sequence repeats (SSRs) ranged from 67 (Ficus sagittata) to 89 (Ficus microdictya) and generally increased linearly with plastid size. Among the plastomes, comparative analysis revealed eight intergenic spacers that were hotspot regions for divergence. Additionally, the clpP, rbcL, and ccsA genes showed evidence of positive selection. Phylogenetic analysis indicated that none of the six traditionally recognized subgenera of Ficus were monophyletic. Divergence time analysis based on the complete chloroplast genome sequences showed that Ficus species diverged rapidly during the early to middle Miocene. This research provides basic resources for further evolutionary studies of Ficus.

Summary: Interactions between mutualists, competitors, and antagonists have contrasting ecological effects that, sustained over generations, can influence micro‐ and macroevolution. Dissimilar benefits and costs for these interactions should cause contrasting co‐diversification patterns between interacting clades, with prevalent co‐speciation by mutualists, association loss by competitors, and host switching by antagonists. We assessed these expectations for a local assemblage of 26 fig species (Moraceae: Ficus), 26 species of mutualistic (pollinating), and 33 species of parasitic (galling) wasps (Chalcidoidea). Using newly acquired gene sequences, we inferred the phylogenies for all three clades. We then compared the three possible pairs of phylogenies to assess phylogenetic congruence and the relative frequencies of co‐speciation, association duplication, switching, and loss. The paired phylogenies of pollinators with their mutualists and competitors were significantly congruent, unlike that of figs and their parasites. The distributions of macroevolutionary events largely agreed with expectations for mutualists and antagonists. By contrast, that for competitors involved relatively frequent association switching, as expected, but also unexpectedly frequent co‐speciation. The latter result likely reflects the heterogeneous nature of competition among fig wasps. These results illustrate the influence of different interspecific interactions on co‐diversification, while also revealing its dependence on specific characteristics of those interactions.

Most pollinator fig wasps are host plant specific, with each species only breeding in the figs of one fig tree species, but increasing numbers of species are known to be pollinated by more than one fig wasp, and in rare instances host switching can result in Ficus species sharing pollinators. In this study, we examined factors facilitating observed host switching at Xishuangbanna in Southwestern (SW) China, where Ficus squamosa is at the northern edge of its range and lacks the fig wasps that pollinate it elsewhere, and its figs are colonized by a Ceratosolen pollinator that routinely breeds in figs of F. heterostyla. We recorded the habitat preferences of F. squamosa and F. heterostyla at Xishuangbanna, and compared characteristics such as fig size, location and colour at receptive phase. Furthermore, the vegetative and reproductive phenologies in the populations of F. squamosa and F. heterostyla were recorded weekly at Xishuangbanna Tropical Botanical Garden for 1 year. Ficus squamosa is a shrub found near fast-flowing rivers, F. heterostyla is a small tree of disturbed forest edges. Although preferring different habitats, they can be found growing close together. Both species have figs located at or near ground level, but they differ in size when pollinated. Fig production in F. squamosa was concentrated in the colder months. F. heterostyla produced more figs in summer but had some throughout the year. The absence of its normal pollinators, in combination with similarly located figs and partially complementary fruiting patterns appear to have facilitated colonization of F. squamosa by the routine pollinator of F. heterostyla. The figs probably also share similar attractant volatiles. This host switching suggests one mechanism whereby fig trees can acquire new pollinators and emphasizes the likely significance of edges of ranges in the genesis of novel fig tree–fig wasp relationships.