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Schley, R. J.

Publications and source records attributed to Schley, R. J..

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Hybridisation and herbivory fuel Amazonian tree radiations

Tropical rainforests, and Amazonia in particular, contain more tree species than anywhere else, most of which arose through rapid evolutionary radiations 1-3. Rapid radiations are often catalysed by ecological opportunity 4-6, which in rainforest trees is presented by intense insect herbivore pressure, spurring the evolution of novel plant defence chemistry to escape it 7. However, we do not understand how long-lived trees can adapt quickly enough to keep pace with rapidly-evolving insect herbivores. Here we show that hybridisation in rainforest trees, which was considered rare, allows exchange of gene clusters used in chemical defence against herbivore attack, facilitating rapid adaptation and diversification. Using genome sequencing for 461 individuals from the genus Inga, a characteristic Amazonian tree radiation, we find that regional tree communities form syngameons - networks of closely related, co-occurring species connected by gene flow. Integrating these genomes with herbivore abundance data from the same communities across the tropical Americas, we show that herbivore compositional turnover coincides with local, recurrent interspecific transfer of defence gene clusters that are retained by balancing selection, consistent with fluctuating selective pressure imposed by shifting herbivore communities. Together, our results demonstrate that hybridisation allows long-lived tropical trees to rapidly evolve chemical defences, fuelling adaptation to the relentless insect herbivory that structures the worlds most species-rich forests.

evolutionary biology↗

The frequency and importance of polyploidy in tropical rainforest tree radiations

O_LIThe presence of two or more copies of the genome in an organism, termed polyploidy, is a crucial force in plant evolution, generating genetic, phenotypic and ecological diversity. The Amazonian tree flora is the most species-rich on Earth, and largely arose as a result of rapid evolutionary radiations. While polyploidy is an important catalyst of rapid radiations, it remains poorly studied in tropical tree radiations. C_LIO_LIWe examined ploidy variation across Inga (Fabaceae), a characteristic Amazonian tree radiation, using DNA sequence data from 1305 loci for 189/282 Inga species. We then tested whether polyploid species experience more positive selection than diploids, particularly in loci underlying chemical defence against herbivory, which is a key ecological pressure affecting rainforest tree diversification. C_LIO_LIWe show that tetraploidy occurs in 14% (N=27) of the Inga species we sequenced, with several widespread species showing geographical ploidy variation, alongside minimal phylogenetic signal in ploidy which suggests recurrent polyploidisation. Interestingly, we found more loci under selection in polyploids than diploids, most notably in chemical defence loci. C_LIO_LIOur results show that polyploidy has arisen independently in several Inga species, and that polyploidisation can lead to elevated selection in chemical defence, helping to shape ecological interactions and influence diversification in Inga. C_LI

evolutionary biology↗

Genomic stability in the Galapagos Scalesia adaptive radiation: Consistent transposable element accumulation despite hybridization and ecological niche shifts

Transposable elements (TEs) have been hypothesized to play a pivotal role in driving diversification by facilitating the emergence of novel phenotypes and the accumulation of divergence between species. Hybridization and adaptation to novel niches are hypothesized to influence TE accumulation in genomes by disrupting genomic regulation, including the suppression of TE replication. The rapid speciation and ecological diversification characteristic of adaptive radiations offer a unique opportunity to examine the link between TE accumulation and speciation, diversification, hybridization and adaptation. Here, focusing on all 15 species of the genus Scalesia (Asteraceae), a radiation endemic to the Galapagos Islands, we test whether hybridization or shifts in ecological niche are associated with changes in TE accumulation in genomes. Our analyses reveal little to no variation in TE accumulation among Scalesia species nor its hybrid populations. Shifts in ecological niches, linked to climatic variation, did not result in discernible changes in TE accumulation, a surprising finding given the anticipated selective pressure imposed by aridity, a factor often linked to genome size reduction. We found no distinct patterns in the temporal accumulation of TEs, and no effects at the class or superfamily level. Our findings challenge the assertion that TEs have directly driven diversification, speciation and local adaptation. Instead, we suggest that TEs may simply be along for the ride, rather than actively contributing to plant diversification.

evolutionary biology↗

Do Reticulate Relationships Between Tropical Trees Drive Diversification? Insights from Inga (Fabaceae)

Evolutionary radiations underlie much of the species diversity of life on Earth, particularly within the worlds most species-rich tree flora - that of the Amazon rainforest. Hybridisation occurs in many radiations, with effects ranging from homogenisation of species to generation of genetic and phenotypic novelty that fuels speciation, but the influence of hybridisation on Amazonian tree radiations has been little studied. We address this using the ubiquitous, species-rich, neotropical tree genus Inga, which typifies rapid radiations of rainforest trees. We assess patterns of gene tree incongruence to ascertain whether hybridisation was associated with rapid radiation in Inga. Given the importance of insect herbivory in structuring rainforest tree communities (and hence the potential for hybridisation to promote adaptation through admixture of defence traits), we also test whether introgression of loci underlying chemical defences against herbivory occurred during the radiation of Inga. Our phylogenomic analyses of 189/288 Inga species using >1300 target capture loci showed widespread introgression in Inga. Specifically, we found widespread phylogenetic incongruence explained by introgression, with phylogenetic networks recovering multiple introgression events across Inga and up to 20% of shared, likely introgressed, genetic variation between some species. In addition, most defence chemistry loci showed evidence of positive selection and marginally higher levels of introgression. Overall, our results suggest that introgression has occurred widely over the course of Ingas history, likely facilitated by extensive dispersal across Amazonia, and that in some cases introgression of chemical defence loci may influence adaptation in Inga.

evolutionary biology↗

The Ecology of Palm Genomes: Repeat-associated genome size expansion is constrained by aridity

O_LIGenome size varies 2,400-fold across plants, influencing their evolution through changes in cell size and cell division rates which impact plants environmental stress tolerance. Repetitive element expansion explains much genome size diversity, and the processes structuring repeat communities are analogous to those structuring ecological communities. However, which environmental stressors influence repeat community dynamics has not yet been examined from an ecological perspective. C_LIO_LIWe measured genome size and leveraged climatic data for 91% of genera within the ecologically diverse palm family (Arecaceae). We then generated genomic repeat profiles for 141 palm species, and analysed repeats using phylogenetically-informed linear models to explore relationships between repeat dynamics and environmental factors. C_LIO_LIWe show that palm genome size and repeat community composition are best explained by aridity. Specifically, EnSpm CACTA repeats were more abundant in palm species from wetter environments, which generally had larger genomes (>2.15Gbp/1C), suggesting amplification. In contrast, Ty1-copia Angela elements were more abundant in drier environments. C_LIO_LIOur results suggest water stress inhibits the expansion of repeats through selection on upper genome size limits. However, Ty1-copia Angela elements, which may associate with stress-response genes, have amplified in arid-adapted palm species. Overall, we provide novel evidence of climate influencing the assembly of repeat communities. C_LI

evolutionary biology↗

The diversification of Pterocarpus (Leguminosae: Papilionoideae) was influenced by biome-switching and infrequent long-distance dispersal

AimPhenotypes which evolved for dispersal over ecological timescales may lead to significant macroevolutionary consequences, such as infrequent long-distance dispersal and diversification in novel biomes. We aimed to reconstruct the phylogenetic history of Pterocarpus (Leguminosae/ Fabaceae) to assess whether seed dispersal phenotypes and biome switching explain the current biogeographical patterns of this group. LocationPantropical TaxonThe Pterocarpus clade, particularly Pterocarpus (Leguminosae/Fabaceae) MethodsWe sequenced ~300 nuclear loci captured using Angiosperms-353, a genomic bait set for flowering plants, from which we generated a time-calibrated phylogenomic tree. To corroborate this, we also generated a time-calibrated phylogenetic tree from data-mined Sanger-sequencing data. We then collated distribution data and fruit dispersal morphology traits to compare trait-dependent and trait-independent biogeographical models, allowing us to assess whether dispersal traits influenced the spatio-temporal evolution of Pterocarpus. Finally, using the results of these model tests, we estimated the ancestral ranges and biomes of Pterocarpus species to better understand their biogeographical history, and assessed the degree and direction of biome switching over the course of Pterocarpus diversification history. ResultsWe recovered well-supported phylogenetic relationships within Pterocarpus, within which there were two subclades - one Neotropical and the other Palaeotropical. Our divergence date estimates suggested that Pterocarpus largely diversified from around 12 Ma, during the Miocene. Trait-dependent biogeographical models were rejected for both range and biome evolution within Pterocarpus, but models parameterising dispersal were supported. Pterocarpus ancestral node shared a range across the new-world and old-world tropics, followed by divergence into two clades, one palaeotropical and one neotropical. Biome switching occurred most frequently into rainforest and grassland. Main conclusionsOverall, our analyses suggest that Pterocarpus underwent infrequent cross-continental dispersal and establishment into novel biomes. While this was minimally impacted by fruit dispersal syndromes, biome switching precipitated by long-distance dispersal and environmental change have played an important role in diversification within Pterocarpus since the Miocene.

evolutionary biology↗

Archaeogenomics of a ~2,100-year-old Egyptian leaf provides a new timestamp on date palm domestication

O_LIThe date palm (Phoenix dactylifera) has been a cornerstone of Middle Eastern and North African agriculture for millennia. It is presumed that date palms were first domesticated in the Persian Gulf and subsequently introduced into North Africa, where their evolution in the latter region appears to have been influenced by gene flow from the wild relative P. theophrasti, which is restricted to Crete and Turkey. However, the timing of gene flow from P. theophrasti to P. dactylifera remains unknown due to the limited archaeobotanical evidence of P. theophrasti and their exclusion from population genomic studies. C_LIO_LIWe addressed this issue by investigating the relatedness and ancestry of a ~2,100-year-old P. dactylifera leaf from Saqqara (Egypt), combining genome sequencing of this ancient specimen with a broad sample of date palm cultivars and closely related species. C_LIO_LIThe ancient Saqqara date palm shares close genetic ancestry with North African date palm populations. We find clear genomic admixture between the Saqqara date palm, P. theophrasti and the closest known relative P. sylvestris. C_LIO_LIOur study highlights that gene flow from P. theophrasti and P. sylvestris to North African date palms had already occurred at least ~2,100 years ago, providing a minimum timestamp for hybridisation between species. C_LI

evolutionary biology↗

Introgression in Brownea suggests that reticulate evolution contributes to Amazonian tree diversity

Hybridization has the potential to generate or homogenize biodiversity and is a particularly common phenomenon in plants, with an estimated 25% of species undergoing inter-specific gene flow. However, hybridization in Amazonias megadiverse tree flora was assumed to be extremely rare despite extensive sympatry between closely related species, and its role in diversification remains enigmatic because it has not yet been examined empirically. Using members of a dominant Amazonian tree family (Brownea, Fabaceae) as a model to address this knowledge gap, our study recovered extensive evidence of hybridization among multiple lineages across phylogenetic scales. More specifically, our results uncovered several historical introgression events between Brownea lineages and indicated that gene tree incongruence in Brownea is best explained by introgression, rather than solely by incomplete lineage sorting. Furthermore, investigation of recent hybridization using [~]19,000 ddRAD loci recovered a high degree of shared variation between two Brownea species which co-occur in the Ecuadorian Amazon. Our analyses also showed that these sympatric lineages exhibit homogeneous rates of introgression among loci relative to the genome-wide average, implying a lack of selection against hybrid genotypes and a persistence of hybridization over time. Our results demonstrate that gene flow between multiple Amazonian tree species has occurred across temporal scales, and contrasts with the prevailing view of hybridizations rarity in Amazonia. Overall, our results provide novel evidence that reticulate evolution influenced diversification in part of the Amazonian tree flora, which is the most diverse on Earth.

evolutionary biology↗