Genomic evidence of prevalent hybridization throughout the evolutionary history of the fig-wasp pollination mutualism

Abstract

Ficus (figs) and their agaonid wasp pollinators present an ecologically important mutualism that also provides a rich comparative system for studying functional co-diversification throughout its coevolutionary history (~75 million years). We obtained entire nuclear, mitochondrial, and chloroplast genomes for 15 species representing all major clades of Ficus. Multiple analyses of these genomic data suggest that hybridization events have occurred throughout Ficus evolutionary history. Furthermore, cophylogenetic reconciliation analyses detect significant incongruence among all nuclear, chloroplast, and mitochondrial-based phylogenies, none of which correspond with any published phylogenies of the associated pollinator wasps. These findings are most consistent with frequent host-switching by the pollinators, leading to fig hybridization, even between distantly related clades. Here, we suggest that these pollinator host-switches and fig hybridization events are a dominant feature of fig/wasp coevolutionary history, and by generating novel genomic combinations in the figs have likely contributed to the remarkable diversity exhibited by this mutualism.

Adaptation of Fig Wasps (Agaodinae) to Their Host Revealed by Large-Scale Transcriptomic Data

“…Our results demonstrate a dramatic contraction across a wide range of gene families in pollinating fig wasps compared to other Hymenoptera, offering support for results from previous studies [ 6 , 33 , 63 , 64 ]. It has been reported that in the genomes of Ceratosolen solmi, Eupristina verticillata , and Wiebesia pumila , many gene families related to chemosensory, detoxification, and innate immune response are reduced [ 6 , 33 , 63 , 64 ].…”

“…Our results demonstrate a dramatic contraction across a wide range of gene families in pollinating fig wasps compared to other Hymenoptera, offering support for results from previous studies [ 6 , 33 , 63 , 64 ]. It has been reported that in the genomes of Ceratosolen solmi, Eupristina verticillata , and Wiebesia pumila , many gene families related to chemosensory, detoxification, and innate immune response are reduced [ 6 , 33 , 63 , 64 ]. This finding is reflected in our transcriptome study: for the whole family of Agaonidae, the contracted genes families at the level of expression in newly emerged adult fig wasps were mainly enriched in relation to signal transduction and immune response in comparison to other parasitic wasps ( Nasonia vitripennis and Copidosoma floridanum ), ants, bees, and other Hymenoptera.…”

“…Chemosensory genes play an important role for insects in foraging, ovipositioning, mating, avoiding natural enemies, and searching for hosts [ 65 ]. Our results showed that Ors, Grs, and Irs in fig wasp species are reduced to a greater extent in comparison to other insect species, with similar numbers as Ceratosolen solmi , Eupristina verticillate , and Wiebes pumila —Ors: 43–46, 48, and 67; Grs: 5, 4, and 4; Irs: 11–31, 30, and 16, respectively [ 6 , 33 , 63 ]. Genes in the Or family are related to the detection of volatile signals, while those in the Gr family generally contribute to the detection of soluble chemical substances.…”

Genome sequencing and comparative analysis of Ficus benghalensis and Ficus religiosa trees reveal evolutionary mechanisms of longevity

“…Further, the observed high percentage of duplicated genes in these genomes may have occurred due to expansion of gene families that provide long lifespan to plants, as in case of Oak genome 32 . Also, the high percentage of inter-species collinearity between the two Ficus genomes might be a result of Ficus hybridization events caused by frequent host switching of the fig pollinators 33 . Among the LTR retrotransposon class of repeats, Gypsy/DIRS1 elements were higher than Ty1/Copia elements in both the species (Supplementary Tables 5-6), similar to other Ficus genomes 7,18,34 .…”

Fitness costs for fig wasps that fail to pollinate their host Ficus perforata

“…This species-specificity makes the system ideal for studying coevolutionary questions. Additionally, because there are over 750 species of fig trees globally, the system allows comparative studies (Cruaud et al 2012;Rasplus et al 2020;Wang et al 2021). Two thirds of fig wasp species pollinate actively, ie they actively use their front legs to first collect pollen from their natal fig and place it into specialized pollen pockets, then actively use their front legs to disperse this pollen onto the flowers in the fig where they oviposit (Frank 1984;Cruaud et al 2012).…”