Population genomics reveal apomixis in a novel system: uniclonal female populations dominate the tropical forest herb family, Hanguanaceae (Commelinales)

Abstract

Background and Aims The abundance of apomixis in tropical plant genera is poorly understood, and this affects the understanding of speciation and evolution. Hanguanaceae is a tropical monogeneric, dioecious plant family. All but two species are solitary herbs with no capability to spread vegetatively. Viable seeds are often produced when males have not been observed. Our aim was to investigate the presence of apomixis in Hanguana. Methods We used reduced representation genomics to study phylogenetics and genetic variability in all populations of Hanguana in Singapore. We measured genome sizes and estimated ploidy levels in 10 species. Key Results Almost all taxa tested were genetically uniform (uniclonal) regardless of the extent of their distribution. The distribution of single clones over distinct localities support our hypothesis of apomictic reproduction. Only one sexually reproducing native species was detected. Triploid and pentaploid states support our hypothesis that the type of apomixis in Hanguana is gametophytic. Conclusions Population genomics tools offer a quick and cost-effective way of detecting excess clonality and thereby inferring apomixis. In the case of Hanguana, the presence of male plants is a strong indicator of sexual reproduction, whereas genome triplication is indicative of apomictic reproduction.

Hanguana deflexa (Hanguanaceae), a new forest species from Sarawak, Borneo

“…We sequenced the tissue of the type collection using ddRADseq with the methods described in full in Niissalo et al (2020) . We mapped the sequences to the consensus sequence published therein, and conducted a phylogenetic reconstruction using 1000 bootstrap replicates with random seed of 1, Cyrtostachys renda as an outgroup, and default settings in RAxML 7.2.8 ( Stamatakis 2006 ).…”

“…We mapped the sequences to the consensus sequence published therein, and conducted a phylogenetic reconstruction using 1000 bootstrap replicates with random seed of 1, Cyrtostachys renda as an outgroup, and default settings in RAxML 7.2.8 ( Stamatakis 2006 ). As a test of ploidy levels, we used Smudgeplot v. 0.2.3dev ( Ranallo-Benavidez et al 2020 ), modified for ddRADseq data as described in Niissalo et al (2020) .…”

“…However, males are only rarely observed and for numerous species, male plants remain unknown. As many female plants produce viable seeds in the absence of males the discovery of polyploidy and apomixis in some species ( Niissalo et al 2020 ) is not surprising. Consequently, only female individuals in the mature fruiting stage are usually used for description of new taxa.…”

“…The presence of stolons, indumentum presence and type, shape of staminodial scales, stigma morphology and position, inflorescence/infructescence architecture, colour of the ripe fruit, and morphology and number of seeds per fruit are considered as the most important ( Siti Nurfazilah et al 2011 ; Leong-Škorničková and Boyce 2015 ). On the infrageneric level, the most phylogenetically informative traits seem to be the presence of stolons and especially the seed shape ( Niissalo et al 2020 ). Both so far known stoloniferous species ( H. anthelminthica and H. nitens Siti Nurfazilah, Mohd Fahmi, Sofiman Othman & P.C.Boyce) share shallowly cupuliform seeds and diverged early from the other non-stoloniferous, forest species.…”

“…Both so far known stoloniferous species ( H. anthelminthica and H. nitens Siti Nurfazilah, Mohd Fahmi, Sofiman Othman & P.C.Boyce) share shallowly cupuliform seeds and diverged early from the other non-stoloniferous, forest species. The forest species can be further divided into two monophyletic groups, one consisting of robust species with bowl shaped seeds (the so-called large forest species) and the second consisting of small-sized species with almost globose, internally deeply excavated seeds with a wedge-shaped ostiole resembling the popular video game main character called pac-man (the so-called small forest species; Niissalo et al 2020 ).…”