Evolutionary and ecological insights from <i>Cytinus</i>: A plant within a plant

Cytinus is a group of plants that grow within other plants: parasitic life cycle has evolved just four times in the plant kingdom. species are externally invisible for most their life, emerging from hosts only to flower and set seed. Owing this cryptic cycle, genus poorly understood likely include several hitherto undescribed species, particularly threatened forest habitat Madagascar. At time unprecedented biodiversity loss extinction, our work on highlights complex biology importance taxonomy-informed conservation. The L. arguably one enigmatic It belongs families plants, which embedded tissues way similar some fungi (Teixeira-Costa & Suetsugu, 2023; Thorogood et al., 2021). Due convergence history, Apodanthaceae, Cytinaceae, Mitrastemonaceae Rafflesiaceae were long-thought be monophyletic. However, molecular phylogenetic data have revealed independent origins, placing Apodanthaceae order Cucurbitales, Ericales, Malpighiales Cytinaceae Malvales, close Neotropical Muntingiaceae (Filipowicz Renner, 2010; Nickrent, 2007, 2020; Nickrent 2004). shows an extreme reduction morphological characters, lacking roots, with stem reduced inflorescence axis beset scale-like leaves, flowering shoots visible during reproductive period when they emerge host (de Vega 2009, 2007). vegetative endophytic system lives entirely roots (rarely stems) host. endophyte inside forms filaments anastomose, ultimately generate bands tissue, sinkers transfer cells. These facilitate absorption water photoassimilates parasite As non-photosynthetic angiosperms, plastome extremely size gene content (Roquet 2016); thus, completely dependent carbon nutrition survival. includes eight accepted native Old World, striking distribution spanning Mediterranean Basin, South Africa Eswatini southern Taxonomic boundaries delimited genus, owing features, poor preservation as dried specimens dearth herbarium records regions, example, Madagascar, where we identified putative taxa, remain described. Even at intra-specific level, studies indicate evolutionary history more than previously understood. Host-specific genetic races or ecotypes appear been overlooked because morphology 2008; Martos press). attract diverse array pollinators, including insects, birds rodents 2009; Hobbhahn Johnson, 2015; Johnson 2011), but biology, mode seed dispersal, remains species. Taken together, promising largely untapped model exploring genetics evolution parasitism, host-driven speciation biology. Here, provide brief review ecology neglected endoparasites present novel its remarkable diversity pollinators predators. We discuss potentially taxa address taxonomic confusion implications conservation risk assessment. family contains two genera curiously disjunct distribution, New World (Bdallophytum Eichler, Mexico Central America Colombia; Alvarado-Cárdenas, Fernández-Alonso Cuadros-Villalobos, 2012) (Cytinus, Southern Africa, Madagascar). Phylogenetic suggest neotropical origin late Cretaceous, highly supported monophyletic sister Bdallophytum (Hernandez-Gutierrez Magallon, 2019; historical biogeographic reconstruction hypothesizes divergence American ancestral lineages around 60 Myr long-distance dispersal tropical (Martos Subsequent colonization Madagascar (where ancestors may obtained climatic refuge), followed by expansion into warm temperate latitudes eventual host-specialization, explain unusual Cytinus. Genetic analyses support monophyly each biogeographical region, is, clade, African clade Malagasy clade. In Macaronesia Asia Minor, occurs thermophilous, maquis-type vegetation it parasitizes shrubs Cistaceae exclusively 2008). Most treatments recognize hypocistis (Figure 1a,b) C. ruber 1c) (Table 1), distinguished mainly colour (yellow-orange pale pink, respectively) identity host, former parasitizing white yellow-flowered Cistus (including Halimium) Helianthemum, latter occurring pink-flowered (Villar, 1997; Webb, 1993). Based measures subtle floral traits, subspecies recognized including: subsp. hypocistis, macranthus Wettst., orientalis Wettst. (ex Hayek), pityusensis Finschow, subexsertum Finschow ex G. Kunkel also kermesinus (Guss.) Arcang. clusii Nyman (both synonyms ruber). More recently, can separated well-characterized associated respectively different not genetically differentiated case among Such prompts re-evaluation taxonomy A detailed examination over years populations number flowers produced, rewards phenology significantly influenced Vega, 2007; de unpublished). Thus, distinction phenotypic data. Again, points specificity underestimated driver Three endemic described Africa: sanguineus (Thunb.) Fourc. (synonym dioicus Juss.) 1d,e), capensis Marloth 1f) recently visseri Burgoyne 1g,h) found Cape floristic Region (in Renosterveld, Flats Dune Strandveld, fynbos) rocky sandstone outcrops northern Provinces ~1,400–2,000 m (Burgoyne, 2006; Smithies Burgoyne, 2010). recent discovery numerous additional taxonomically above (Hobbhahn, unpublished; unpublished) richer synonymized under (Goldblatt Manning, 2000); however, differences pollination syndromes, (Hobbhahn 2013, press) all recognition specialized Asteraceae and, lesser extent, Thymelaeaceae Rutaceae noted specific Helichrysum, Metalasia, Anaxeton, Oedera Elytropappus (Asteraceae) Passerina (Thymelaeaceae) thorough investigation reliable meaningful parameters defining necessary inform Madagascar: malagasicus Jum. H. Perrier 1i) known solely type specimen collected 1912 (Jumelle la Bâthie, 1915), baronii Baker f. 1j–l) glandulosus 1). All occur primary, humid forests. baronii, Masoala peninsula, Massif du Tsaratanana (NE Madagascar) specialize Croton (Euphorbiaceae); was first parasitising Dicoryphe (Hamamelidaceae), malagasicus, Analamazaotra (Centre-East Madagascar), Dombeya (Malvaceae) (Baker, 1888; Jumelle 1915). identification these cases dubious. field observations remote locations further await discovery. morphological, phenological data, propose least unreported 1; Figure 2). imagery ecological information (see Section 3). (Cytinus sp1) blooms November observed Peninsula 0–100 sp., forming population ~100 individuals (year 1996; Schatz, personal communication). year 2015, again, high density 2a,b). sp2 2c–e) August Tsinjoarivo-Ambalaomby protected area (Central-East 1,400–1,600 m. area, 13 km apart, male female flowers; until available, tentatively consider correspond same taxon. vernacular name ‘Atoditany’, meaning ‘egg earth’. morphologically taxon, between September, showing relatively flowers, NE Marojejy National Park, 650 away 2f–h). relatedness require careful analysis. sp3 summit mountain Maromokotro, Polyscias (Araliaceae). record 2010 again 2022 2i–k). Finally, sp4 October later Anjanaharibe-Sud Special Reserve 2l–n), small 40 inflorescences 500 m2 (P. Hošek, combination vouchers, essential confirm produce unisexual fleshy 3), there exists astonishing geographical variation sexual systems (monoecy dioecy) colour, size, scent rewards, suggestive multiple pollinator shifts. monoecious, comprises single, short spike lateral central flowers. On given root, clusters up 20 appear, usually produced endophyte; cases, distinct, suggesting infections tetramerous yellow (C. hypocistis) white-pinkish ruber) (female wider longer males), secrete limited nectar (c. 1 μl/24 h) dominated few aromatics compounds irregular terpenes (mainly 4-oxoisophorone, (E)-cinnamaldehyde (E)-cinnamyl alcohol) ant 1b). While seeking nectar, ants consistently touch organs carry large pollen loads (each amounts pollen, 2.5 × 106 grains/flower), acting effective abundant 2014). dioecious, either solitary short, few-flowered spikes protruding root produces hexamerous (occasionally pentamerous), vermillion, scentless, easily accessible offer copious, diluted (40 narrowly tubular nectaries Visser, 1981). This adaptations conforms bird syndrome confirmed pollinated Malachite Sunbirds (Nectarinia famosa) that, while visiting forage efficiently copious beaks 1e) 2015). contrast, (with four, seldom tepals, dark maroon blooming July September), five [six] scarlet January May), discovered possess characteristics consistent small, ground-dwelling mammals. unusually robust contain (up 130 μl) concentrated 2011). densely hairy tepals tightly infolded, so closed throughout anthesis emit strong, vanilla-like scent, those pungent reminiscent nail-polish remover, aliphatic ketones (3-hexanone 1-hexen-3-one). Floral suggested play important role both attraction mammals, Aethomys sp. (Muridae) capensis, Rhabdomys pumilio, Mus minutoides Elephantulus brachyrhynchus (Macroscelididae) 1h) visseri, open consuming 2013; mystery, features adapted mammals (hinted Like counterparts mainland, borne arranged Jumelle, 1923; 1915) grows trunks 1j), producing surrounded orbicular scale leaves. hexamerous, scented 1k). Recent using motion-sensor camera recordings visitation Eliurus Nesomys (Nesomyidae) visit 1l). report To date, virtually nothing about chambers (hexamerous, brown, glabrous inflorescence, aestivation spiral) (large conical 15 cm across, 5–16 brownish pentamerous, big chambers) 1) suggests characters point mammal pollination. sp1 large, solitary, 2a), sweet fragrance resembling fruit slight fermentation odour. Although bears resemblance thicker, fleshier somewhat waxy tepals; rather stems. white-brownish marked dimorphism, globose whitish black stigma 2c) brownish, bearing scale-leaves 2d,e). Both greatly enlarged chambers. form north possesses 2f); smaller shorter rounder perianth lobes 2g). hemisphere taxon very ~14 diameter, distinctly tepals. Only observed. white, cm, covered conspicuously imbricate, obovate scales 2l,m). six wide 2n). Scales turn rapidly open, emitting like honeydew melon (S. Goodman, Virtually potential new taxa. (and Marojejy) reported occasionally consumed lemur (Propithecus sp.) (Irwin E. Patel R. Desiré, communication) 2h, note sifaka holding hand), sifakas cannot ruled out. examined date berry-like fruits containing many thousands dust-like seeds undifferentiated embryos (Bouman Meijer, 1994; 2011; Oliveira, Ants efficient dispersers mice Apodemus sylvaticus extent rabbit Oryctolagus cuniculus consume quantity night. They defecate droppings hundreds viable right next eat, dispersed hosts. (genus Aphaenogaster, Crematogaster, Pheidolle, Tetramorium Tapinoma) disperse quantities day them hills, often Cistaceae, even being base trunks. Additionally, Cytinus, endozoochory beetles, behaviour near establishment re-infection natal Fine-scale events distances lizards (Smithies 2010); rats dry (Perrier 1923). Foraging attracted predate 2007), lemurs mature (R. communication), dispersers. Details germination infection despite extensive attempts germinate almost certain exposure host-derived stimulants passage through intestinal disperser germinate, holoparasitic plants. used traditional medicine since ancient times. 2,000 ago, Hippocrates Dioscorides recommended juice treat variety disorders then indigestion, bleedings, dysentery, constipation skin inflammation (Baumann, 1993; Lev Amar, Sanna Satil 2017). plants' hydrolysable tannins cytotoxic activity against broad spectrum cancer cell lines (Magiatis 2001) extracts antimicrobial, antioxidant anti-inflammatory activities (Maisetta Silva 2020), surprisingly, strong antiviral SARS-CoV-2 Araujo 2023). traditionally due nutritional properties (Satil 2017; Tardío 2006). unaware any reports uses Understanding ecology, patterns, structure availability critical planning involving (Barcelona Marvier Smith, Pelser widespread evaluated IUCN list endangered local areas, such eastern Bulgaria (Petrova Vladimirov, 2009), included ‘special interest’ (Boletin Oficial Región Murcia (BORM), 2003) Critically Endangered (CR). Canary Islands, status requires Red Least Concern (LC) category, considered critically collection places, thought become extinct (Raimondo 2009). formerly vulnerable 2006), category LC List Eswatini. should planning, host-defined races, comprising scarce fragmented unique genotypes management. yet reviewed, anthropogenic extinctions taking place island (Ralimanana 2022) rapid destruction, advocate inclusion CR Specifically, suspect already recorded 1912. An urgent assessment biological will crucial management Extensive sampling combined molecular, elucidate relationships With respect sampling, particular emphasis (1) diagnosis, identify host-specific efforts, (2) understand explored changing geographic region. Given systems, research could involve mapping traits chemistry onto phylogeny infer pathways evolution. conservation, recommend well preserved seedbanks, mechanisms initial processes warrant (Thorogood 2022). situ threat. biogeography three major centres diversification, specialization makes diversification Clara Chris J. conceived manuscript. led writing prepared figures. made drawings. authors contributed drafts gave final approval publication. grateful Prof. Baker, Mr. Irwin, Dr. Martin sharing pictures declare no conflict interest. Data applicable article, datasets generated analysed current study.