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Premise: Cultivation and naturalization of plants beyond their natural range can bring previously geographically isolated taxa together, increasing the opportunity for hybridization, the outcomes of which are not predictable. Here, we explored the phenotypic and genomic effects of interspecific gene flow following the widespread cultivation of Mentha spicata (spearmint), M. longifolia, and M. suaveolens. Methods: We morphologically evaluated 155 herbarium specimens of three Mentha species and sequenced the genomes of a subset of 93 specimens. We analyzed the whole genomes in a population and the phylogenetic framework and associated genomic classifications in conjunction with the morphological assessments. Results: The allopolyploid M. spicata, which likely evolved in cultivation, had altered trichome characters, that is possibly a product of human selection for a more palatable plant or a byproduct of selection for essential oils. There were signs of genetic admixture between mints, including allopolyploids, indicating that the reproductive barriers between Mentha species with differences in ploidy are likely incomplete. Still, despite gene flow between species, we found that genetic variants associated with the cultivated trichome morphology continue to segregate. Conclusions: Although hybridization, allopolyploidization, and human selection during cultivation can increase species richness (e.g., by forming hybrid taxa), we showed that unless reproductive barriers are strong, these processes can also result in mixing of genes between species and the potential loss of natural biodiversity.

Conservation and restoration planning of extremely rare species relies on an understanding of the genetic diversity and population dynamics within a species to overcome potential inbreeding depression. Nānū or Nāʻū (Gardenia remyi H. Mann.) is an endemic tree native to the Hawaiian Islands and is one of more than 200 endangered plant species in Hawaiʻi with less than 50 individuals remaining in the wild. Efforts to understand the genetic diversity and connectivity between wild populations are foundational to conservation management plans, however little is known of the population structure of the species. In this study we utilize double digest restriction-site associated sequencing (ddRADSeq) on both historical herbarium specimens and samples from living ex situ collections to: (1) Test the hypothesis that we can capture genetic diversity in herbarium material of G. remyi using ddRADSeq, and (2) test the hypothesis that there are genetically distinct populations or subpopulation units among different Hawaiian islands. Usable sequencing data from thirty-seven samples of herbarium specimens collected between 1952 and 2017 and twenty wild sourced living collection samples were obtained representing all four islands where G. remyi is known to occur. Phylogenetic and population structure analysis revealed a monophyletic ingroup and a clear division between G. remyi samples of the northern island of Kauaʻi and those from the more southeastern younger islands of Molokaʻi, Maui and Hawaiʻi islands. The Kauaʻi samples were further split into a subpopulation from Southern Kauaʻi and the subpopulations from Northern Kauaʻi. Some admixed samples were detected. Our results are consistent with subpopulations of G. remyi, which needs to be considered in future conservation planning and breeding efforts to minimize inbreeding depression.

Ecotypes are distinct populations within a species that are adapted to specific environmental conditions. Understanding how these ecotypes become established, and how they interact when reunited, is fundamental to elucidating how ecological adaptations are maintained. This study focuses on Themeda triandra, a dominant grassland species across Asia, Africa and Australia. It is the most widespread plant in Australia, where it has distinct ecotypes that are usually restricted to either wetter and cooler coastal regions or the drier and hotter interior. We generate a reference genome for T. triandra and use whole genome sequencing for over 80 Themeda accessions to reconstruct the evolutionary history of T. triandra and related taxa. Organelle phylogenies confirm that Australia was colonized by T. triandra twice, with the division between ecotypes predating their arrival in Australia. The nuclear genome provides evidence of differences in the dominant ploidal level and gene-flow among the ecotypes. In northern Queensland there appears to be a hybrid zone between ecotypes with admixed nuclear genomes and shared chloroplast haplotypes. Conversely, in the cracking claypans of Western Australia, there is cytonuclear discordance with individuals possessing the coastal chloroplast and interior clade nuclear genome. This chloroplast capture is potentially a result of adaptive introgression, with selection detected in the rpoC2 gene which is associated with water use efficiency. The reason that T. triandra is the most widespread plant in Australia appears to be a result of distinct ecotypic genetic variation and genome duplication, with the importance of each depending on the geographic scale considered.

Ecotypes are distinct populations within a species that are adapted to specific environmental conditions. Understanding how these ecotypes become established, and how they interact when reunited, is fundamental to elucidating how ecological adaptations are maintained. This study focuses on Themeda triandra, a dominant grassland species across Asia, Africa and Australia. It is the most widespread plant in Australia, where it has distinct ecotypes that are usually restricted to either wetter and cooler coastal regions or the drier and hotter interior. We generate a reference genome for T. triandra and use whole genome sequencing for over 80 Themeda accessions to reconstruct the evolutionary history of T. triandra and related taxa. Organelle phylogenies confirm that Australia was colonized by T. triandra twice, with the division between ecotypes predating their arrival in Australia. The nuclear genome provides evidence of differences in the dominant ploidal level and gene-flow among the ecotypes. In northern Queensland there appears to be a hybrid zone between ecotypes with admixed nuclear genomes and shared chloroplast haplotypes. Conversely, in the cracking claypans of Western Australia, there is cytonuclear discordance with individuals possessing the coastal chloroplast and interior clade nuclear genome. This chloroplast capture is potentially a result of adaptive introgression, with selection detected in the rpoC2 gene which is associated with water use efficiency. The reason that T. triandra is the most widespread plant in Australia appears to be a result of distinct ecotypic genetic variation and genome duplication, with the importance of each depending on the geographic scale considered.

The genus Mentha is taxonomically and phylogenetically challenging due to complex genomes, polyploidization and an extensive historical nomenclature, potentially hiding cryptic taxa. A straightforward interpretation of phylogenetic relationships within the section Mentha is further hindered by dominant but outdated concepts on historically identified hybrid taxa. Mentha spicata is traditionally considered to be of hybrid origin, but the evidence for this is weak. Here, we aim to understand the phylogenetic relationships within the section Mentha using large sample sizes and to revisit the hybrid status and identity of M. spicata. We show that two of three traditional species in the subsection Spicatae are polyphyletic, as is the subsection as a whole, while the real number of cryptic species was underestimated. Compared to previous studies we present a fundamentally different phylogeny, with a basal split between M. spicata s.s. and M. longifolia s.s. Cluster analyses of morphological and genotypic data demonstrate that there is a dissociation between morphologically and genotypically defined groups of samples. We did not find any evidence that M. spicata is of hybrid origin, and we conclude its taxonomic status should be revised. The combination of genetic and phenotypic information is essential when evaluating hyperdiverse taxonomic groups.

Geographical isolation facilitates the emergence of distinct phenotypes within a single species, but reproductive barriers or selection are needed to maintain the polymorphism after secondary contact. Here, we explore the processes that maintain intraspecific variation of C4 photosynthesis, a complex trait that results from the combined action of multiple genes. The grass Alloteropsis semialata includes C4 and non-C4 populations, which have coexisted as a polyploid series for more than 1 million years in the miombo woodlands of Africa. Using population genomics, we show that there is genome-wide divergence for the photosynthetic types, but the current geographical distribution does not reflect a simple habitat displacement scenario as the genetic clusters overlap, being occasionally mixed within a given habitat. Despite evidence of recurrent introgression between non-C4 and C4 groups, in both diploids and polyploids, the distinct genetic lineages retain their identity, potentially because of selection against hybrids. Coupled with strong isolation by distance within each genetic group, this selection created a geographical mosaic of photosynthetic types. Diploid C4 and non-C4 types never grew together, and the C4 type from mixed populations constantly belonged to the hexaploid lineage. By limiting reproductive interactions between photosynthetic types, the ploidy difference probably allows their co-occurrence, reinforcing the functional diversity within this species. Together, these factors enabled the persistence of divergent physiological traits of ecological importance within a single species despite gene flow and habitat overlap.

C 4 photosynthesis evolved multiple times independently in angiosperms, but most origins are relatively old so that the early events linked to photosynthetic diversification are blurred. The grass Alloteropsis semialata is an exception, as this species encompasses C 4 and non-C 4 populations. Using phylogenomics and population genomics, we infer the history of dispersal and secondary gene flow before, during and after photosynthetic divergence in A. semialata. We further analyse the genome composition of individuals with varied ploidy levels to establish the origins of polyploids in this species. Detailed organelle phylogenies indicate limited seed dispersal within the mountainous region of origin and the emergence of a C 4 lineage after dispersal to warmer areas of lower elevation. Nuclear genome analyses highlight repeated secondary gene flow. In particular, the nuclear genome associated with the C 4 phenotype was swept into a distantly related maternal lineage probably via unidirectional pollen flow. Multiple intraspecific allopolyploidy events mediated additional secondary genetic exchanges between photosynthetic types. Overall, our results show that limited dispersal and isolation allowed lineage divergence, with photosynthetic innovation happening after migration to new environments, and pollen-mediated gene flow led to the rapid spread of the derived C 4 physiology away from its region of origin.

Evidence of eukaryote-to-eukaryote lateral gene transfer (LGT) has accumulated in recent years, but the selective pressures governing the evolutionary fate of these genes within recipient species remain largely unexplored. Among non-parasitic plants, successful LGT has been reported between different grass species. Here, we use the grass Alloteropsis semialata, a species that possesses multigene LGT fragments that were acquired recently from distantly related grass species, to test the hypothesis that the successful LGT conferred an advantage and were thus rapidly swept into the recipient species. Combining whole-genome and population-level RAD sequencing, we show that the multigene LGT fragments were rapidly integrated in the recipient genome, likely due to positive selection for genes encoding proteins that added novel functions. These fragments also contained physically linked hitchhiking protein-coding genes, and subsequent genomic erosion has generated gene presence-absence polymorphisms that persist in multiple geographic locations, becoming part of the standing genetic variation. Importantly, one of the hitchhiking genes underwent a secondary rapid spread in some populations. This shows that eukaryotic LGT can have a delayed impact, contributing to local adaptation and intraspecific ecological diversification. Therefore, while short-term LGT integration is mediated by positive selection on some of the transferred genes, physically linked hitchhikers can remain functional and augment the standing genetic variation with delayed adaptive consequences.

C4 photosynthesis is a complex trait that boosts productivity in tropical conditions. Compared to C3 species, the C4 state seems to require numerous novelties, but species comparisons can be confounded by long divergence times. Here, we exploit the photosynthetic diversity that exists within a single species, the grass Alloteropsis semialata, to detect changes in gene expression associated with different photosynthetic phenotypes. Phylogenetically-informed comparative transcriptomics show that intermediates with a weak C4 cycle are separated from the C3 phenotype by increases in the expression of 58 genes (0.22% of genes expressed in the leaves), including those encoding just three core C4 enzymes: ASP-AT, PCK, and PEPC. The subsequent transition to full C4 physiology was accompanied by increases in another 15 genes (0.06%), including only the core C4 enzyme PPDK. These changes likely created a rudimentary C4 physiology, and isolated populations subsequently improved this emerging C4 physiology, resulting in a patchwork of expression for some C4-accessory genes. Our work shows how C4 assembly in A. semialata happened in incremental steps, each requiring few alterations over the previous one. These create short bridges across adaptive landscapes that likely facilitated the recurrent origins of C4 photosynthesis through a gradual process of evolution.

C4 photosynthesis is a complex trait that boosts productivity in warm environments. Paradoxically, it evolved independently in numerous plant lineages, despite requiring specialised leaf anatomy. The anatomical modifications underlying C4 evolution have previously been evaluated through interspecific comparisons, which capture numerous changes besides those needed for C4 functionality. Here, we quantify the anatomical changes accompanying the transition between non‐C4 and C4 phenotypes by sampling widely across the continuum of leaf anatomical traits in the grass Alloteropsis semialata. Within this species, the only trait that is shared among and specific to C4 individuals is an increase in vein density, driven specifically by minor vein development that yields multiple secondary effects facilitating C4 function. For species with the necessary anatomical preconditions, developmental proliferation of veins can therefore be sufficient to produce a functional C4 leaf anatomy, creating an evolutionary entry point to complex C4 syndromes that can become more specialised.

A fundamental tenet of multicellular eukaryotic evolution is that vertical inheritance is paramount, with natural selection acting on genetic variants transferred from parents to offspring. This lineal process means that an organism's adaptive potential can be restricted by its evolutionary history, the amount of standing genetic variation, and its mutation rate. Lateral gene transfer (LGT) theoretically provides a mechanism to bypass many of these limitations, but the evolutionary importance and frequency of this process in multicellular eukaryotes, such as plants, remains debated. We address this issue by assembling a chromosome-level genome for the grass Alloteropsis semialata, a species surmised to exhibit two LGTs, and screen it for other grass-to-grass LGTs using genomic data from 146 other grass species. Through stringent phylogenomic analyses, we discovered 57 additional LGTs in the A. semialata nuclear genome, involving at least nine different donor species. The LGTs are clustered in 23 laterally acquired genomic fragments that are up to 170 kb long and have accumulated during the diversification of Alloteropsis. The majority of the 59 LGTs in A. semialata are expressed, and we show that they have added functions to the recipient genome. Functional LGTs were further detected in the genomes of five other grass species, demonstrating that this process is likely widespread in this globally important group of plants. LGT therefore appears to represent a potent evolutionary force capable of spreading functional genes among distantly related grass species.