Wrong flowers? The evolutionary puzzle of Jongkindia (Passifloraceae s.l.), a new monotypic genus and tribe from Liberia, West Africa

From Firenze University Press Journal: Journal of Plant Taxonomy and Geography (Webbia)

Frans J. Breteler, Grintweg 303

Floris C. Breman, Biosystematics Group, Wageningen University & Research

Di Lei, Biosystematics Group, Wageningen University & Research

Freek T. Bakker, Biosystematics Group, Wageningen University & Research

Jongkindia, a small tree species endemic to a local area in southeast Liberia, is described as a new monotypic genus of Passifloraceae sens. lat. Its only species Jong-kindia mulbahii combines floral characteristics of the Turneraceae and fruit character-istics of the Passifloraceae s.s. (or subfamily Passifloroideae in APG) and can therefore be regarded to occupy an isolated morphological position. This is confirmed here by DNA sequence-based phylogenetic analyses including most Passifloracean genera, which places it as sister to Passifloroideae. We delineate 16 morphological characters and their states and optimise them on our reconstructed phylogenetic tree. Based on these results we consider the Passifloraceae fruit characteristics (berries with arilled seeds) as synapomorphic for Passifloroideae. The monotypic Pibiria and Jongkindiaare predominantly characterised by autapomorphies. On the other hand, the Adenia/Passiflora clade is characterised by polymorphisms. We place Jongkindia in a new tribe Jongkindieae Breteler & F.T.Bakker. A draft plastome sequence for Jongkindia mulbahiiis presented and evidence for two mitome to plastome (mtpt) fragment transfers is dis-cussed. Structurally the Jongkindia plastome appears similar to that of Populus, Adenia, Mitostemma, Dilkea, and Passiflora pittieri, but not to contain the previously-described major inversions within other, more derived, Passiflora plastomes.Ongoing botanical exploration of Liberia (Breteler 2020; Jongkind 2012, 2015a, b, c; 2016; 2017; 2019; Jongkind and Breteler 2020) revealed the presence of a thus far undescribed species of Passifloraceae s.l., near Sapo National park (Sinoe County, Liberia) which contains “the second-largest area of primary tropical rainforest in West Africa.” (Freeman et al. 2019). The undescribed species presented here appears somewhat of a conundrum: in spite of its 4- instead of 5-merous flowers it is best placed in Turneraceae (now Turneroideae sensu APG III (2009) and IV (2016)) because of its tubular calyx with the petals insterted on it and because of the absence of a corona. However, Turneroideae have capsular fruits (Arbo 2007) whereas the new species presented here has an indehis-cent fleshy fruit, common in Passiflora (in Passifloroideae sensu APG).

Wurdack et al. (2009) maintained Turneraceae and Malesherbiaceae as separate under Passif loraceae s.l. but Takuoka (2012), based on comparison of rbcL, atpB, matK, and 18S rDNA sequences, considered a well-sup-ported monophyletic Passifloraceae ss. and Turneraceae as (well-supported) sister groups. Both Xi et al. (2012), based on concatenated analysis of 82 plastid genes from 58 spe-cies, and Cai et al. (2021), based on multi-species coales-cent analysis of 423 single-copy nuclear loci from 64 taxa, support a ‘Parietal clade’ in which Turneraceae and Pas-sifloraceae are sister groups, with Malesherbiaceae sister to them. The two latter studies differ in the placement of Achariaceae, which is sister to the remainder of the Pari-etal clade (Xi et al. 2012) or in a derived position within it (Cai et al. 2021). Within the Parietal clade, the two studies differ with regards monophyly of the salicoids sensu Xi et al. (2012), which is supported by the concatenated analysis but not in any of the coalescent methods (Cai et al. 2021).

Within Passifloraceae s.s., Takuoka (2012) recognises monophyletic tribes Passifloreae and Paropsieae, wich is also adopted by APG. The first is distributed in the Old and New World and the second only in Old World (mainly Africa; Table 1). Maas et al. (2019) described the enigmatic ‘unknown yellow’ Pibiria as a lineage sister to Turneroidea and chose to place it at subfamily-level, which brings the number of recognised subfamilies in Passifloraceae to four, i.e. Passifloroideae, Turneroideae, Pibirioideae and MalesherbioideaeGiven the remarkable combination of Tu r n e ra-like floral morphology and Passiflora-like fruits in the new species presented here it will be interesting to infer its phylogenetic position within this part of Malpighiales, known to present major challenges (such as incomplete lineage sorting, gene tree error and horizontal gene transfer) to phylogenetic reconstruction (Xi et al. 2012; Cai et al. 2020; APG IV). Therefore, we generated DNA sequences for this species, both Sanger and Illumina HiSeq, and compared it with publicly available sequence data for Passif loraceae s.l. We find our new species, which we refer to as Jongkindia mulbahii (see below), to be in an isolated position on a relatively short branch between, on the one hand, the Parietal clade (or Pas-sifloroideae, to which it is sister) including a Barteria/Paropsia clade (both genera of small trees; Breteler 1999; 2003; de Vos and Breteler 2009), and the Turneroideae clade on the other. It is described and illustrated here as a new monotypic genus, and its draft plastome is com-pared with plastomes from Adenia, Passiflora, Dilkea, Mitostemma and allies.



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