Echoes of ancient introgression punctuate stable genomic lineages in the evolution of figs

Abstract

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 in Ficus , 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 of Ficus . We present a well-resolved phylogenomic backbone for Ficus , 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.

Field sampling of fig pollinator wasps across host species and host developmental phase: Implications for host recognition and specificity

“…With some exceptions, pollinating wasps exhibit high fig host specificity, though increasingly host sharing and host switching have been documented (Moe et al, 2011 ; Molbo et al, 2003 ; Satler et al, 2019 ). Host switching and sharing are consistent with genetic data indicating that hybridization and introgression occur over ecological time scales and that these processes have occurred throughout the history of Ficus (Gardner et al, 2023 ; Satler et al, 2022 ; Wang, Zhang, et al, 2021 ). Host specificity will depend on fig host recognition and therefore identifying cues used by pollinators to identify an appropriate host within their ecological context is important (Bronstein, 1987 ; Compton, 1993 ).…”

“…However, increased sampling, collectioning of molecular data from multiple loci or genomic data, and improved co‐phylogenetic analyses, have eroded the support for this binary scenario of strict co‐adaptation and co‐speciation (Cook & Segar, 2010 ; Cruaud, Cook, et al, 2012 ; Hembry & Althoff, 2016 ; Herre et al, 2008 ; Satler et al, 2019 , 2020 , 2022 ). These more recent analyses indicate that pollinator and fig phylogenies are often incongruent at lower taxonomic levels (species within Ficus sections or within wasp genera), and there is increasing evidence for regular hybridization between figs (Gardner et al, 2023 ; Jackson et al, 2008 ; Machado et al, 2005 ; Satler et al, 2019 , 2020 , 2022 ; Wang, Zhang, et al, 2021 ; Wilde et al, 2020 ). And a recent co‐phylogenetic analysis of a well‐studied community of Neotropical fig species and their associated pollinator species suggested that host‐shift events have been as common as strict co‐speciation events (Satler et al, 2019 ).…”

Hybridization, polyploidization, and morphological convergence make dozens of taxa into one chaotic genetic pool: a phylogenomic case of the Ficus erecta species complex (Moraceae)

“…The previous studies have identified subsect. Frutescentiae as a robust monophyletic group within the genus Ficus , characterized by their dioecious syconia, predominantly small shrub-like habit, the distinct Terminalia-branching pattern, axillary figs, staminate flowers mostly scattered or near the ostiole,stamens 2 or 3, representing one of its nine primary branches ( Berg, 2003 ; Gardner et al., 2023 ). Addressing taxonomic issues within any individual species of the complex necessitates a comprehensive understanding of the genetic backdrop of the entire subsection, highlighting the intertwined evolutionary narratives within this group.…”

A high-quality chromosome-level genome assembly of Ficus hirta

“…Fig trees occupy a broad range of habitats 1 , 2 and are among the most ecologically important plant groups in tropical forests 3 , 4 . The genus is characterized by its enclosed inflorescences (figs, also called syconia) that vary in size and location, but have remained unchanged in fundamental structure since the genus first appeared around 45 mya 5 – 7 . The evolutionary history of the genus has therefore combined extensive radiation and ecological diversification with a reproductive conservatism that is linked to their unique interaction with the trees’ only pollinators (fig wasps, Hymenoptera Agaonidae).…”

“…The significance of hybridization in Ficus diversification has been debated, but Gardner et al . have shown that while introgression has taken place, it has not had a major impact on evolution in the genus 7 .…”