Comparative transcriptomics and gene expression divergence associated with homoploid hybrid speciation in Argyranthemum.

Ecological isolation is increasingly thought to play an important role in speciation, especially for the origin and reproductive isolation of homoploid hybrid species. However, the extent to which divergent and/or transgressive gene expression changes are involved in speciation is not well studied. In this study, we employ comparative transcriptomics to investigate gene expression changes associated with the origin and evolution of two homoploid hybrid plant species, Argyranthemum sundingii and A. lemsii (Asteraceae). As there is no standard methodology for comparative transcriptomics, we examined five different pipelines for data assembly and analysing gene expression across the four species (two hybrid and two parental). We note biases and problems with all pipelines, and the approach used affected the biological interpretation of the data. Using the approach that we found to be optimal, we identify transcripts showing DE between the parental taxa and between the homoploid hybrid species and their parents; in several cases, putative functions of these DE transcripts have a plausible role in ecological adaptation and could be the cause or consequence of ecological speciation. Although independently derived, the homoploid hybrid species have converged on similar expression phenotypes, likely due to adaptation to similar habitats.

Maintenance and expansion of genetic and trait variation following domestication in a clonal crop.

Clonal propagation enables favourable crop genotypes to be rapidly selected and multiplied. However, the absence of sexual propagation can lead to low genetic diversity and accumulation of deleterious mutations, which may eventually render crops less resilient to pathogens or environmental change. To better understand this trade-off, we characterize the domestication and contemporary genetic diversity of Enset (Ensete ventricosum), an indigenous African relative of bananas (Musa) and a principal starch staple for 20 million Ethiopians. Wild enset reproduction occurs strictly by sexual outcrossing, but for cultivation, it is propagated clonally and associated with diversification and specialization into hundreds of named landraces. We applied tGBS sequencing to generate genome-wide genotypes for 192 accessions from across enset's cultivated distribution, and surveyed 1340 farmers on enset agronomic traits. Overall, reduced heterozygosity in the domesticated lineage was consistent with a domestication bottleneck that retained 37% of wild diversity. However, an excess of putatively deleterious missense mutations at low frequency present as heterozygotes suggested an accumulation of mutational load in clonal domesticated lineages. Our evidence indicates that the major domesticated lineages initially arose through historic sexual recombination associated with a domestication bottleneck, followed by the amplification of favourable genotypes through an extended period of clonal propagation. Among domesticated lineages, we found a significant phylogenetic signal for multiple farmer-identified food, nutrition and disease resistance traits and little evidence of contemporary recombination. The development of future-climate adapted genotypes may require crop breeding, but outcrossing risks exposing deleterious alleles as homozygotes. This trade-off may partly explain the ubiquity and persistence of clonal propagation over recent centuries of comparative climate stability.

The role of geography, ecology, and hybridization in the evolutionary history of Canary Island Descurainia.

PREMISE: Oceanic islands offer the opportunity to understand evolutionary processes underlying rapid diversification. Along with geographic isolation and ecological shifts, a growing body of genomic evidence has suggested that hybridization can play an important role in island evolution. Here we use genotyping-by-sequencing (GBS) to understand the roles of hybridization, ecology, and geographic isolation in the radiation of Canary Island Descurainia (Brassicaceae). METHODS: We carried out GBS for multiple individuals of all Canary Island species and two outgroups. Phylogenetic analyses of the GBS data were performed using both supermatrix and gene tree approaches and hybridization events were examined using D-statistics and Approximate Bayesian Computation. Climatic data were analyzed to examine the relationship between ecology and diversification. RESULTS: Analysis of the supermatrix data set resulted in a fully resolved phylogeny. Species networks suggest a hybridization event has occurred for D. gilva, with these results being supported by Approximate Bayesian Computation analysis. Strong phylogenetic signals for temperature and precipitation indicate one major ecological shift within Canary Island Descurainia. CONCLUSIONS: Inter-island dispersal played a significant role in the diversification of Descurainia, with evidence of only one major shift in climate preferences. Despite weak reproductive barriers and the occurrence of hybrids, hybridization appears to have played only a limited role in the diversification of the group with a single instance detected. The results highlight the need to use phylogenetic network approaches that can simultaneously accommodate incomplete lineage sorting and gene flow when studying groups prone to hybridization; patterns that might otherwise be obscured in species trees.

Geographical isolation, habitat shifts and hybridisation in the diversification of the Macaronesian endemic genus Argyranthemum (Asteraceae).

Inferring the processes responsible for the rich endemic diversity of oceanic island floras is important for our understanding of plant evolution and setting practical conservation priorities. This requires an accurate knowledge of phylogenetic relationships, which have often been difficult to resolve due to a lack of genetic variation. We employed genotyping-by-sequencing (GBS) to investigate how geographical isolation, habitat shifts, and hybridisation have contributed to the evolution of diversity observed in Argyranthemum Webb (Asteraceae), the largest genus of flowering plants endemic to the Macaronesian archipelagos. Species relationships were resolved, and biogeographical stochastic mapping identified intra-island speciation as the most frequent biogeographic process underlying diversification, contrary to the prevailing view in Argyranthemum and the Canary Islands. D-statistics revealed significant evidence of hybridisation between lineages co-occurring on the same island, however there was little support for the hypothesis that hybridisation may be responsible for the occurrence of nonmonophyletic multi-island endemic (MIE) species. Geographic isolation, habitat shifts and hybridisation have all contributed to the diversification of Argyranthemum, with intra-island speciation found to be more frequent than previously thought. Morphological convergence is also proposed to explain the occurrence of nonmonophyletic MIE species. This study reveals greater complexity in the evolutionary processes generating Macaronesian endemic diversity.

Independent homoploid hybrid speciation events in the Macaronesian endemic genus Argyranthemum.

Well-characterized examples of homoploid hybrid speciation (HHS) are rare in nature, yet they offer the potential to study a number of evolutionary processes. In this study, we investigate putative homoploid hybrid species in the genus Argyranthemum (Asteraceae), a group of plants endemic to the Macaronesian archipelagos of the North Atlantic Ocean. We specifically address a number of knowledge gaps surrounding the origin(s) of A. sundingii and A. lemsii, which are thought to be derived from the same parental cross. Comparisons of leaf morphology suggest that A. sundingii and A. lemsii are distinct from their parental progenitors and distinguishable from each other based on leaf area. Ecological niche modelling (ENM) demonstrated that the homoploid hybrid species occupy novel habitats that are intermediate relative to the parental species. Nuclear simple sequence repeat markers (SSRs) and single nucleotide polymorphism (SNP) data indicate that the homoploid hybrid species are distinct from the parental taxa, while population-level sampling of chloroplast SSRs and approximate Bayesian computation show that A. sundingii and A. lemsii are independently derived from the same parental cross. As such, Argyranthemum represents an example of independent homoploid hybrid speciation events with evidence of divergence in leaf morphology and adaptation to novel intermediate habitats. On oceanic islands, which are often typified by steep ecological gradients and inhabited by recently derived species with weak reproductive barriers, multiple HHS events from the same parental cross are not only possible but also likely to have played a more important role in oceanic island radiations than we currently think.

Transcriptome sequencing and simple sequence repeat marker development for three Macaronesian endemic plant species.

PREMISE OF THE STUDY: Oceanic islands offer unparalleled opportunities to investigate evolutionary processes such as adaptation and speciation. However, few genomic resources are available for oceanic island endemics. In this study, we publish transcriptome sequences from three Macaronesian endemic plant species (Argyranthemum broussonetii [Asteraceae], Descurainia bourgaeana [Brassicaceae], and Echium wildpretii [Boraginaceae]) that are representative of lineages that have radiated in the region. In addition, the utility of transcriptome data for marker development is demonstrated. METHODS AND RESULTS: Transcriptomes from the three plant species were sequenced, assembled, and annotated. Between 1972 and 2282 simple sequence repeats (SSRs) were identified for each taxon. Primers were designed and tested for 30 of the candidate SSRs identified in Argyranthemum, of which 12 amplified well across three species and eight were polymorphic. CONCLUSIONS: We demonstrate here that a single transcriptome sequence is sufficient to identify hundreds of polymorphic SSR markers. The SSRs are applicable to a wide range of questions relating to the evolution of island lineages.