Pollinator sharing and hybridization in a pair of dioecious figs sheds light on the pathways to speciation
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PROVIDER: S-EPMC10693000 | biostudies-literature | 2023 Oct
REPOSITORIES: biostudies-literature
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Project description:The obligate pollination mutualism between figs (Ficus, Moraceae) and pollinator wasps (Agaonidae, Hymenoptera) is a classic example of cospeciation. However, examples of phylogenetic incongruencies between figs and their pollinators suggest that pollinators may speciate by host shifting. To investigate the mechanism of speciation by host shifting, we examined the phylogenetic relationships and population genetic structures of six closely related fig species and their pollinators from southern China and Taiwan-Ryukyu islands using various molecular markers. The results revealed 1) an extraordinary case of pollinator sharing, in which five distinct fig species share a single pollinator species in southern China; 2) two types of copollination, namely, sympatric copollination by pollinator duplication or pollinator migration, and allopatric copollination by host migration and new pollinator acquisition; 3) fig species from southern China have colonized Taiwan repeatedly and one of these events has been followed by host shifting, reestablishment of host specificity, and pollinator speciation, in order. Based on our results, we propose a model for pollinator speciation by host shifting in which the reestablishment of host-specificity plays a central role in the speciation process. These findings provide important insights into understanding the mechanisms underlying pollinator speciation and host specificity in obligate pollination mutualism.
| S-EPMC8993897 | biostudies-literature
Project description:Obligate pollination mutualisms, in which plant and pollinator lineages depend on each other for reproduction, often exhibit high levels of species specificity. However, cases in which two or more pollinator species share a single host species (host sharing), or two or more host species share a single pollinator species (pollinator sharing), are known to occur in current ecological time. Further, evidence for host switching in evolutionary time is increasingly being recognized in these systems. The degree to which departures from strict specificity differentially affect the potential for hybridization and introgression in the associated host or pollinator is unclear. We addressed this question using genome-wide sequence data from five sympatric Panamanian free-standing fig species (Ficus subgenus Pharmacosycea, section Pharmacosycea) and their six associated fig-pollinator wasp species (Tetrapus). Two of the five fig species, F. glabrata and F. maxima, were found to regularly share pollinators. In these species, ongoing hybridization was demonstrated by the detection of several first-generation (F1) hybrid individuals, and historical introgression was indicated by phylogenetic network analysis. By contrast, although two of the pollinator species regularly share hosts, all six species were genetically distinct and deeply divergent, with no evidence for either hybridization or introgression. This pattern is consistent with results from other obligate pollination mutualisms, suggesting that, in contrast to their host plants, pollinators appear to be reproductively isolated, even when different species of pollinators mate in shared hosts.
| S-EPMC9848820 | biostudies-literature
Project description:BackgroundHost specificity among pollinator fig wasps (Agaonidae) depends on host plant specific volatile cues, but fig wasps must also pass through a narrow physical barrier (the ostiole) if they are to pollinate and oviposit. Across South East Asia the dioecious shrub Ficus hirta is associated with at least ten pollinator species allied to Valisia javana. Ficus triloba has a single recorded pollinator, Valisia esquirolianae. Receptive figs of F. hirta are usually much smaller than those of F. triloba, but at a mainland site where F. hirta has atypically large figs we identified both V. esquirolianae and V. javana from both Ficus species using COI and ITS2 sequencing. To investigate whether this host overlap was exceptional we reared fig wasps from the two trees elsewhere and recorded features that may facilitate host transfer between them, including attractant volatiles, reproductive phenology and the sizes of their figs and fig wasps.ResultsThe two Ficus species were found to support both Valisia species at several of the sites, suggesting that the differences we detected in volatile profiles, ostiole sizes and pollinator head sizes are not strict barriers to host sharing. Valisia javana colonised F. triloba more frequently than V. esquirolianae colonised F. hirta.ConclusionsThis asymmetric sharing of pollinators may reflect the relative abundance of the two species of fig wasps and differences in host reproductive phenology. Asynchronous flowering of individual F. hirta may favor local retention of pollinators, in contrast to the tree-wide synchrony of F. triloba figs, which can generate local shortages of V. esquirolianae. If the pollinator sharing by male figs of F. triloba and F. hirta also occurs in female figs then this could result in gene flow between them.
| S-EPMC8941105 | biostudies-literature
Project description:Hybridization and insect pollination are widely believed to increase rates of plant diversification. The extreme diversity of figs (Ficus) and their obligate pollinators, fig wasps (Agaonidae), provides an opportunity to examine the possible role of pollinator-mediated hybridization in plant diversification. Increasing evidence suggests that pollinator sharing and hybridization occurs among fig taxa, despite relatively strict coevolution with the pollinating wasp. Using five sympatric dioecious fig taxa and their pollinators, we examine the degree of pollinator sharing and inter-taxa gene flow. We experimentally test pollinator preference for floral volatiles, the main host recognition signal, from different figs. All five fig taxa shared pollinators with other taxa, and gene flow occurred between fig taxa within and between sections. Floral volatiles of each taxon attracted more than one pollinator species. Floral volatiles were more similar between closely related figs, which experienced higher levels of pollinator sharing and inter-taxa gene flow. This study demonstrates that pollinator sharing and inter-taxa gene flow occurs among closely related sympatric dioecious fig taxa and that pollinators choose the floral volatiles of multiple fig taxa. The implications of pollinator sharing and inter-taxa gene flow on diversification, occurring even in this highly specialized obligate pollination system, require further study.
| S-EPMC4843646 | biostudies-literature
Project description:The genus Liriodendron belongs to the family Magnoliaceae, which resides within the magnoliids, an early diverging lineage of the Mesangiospermae. However, the phylogenetic relationship of magnoliids with eudicots and monocots has not been conclusively resolved and thus remains to be determined1-6. Liriodendron is a relict lineage from the Tertiary with two distinct species-one East Asian (L. chinense (Hemsley) Sargent) and one eastern North American (L. tulipifera Linn)-identified as a vicariad species pair. However, the genetic divergence and evolutionary trajectories of these species remain to be elucidated at the whole-genome level7. Here, we report the first de novo genome assembly of a plant in the Magnoliaceae, L. chinense. Phylogenetic analyses suggest that magnoliids are sister to the clade consisting of eudicots and monocots, with rapid diversification occurring in the common ancestor of these three lineages. Analyses of population genetic structure indicate that L. chinense has diverged into two lineages-the eastern and western groups-in China. While L. tulipifera in North America is genetically positioned between the two L. chinense groups, it is closer to the eastern group. This result is consistent with phenotypic observations that suggest that the eastern and western groups of China may have diverged long ago, possibly before the intercontinental differentiation between L. chinense and L. tulipifera. Genetic diversity analyses show that L. chinense has tenfold higher genetic diversity than L. tulipifera, suggesting that the complicated regions comprising east-west-orientated mountains and the Yangtze river basin (especially near 30° N latitude) in East Asia offered more successful refugia than the south-north-orientated mountain valleys in eastern North America during the Quaternary glacial period.
| S-EPMC6784881 | biostudies-literature
Project description:Differences in breeding system are associated with correlated ecological and morphological changes in plants. In Ficus, dioecy and monoecy are strongly associated with different suites of traits (tree height, population density, fruiting frequency, pollinator dispersal ecology). Although approximately 30% of fig species are pollinated by multiple species of fig-pollinating wasps, it has been suggested that copollinators are rare in dioecious figs. Here, we test whether there is a connection between the fig breeding system and copollinator incidence and diversification by conducting a meta-analysis of molecular data from pollinators of 119 fig species that includes new data from 15 Asian fig species. We find that the incidence of copollinators is not significantly different between monoecious and dioecious Ficus. Surprisingly, while all copollinators in dioecious figs are sister taxa, only 32.1% in monoecious figs are sister taxa. We present hypotheses to explain those patterns and discuss their consequences on the evolution of this mutualism.
| S-EPMC4328460 | biostudies-literature
Project description:The specificity of pollinator host choice influences opportunities for reproductive isolation in their host plants. Similarly, host plants can influence opportunities for reproductive isolation in their pollinators. For example, in the fig and fig wasp mutualism, offspring of fig pollinator wasps mate inside the inflorescence that the mothers pollinate. Although often host specific, multiple fig pollinator species are sometimes associated with the same fig species, potentially enabling hybridization between wasp species. Here, we study the 19 pollinator species (Pegoscapus spp.) associated with an entire community of 16 Panamanian strangler fig species (Ficus subgenus Urostigma, section Americanae) to determine whether the previously documented history of pollinator host switching and current host sharing predicts genetic admixture among the pollinator species, as has been observed in their host figs. Specifically, we use genome-wide ultraconserved element (UCE) loci to estimate phylogenetic relationships and test for hybridization and introgression among the pollinator species. In all cases, we recover well-delimited pollinator species that contain high interspecific divergence. Even among pairs of pollinator species that currently reproduce within syconia of shared host fig species, we found no evidence of hybridization or introgression. This is in contrast to their host figs, where hybridization and introgression have been detected within this community, and more generally, within figs worldwide. Consistent with general patterns recovered among other obligate pollination mutualisms (e.g. yucca moths and yuccas), our results suggest that while hybridization and introgression are processes operating within the host plants, these processes are relatively unimportant within their associated insect pollinators.
| S-EPMC9545327 | biostudies-literature
Project description:BackgroundUnderstanding biodiversity patterns and their underlying mechanisms is of interest to ecologists, biogeographers and conservationists and is critically important for conservation efforts. The Indo-Burma hotspot features high species diversity and endemism, yet it also faces significant threats and biodiversity losses; however, few studies have explored the genetic structure and underlying mechanisms of Indo-Burmese species. Here, we conducted a comparative phylogeographic analysis of two closely related dioecious Ficus species, F. hispida and F. heterostyla, based on wide and intensive population sampling across Indo-Burma ranges, using chloroplast (psbA-trnH, trnS-trnG) and nuclear microsatellite (nSSR) markers, as well as ecological niche modeling.ResultsThe results indicated large numbers of population-specific cpDNA haplotypes and nSSR alleles in the two species. F. hispida showed slightly higher chloroplast diversity but lower nuclear diversity than F. heterostyla. Low-altitude mountainous areas of northern Indo-Burma were revealed to have high genetic diversity and high habitat suitability, suggesting potential climate refugia and conservation priority areas. Strong phylogeographic structure and a marked east‒west differentiation pattern were observed in both species, due to the interactions between biotic and abiotic factors. Interspecific dissimilarities at fine-scale genetic structure and asynchronized historical dynamics of east‒west differentiation between species were also detected, which were attributed to different species-specific traits.ConclusionsWe confirm hypothesized predictions that interactions between biotic and abiotic factors largely determine the patterns of genetic diversity and phylogeographic structure of Indo-Burmese plants. The east‒west genetic differentiation pattern observed in two targeted figs can be generalized to some other Indo-Burmese plants. The results and findings of this work will contribute to the conservation of Indo-Burmese biodiversity and facilitate targeted conservation efforts for different species.
| S-EPMC10273766 | biostudies-literature
Project description:Acoustic communication is enabled by the evolution of specialised hearing and sound producing organs. In this study, we performed a large-scale macroevolutionary study to understand how both hearing and sound production evolved and affected diversification in the insect order Orthoptera, which includes many familiar singing insects, such as crickets, katydids, and grasshoppers. Using phylogenomic data, we firmly establish phylogenetic relationships among the major lineages and divergence time estimates within Orthoptera, as well as the lineage-specific and dynamic patterns of evolution for hearing and sound producing organs. In the suborder Ensifera, we infer that forewing-based stridulation and tibial tympanal ears co-evolved, but in the suborder Caelifera, abdominal tympanal ears first evolved in a non-sexual context, and later co-opted for sexual signalling when sound producing organs evolved. However, we find little evidence that the evolution of hearing and sound producing organs increased diversification rates in those lineages with known acoustic communication.
| S-EPMC7532154 | biostudies-literature
Project description:Deeply diverged yet hybridizing species provide a system to investigate the final stages of the speciation process. We study a hybridizing pair of salamander species-the morphologically and genetically drastically different newts Triturus cristatus and T. marmoratus-with a panel of 32 nuclear and mitochondrial genetic markers. Morphologically identified hybrids are mostly of the F1 generation and mothered by T. cristatus. The sex ratio of the F1 hybrid class is reciprocally skewed, with a preponderance of females in T. cristatus-mothered hybrids and males in T. marmoratus-mothered hybrids. This amounts to the Haldane effect operating in one direction of the cross. Deeper generation hybrids are occasionally produced, possibly including F1 hybrid × backcross hybrid offspring. Interspecific gene flow is low, yet skewed toward T. cristatus. This asymmetry may be caused by hybrid zone movement, with the superseding species being predisposed to introgression. The persisting gene flow between deeply differentiated species supports the notion that full genetic isolation may be selected against. Conversely, published morphological data suggest that introgressive hybridization is detrimental, with digital malformations occurring more frequently in the area of sympatry. Finally, to assist field identification, both within the area of natural range overlap and concerning anthropogenic introductions elsewhere, we document the phenotypical variation of two generations of hybrids compared with both parental species. We suggest that fluctuating range boundaries, ecological segregation, cytonuclear incompatibilities and hybrid breakdown through Bateson-Dobzhansky-Muller incompatibilities all contribute to species integrity, despite incomplete isolation during secondary contact.
| S-EPMC8674889 | biostudies-literature