By Jia Hua Wang
With over 300,000 extant species, flowering plants, or angiosperms, form ca. 90% of all terrestrial vegetation, making them the most ecologically diverse and abundant land plants (Soltis & Soltis, 2014). Apart from taigas and temperate rainforests, angiosperms dominate nearly all terrestrial ecosystems and have representatives in many aquatic environments (Feild & Arens, 2005). By serving as primary producers, angiosperms play a vital role in ecosystem functioning, and many biological lineages have diversified alongside angiosperms and the ecosystems that they have created (Magallón et al., 2015). However, in spite of their present abundance, fossil records suggest the rise of angiosperms was a geologically recent event, occurring in the Early Cretaceous period (ca. 135 million years ago) (Feild & Arens, 2005). The sudden origin and rapid diversification of angiosperms was characterized by Charles Darwin as “an abominable mystery”, for it potentially undermined his theory of gradual evolution by natural selection (Crepet, 2000). Presently, the integration of palaeobotany, phylogenetics and other related fields has facilitated myriad elucidations regarding the evolutionary success of angiosperms (Soltis & Soltis, 2014). Specifically, these methods have allowed researchers to gain insight into the evolutionary origin of angiosperms and the key innovations that led to their successful radiation.
Whole genome duplication (WGD), or polyploidization, is a relatively common occurrence in plant genomes that results in variations in genomic size and content which may produce novel phenotypes and/or patterns of gene expression (Soltis & Soltis, 2016). Notably, polyploidy is most prevalent in angiosperms as compared to other land plants, and 15% of angiosperm speciation events are estimated to be a result of a change in ploidy (Dodsworth, Chase & Leitch, 2016). A recent study on 106 unambiguous WGD events in the angiosperm phylogeny showed that 46 were closely linked to increased diversification, with higher speciation rates in succeeding rounds of WGD events (Landis et al., 2018).
To gain insight into angiosperm evolution, the Amborella Genome Project was carried out to sequence the genome of Amborella trichopoda, which forms putatively the most basal lineage of extant angiosperms (Amborella Genome Project, 2013). Being the sister group to all other extant angiosperms, coupled with the lack of recent lineage-specific duplications detected in its genome, A. trichopoda is an excellent fit for inferring the genomic content of the last common ancestor (LCA) of extant angiosperms (Jiao et al., 2011). Additionally, comparative genomic analyses of the A. trichopoda genome with those of other angiosperms assist in interpreting the effects of further genomic variations in different lineages. Results of the project suggest that the first angiosperm evolved from a WGD event around 160 million years ago which introduced new gene families that served as fodder for early diversification (Amborella Genome Project, 2013).
While most duplicated genes following a WGD event become non-functional (and subsequently lost), evolutionary novelties may arise via subfunctionalization or neofunctionalization. Subfunctionalization occurs when duplicated genes, or paralogs, specialize in a subset of ancestral functions, while neofunctionalization results in novel functions due to coding or regulatory changes (Moriyama & Koshiba-Takeuchi, 2018). Key innovations refer to novel phenotypic traits which lead to the radiation and success of a taxonomic group, and a critical one that arose in angiosperms is the origin of the flower catalyzed by an ancient WGD event (Soltis & Soltis, 2016). Duplication of MADS-box genes and subfunctionalization of the resulting paralogous gene copies form the transcription factor complexes involved in flower development via the ABC model (Dodsworth, Chase & Leitch, 2016). It is important to note that the origin of the flower was not solely due to the formation of novel floral genes, as more than 70% of genes with known function in floral structures, flowering time or other regulatory pathways were found in the LCA of all extant seed plants, including gymnosperms. This suggests that many pre-existing genes were recruited and later designated floral functions (Amborella Genome Project, 2013).
Significantly, these ancestral WGD events resulted in the diversification of regulatory genes critical to seed and flower development. However, they alone may not be sufficient to account for the rise and eventual dominance of angiosperms. Presently, angiosperm diversification is also attributed to changing climate conditions, migrations events, evolutionary arms races (e.g. herbivory) and co-radiation between pollinator and plant host (Schranz, Mohammadin & Edger, 2012). The availability of diverse ecological areas for colonization and expansion also plays a significant role in what is known as diversity-dependent diversification (Vamosi & Vamosi, 2010).
Following the formation of flowers, insect pollination became widely regarded as the dominant pollination mode in angiosperms during the Early Cretaceous period, with 86% of basal extant angiosperm families containing species that are zoophilous (i.e. animal-pollinated). This is further supported by the study of Cretaceous fossil insect record alongside angiosperm flower and pollen morphology (Hu et al., 2008). For instance, a species of tumbling flower beetle, Angimordella burmitina, was found preserved in Burmese amber carrying tricolpate (i.e. three-grooved) eudicot pollen grains. The presence of pollen grooves and single-species pollen clusters suggests insect pollination, as wind-pollinated pollen grains are smooth and more randomly dispersed. Additionally, the beetle also displays a flower-visiting body shape and adapted mouthpart for pollen feeding. This provides strong evidence that insect pollination was well-established at least 99 million years ago (Bao et al., 2019). With such intimate mutualistic interactions between insect pollinators and the food-rewarding angiosperms, specialization in flower form and shape to increase perceived attractiveness to pollinators could serve to improve reproductive success by increasing the range, frequency and efficiency of pollen transfer between plants of the same species (Armbruster, 2014). This forms the basis of coevolutionary floral specialization (e.g. morphology, color, scent, flowering time) which is thought to increase diversification rate.
In addition to their astounding diversity, angiosperms are also characterised by a high relative abundance relative to other land plants. This shows that angiosperms were able to outcompete previously dominant gymnosperms and ferns. As aforementioned, angiosperm phylogeny is studded with multiple WGD events. However, polyploidy is not always advantageous and can form barriers to selection due to reduced fertility or disruption to gene networks. As such, polyploids are sometimes referred to as “evolutionary dead ends”. In this regard, diploidization, which reverts a polyploid genome back into a diploid one, could help to negate the negative effects of polyploidy while allowing for genome downsizing and reorganisation (Dodsworth, Chase & Leitch, 2016). The post-polyploidization diploidization found typically in angiosperms thus allows for reduced cell size and genome which allows packing of more vascular tissues and stomata. With increased efficiency of nutrient and gaseous exchange, angiosperms are able to exhibit higher productivity and successfully invade many ecological niches (Simonin & Roddy, 2018).
However, there remain many controversies regarding the evolutionary history of angiosperms. Recent molecular analyses of 2,881 chloroplast genomes, encompassing 85% of extant angiosperm families, dated the origin of angiosperms to over 200 million years ago in the Late Triassic period (Li et al., 2019). This suggests a much earlier origin than proposed by paleontological records, which refute any significant pre-Cretaceous diversification. It was also widely regarded that the switch from wind pollination employed by gymnosperms to insect pollination led to an acceleration in angiosperm diversification and radiation, but many extinct gymnosperms (e.g. Bennettitales) are now found to be insect-pollinated as well (van der Kooi & Ollerton, 2020). This implies that some insect pollinators, such as the oedemerid beetle Darwinylus marcosi, transitioned from a gymnosperm host association onto an angiosperm one (Peris et al., 2017). It is also worth noting that early angiosperm flowers were relatively plain and unattractive to pollinators, and by the time large showy flowers appeared in the Mid Cretaceous period, there was already high angiosperm diversity (Hu et al., 2008). This can only be explained by the existence of other factors that increased diversification rate.
In summary, the diversity of angiosperms may be attributed considerably to coevolution with pollinators and herbivores, and their ability to outcompete previously dominant plant species could be a result of rapid genome downsizing during the Early Cretaceous period. While there is no single theory that can explain the diversity and abundance exhibited by angiosperms, it is likely that each played a unique role under different spatial and temporal contexts. Currently, until further palaeontological evidence and evolutionary models are discovered, Darwin’s mystery may remain unanswered.
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