Lactucinae

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Lactucinae

Systematics

The Lactucinae comprise about 200 species, distributed in Europe, Africa, Asia and North America (Kilian & al. 2017) and have a preference of montane habitats. The subtribe has two centres of diversity, one in the Mediterranean-SW Asian region, the second in the Sino-Himalayan region. Many species are mesic tall forbs, others are perennial herbs of other kinds, among them being the only scandent herbs found in the tribe, or rosette herbs and acaulescent herbs; more rarely they are xeric subshrubs and annual herbs (Wang & al. 2013). The subtribe constitutes a lineage within the larger of the two core groups of the tribe (Kilian & al. 2009; Tremetsberger & al. 2012; Kilian & al. 2017a).

During the 19th and 20th centrury, the Lactucinae were not usually recognised as a separate subtribe but its members were placed in a large subtribe Crepidinae or a corresponding group (Hoffmann 1899–94; Stebbins 1953; Jeffrey 1966). This changed only towards the end of the 20th century, when a morphological phylogenetic analysis by Bremer (1994) revealed the Crepidinae s.l. to be polyphyletic and the Lactucinae, Crepidinae s.str. and Sonchinae to constitute separate lineages. These were corroborated by phylogenies based on chloroplast DNA restriction site variation (Whitton & al. 1995), nrITS (Kilian & al. 2009; Tremetsberger & al. 2012; Kilian & al. 2017a) and non-coding plastid DNA loci (Kilian & al. 2017a).

Compared to the circumscription of the Lactucinae by Bremer (1994), which was largely maintained by Lack (2006), Kilian & al. (2009) excluded from subtribe Lactucinae four genera inferred from their nrITS phylogeny: (1) Nabalus s.l., which is clearly separated from Prenanthes s.str. and nested in the Crepidinae with an affinity to Soroseris; (2) Syncalathium, which in the sense of the type of its name S. kawaguchii is a member of the Crepidinae also with an affinity to Soroseris, a result supported by karyological (Zhang & al. 2007, 2009), palynological (Blackmore & Persson 1996) and further molecular (Zhang & al. 2011a, b) analyses; (3) Prenanthes, in the sense of the type of its name P. purpurea and thus as a monospecific genus, which was surprisingly found allied in nrITS phylogenies with subtribe Hypochaeridinae; (4) Faberia, but based on morphological data only.

Extensive molecular phylogenetic studies of the Lactucinae based on nrITS and five non-coding plastid DNA loci by Wang & al. (2013), focussing on the Sino-Himalayan centre of diversity, and by Kilian & al. (2017a), covering all species groups on a global scale, provided new insights into the circumscription of the subtribe. Accordingly, the redelimited monophyletic core of the Lactucinae is composed of seven lineages that also include Prenanthes, which is confirmed to have a single species, P. purpurea:

(1) Prenanthes lineage: Kilian & al. (2017a) confirmed the exclusion of the last potential congeners from Prenanthes (the Caucasian P. abietina, the North American species placed into Prenanthes or Nabalus, the scandent Prenanthes species of Sumatra and Java, the scandent tropical African P. subpeltata) and hence the assumption by Kilian & Gemeinholzer (2007), Kilian & al. (2009) and Wang & al. (2013) that P. purpurea forms an isolated lineage of the Lactucinae of its own. P. purpurea is resolved by Kilian & al. (2017a) as sister to the other six lineages of the Lactucinae in both the nrITS and plastid DNA phylogenies. Earlier findings of an affinity of Prenanthes with the Hypochaeridinae in ITS phylogenies seem to be due to long branch attraction in scarce samplings.

(2) Cicerbita lineage: The lineage consists of two sister clades: one includes the widespread European C. alpina, providing the type of the generic name Cicerbita, the Balkan endemic C. pancicii and the Caucasian-Turkish C. petiolata. The other has two subclades, one represented by Mycelis muralis, the second by a few closely related and partly doubtfully distinct, chiefly SW Asian species of Cephalorrhynchus in the sense of its type, among them the SE European–SW Asian C. hispidus.

(3)-(4) Notoseris and Paraprenanthes lineages: These include the respective near-endemic Chinese genera in the revised circumscription by Wang & al. (2013). In contrast to the nrITS phylogeny, the two lineages are resolved as a single clade in the plastid DNA phylogeny by Wang & al. (2012) and Kilian & al. (2017a).

(5) Kovalevskiella lineage: First recognised and provisionally referred to as “Cicerbita II lineage” by Wang & al. (2013), this chiefly Central Asian lineage includes, among others, three of the six species of the genus Kovalevskiella, including K. zeravschanica, which provides the type of that generic name. The other three species of the genus are nested in the Melanoseris lineage.

(6) Melanoseris lineage: Recognised by Wang & al. (2013) as the genus Melanoseris (as revived by Shih & Kilian in Shih & al. 2011), this lineage unites the Sino-Himalayan genera Chaetoseris and Stenoseris with a number of species of the same region formerly asigned to genera such as Prenanthes, Mulgedium, Cephalorrhynchus, Cicerbita and Lactuca. The monospecific near-endemic Chinese genus Parasyncalathium is also deeply nested in the Melanoseris lineage. Kilian & al. (2017a) show that besides the Sino-Himalayan clade of Melanoseris, which is formed by these taxa and extends to SE Asia, Sumatra and Java, this sizable lineage moreover includes a SW Asian clade (with e.g. Steptorhamphus, typified by S. crambifolius) and a tropical African clade (for the latter see also Wei & al. 2015).

(7) Lactuca lineage: It includes the genus Lactuca and the former segregates Lactucella (typified by L. undulata ≡ Lactuca undulata), Lagedium (typified by L. sibiricum ≡ Lactuca sibirica), Mulgedium (typified by M. runcinatum = Lactuca tatarica), Pterocypsela (typified by P. indica ≡ Lactuca indica), Scariola (typified by S. viminea ≡ Lactuca viminea).

Two further lineages shift between Lactucinae and Crepidinae in the nuclear and plastid DNA phylogenies:

(8) Faberia lineage: This lineage is allied to the Lactucinae in the nuclear phylogeny but nested in the subtribe Crepidinae in the pastid DNA phylogeny. This corresponds to the karyological evidence that the genus is alloploid with a chromosome number of 2n = 34 (Liu & al. 2012; Liu & Ren 2013), and thus most likely result of reticulate evolution involving a maternal ancestor from the Crepidinae and a paternal ancestor from the Lactucinae. Whether the nuclear or plastid DNA phylogeny provide the better estimate for the taxon phylogeny is an open question, because morphology appears little decisive in this case. Wang & al. (2013) preferred to follow the nuclear phylogeny and maintained Faberia as a member of the Lactucinae, a decision which is followed here.

(9) Astartoseris lineage: Like Faberia this monospecifc lineage endemic to Cyprus and Lebanon is nested in the Lactucinae in the nuclear phylogeny but in the Crepidinae in the pastid DNA phylogeny (Kilian & al. 2017a, b). In contrast to Faberia the taxon is diploid with a chromosome number of 2n = 18. Morphologically it is somehow intermediate between the Lactucinae and Crepidinae: showing Lactucinae feature in particular in capitula morphology and flower colour, the achene ribbing pattern is of a type characteristic of the Crepidinae (Kilian & al. 2017b). It is an early diverging orphan lineage of the Lactucinae in the nuclear phylogeny and has been classified as a genus of its own by Kilian & al. (2017b).

Kilian & al. (2017a), summarising the findings from their phylogenetic analyses, molecular clock dating and ancestral area estimations, hypothesise an origin of the Lactucinae in the SW Asian-European region between Tethys Sea and Paratethys (the sub-Paratethys region) during the second half of the Early Miocene (c. 18–19 mya). The start of its diversification is estimated to have taken place with the beginning of the Middle Miocene (c. 16–17 mya) and diversification of the core Lactucinae to have started then at least around 12–13 mya following the Middle Miocene decline in temperature, coupled with an eastward migration through Asia. One sublineage of the Melanoseris lineage took the route into tropical E Africa after the final closure of the Tethys in the east and after Late Miocene orogeny had created a suitable corridor. Still other lineages expanded westward.

The crucial problem with the lineages of the subtribe revealed in the molecular phylogenetic reconstruction, is, however, that the apparent morphological differences between the lineages are very vage, while at the same time often species of one lineage show more similarity with species of other lineages than with some of the same lineage. No morphological synapomorphies for the molecular lineages are evident currently. Sennikov (in Lazkov & al. 2014) correctly stated that this "may be explained by the rapid diversification of this group in its evolutionary history, similarly to what had been concluded for the subdivision of the Cichorieae at the level of subtribe (Tremetsberger et al. 2013)". Sennikov (in Lazkov & al. 2014) therefore proposed a very wide circumscription of Lactuca, lumbing all genera of the core Lactucinae under Lactuca. Kilian & al (2017a) state that the translation of the phylogenetic reconstruction of the Lactucinae into a natural but nevertheless practicable classification is still work in progress. This generic classification shall recognise monophyletic as well as diagnosable entities and be based on the knowledge about character evolution in the group.

For the time being, taxonomy of the subtribe inevitablely remains provisional, not the least since also the molecular phylogenies show considerable incongruences. The classification here consequently is work in progress and in principal guided by the nrITS phylogeny. In several cases thus lineages resolved are shown rather than taxonomic entities.

References


Blackmore S. & Persson V. 1996: Palynology and systematics of the Crepidinae (Compositae: Lactuceae). – Pp. 111–122 in: Hind D. J. N. & Beentje H. J. (ed.), Proceedings of the International Compositae Conference, Kew, 1994, 1. Compositae: Systematics. – Kew: Royal Botanic Gardens.

Bremer K. 1994: Asteraceae. Cladistics and classification. – Portland: Timber.

Hoffmann O. 1890–94: Compositae. – Pp. 87–387 in: Engler A. & Prantl K. (ed.), Die natürlichen Pflanzenfamilien 4(5). – Leipzig: Engelmann.

Jeffrey C. 1966: Notes in Compositae I. The Cichorieae in East Tropical Africa. – Kew Bull. 18: 427–486. // ➪ //

Kilian N., Gemeinholzer B. & Lack H. W. 2009: Tribe Cichorieae. – In: Funk V. A., Susanna A., Stuessy T. & Bayer R. (ed.), Systematics, evolution, and biogeography of the Compositae. – Vienna: IAPT.

Kilian N., Sennikov A., Wang Z.-H., Gemeinholzer B. & Zhang J.-W. 2017[a]: Sub-Paratethyan origin and Middle to Late Miocene principal diversification of the Lactucinae (Cichorieae, Compositae) inferred from molecular phylogenetics, divergence-dating and biogeographic analysis. – Taxon 66: 675-703. // ➪ //

Kilian N., Hand R., Hadjikyriakou G. N., Christodoulou C. S. & Bou Dagher-Kharrat M. 2017[b]: Astartoseris (Cichorieae, Asteraceae), a new, systematically isolated monospecific genus accommodating Lactuca triquetra endemic to Lebanon and Cyprus. — Willdenowia 47: 115–125. // ➪ //

Koopman W. J. M., Guetta E., Van de Wiel, C. C. M., Vosman B. & Van den Berg R.G. 1998. Phylogenetic relationships among Lactuca (Asteraceae) species and related genera based on ITS-1 DNA sequences. – Amer. J. Bot. 85: 1517–1530.

Lack H. W. 2006: Tribe Cichorieae Lam. & DC. – Pp. 180–199 in: Kadereit J. W. & Jeffrey C. (ed.), The families and genera of vascular plants 8. – Berlin: Springer.

Lazkov G. A., Sennikov A. N., Koichubekova G. A. & Naumenko A. N. 2014: Taxonomic corrections and new records in vascular plants of Kyrgyzstan, 3. – Memoranda Soc. Fauna Fl. Fenn. 90: 91–110.

Liu Y. & Ren C. 2013: Cytotaxonomy of Prenanthes faberi (Compositae – Cichorieae). – Nordic J. Bot. 31: xxx–xxx. // ➪ //

Liu Y., Tao D. & Yang Q.-E. 2012: Karyology of the genus Faberia (Cichorieae – Asteraceae) and its systematic implications. – Nordic J. Bot. 29: 365–371. // ➪ //

Shih C., Ge X. J.; Kilian N., Kirschner J., Štěpánek J., Sukhorukov A. P., Mavrodiev E. V. & Gottschlich G. 2011: Cichorieae. – Pp. 195–353 in: Wu Z. Y., Raven P. H. & Hong D. Y. (ed.), Flora of China 20–21. Asteraceae. – Beijing: Science Press & St Louis: Missouri Botanical Garden. // ➪ //

Stebbins G. L. 1953: A new classification of the tribe Cichorieae, family Compositae. – Madroño 12: 65–81.

Tremetsberger K., Gemeinholzer B., Zetzsche H., Blackmore S., Kilian N. & Talavera S. 2012: Divergence time estimation in Cichorieae (Asteraceae) using a fossil-calibrated relaxed molecular clock. – Org. Divers. Evol. 13: 1-13. // ➪ //

Wang Z. H., Peng. H. & Kilian N. 2013: Molecular phylogeny of the Lactuca alliance (Cichorieae subtribe Lactucinae, Asteraceae) with focus on their Chinese centre of diversity detects potential events of reticulation and chloroplast capture. – PLoS ONE 8(12): e82692 // ➪ //

Wei Z., Zhu S.-X, Van den Berg R. G., Bakker F. T. & Schranz M. E. 2015: Phylogenetic relationships within Lactuca L. (Asteraceae), including African species, based on chloroplast DNA sequence comparisons. – Genet. Resoucres Crop Evol. 64: 55-71. // ➪ //

Whitton J., Wallace R. S. & Jansen R. K. 1995: Phylogenetic relationships and patterns of character change in the tribe Lactuceae (Asteraceae) based on chloroplast DNA restriction site variation. – Canad. J. Bot. 73: 1058–1073.

Zhang J.-W., Sun H. & Nie E.-L. 2007: Karyological studies on the Sino-Himalayan endemic Soroseris and two related genera of tribe Lactuceae (Asteraceae). – Bot. J. Linn. Soc. 154: 79–87.

Zhang J. W., Nie Z. L. & Sun H. 2009: Cytological study on the genus Syncalathium (Asteraceae-Lactuceae), an endemic taxon to alpine scree of the Sino-Himalayas. – J. Syst. Evol. 47: 226–230.

Zhang J.-W., Nie Z. N., Wen J. & Sun H. 2011: Molecular phylogeny and biogeography of three closely related genera, Soroseris, Stebbinsia, and Syncalathium (Asteraceae, Cichorieae), endemic to the Tibetan Plateau, SW China. – Taxon 60: 15–26. // ➪ //

Zhang, J.-W., Boufford D. E.& Sun H. 2011: Parasyncalathium J.W. Zhang, Boufford & H. Sun (Asteraceae, Cichorieae): A new genus endemic to the Himalaya-Hengduan Mountains. – Taxon 60: 1678–1684. // ➪ //

Distribution

Africa: Algeria native; Angola native; Azores native; Benin native; Botswana introduced; Burkina native; Burundi native; Cameroon native; Canary Is. native; Cape Provinces (Eastern Cape Province native, Northern Cape Province native, Western Cape Province native); Central African Republic native; Chad native; Comoros (Comoros native); Congo native; Djibouti native; Egypt native; Equatorial Guinea native; Eritrea native; Ethiopia native; Free State native; Ghana native; Guinea native; Gulf of Guinea Is. (Bioko native); Ivory Coast native; Kenya native; KwaZulu-Natal native; Lesotho native; Liberia native; Libya native; Madagascar native; Madeira introduced; Malawi native; Mali native; Mauritius native; Morocco native; Mozambique native; Namibia native; Niger native; Nigeria native; Northern Provinces (Gauteng native, Mpumalanga native, North-West Province native, Northern Province native); Rodrigues native; Rwanda native; Réunion native; Seychelles introduced; Sierra Leone native; Somalia native; Sudan native; Swaziland native; Tanzania native; Togo native; Tunisia native; Uganda native; Zaire native; Zambia native; Zimbabwe native Asia-Temperate: Afghanistan native; Altay native; Amur native; Buryatiya native; China North-Central (Gansu native, Hebei native, Shaanxi native, Shandong native, Shanxi native); China South-Central (Chongqing native, Guizhou native, Hubei native, Sichuan native, Yunnan native); China Southeast (Anhui native, Fujian native, Guangdong native, Guangxi native, Henan native, Hunan native, Jiangsu native, Jiangxi native, Zhejiang native); Chita native; Cyprus native; East Aegean Is. native; Gulf States (Qatar introduced, United Arab Emirates native); Hainan native; Inner Mongolia (Nei Mongol native, Ningxia native); Iran native; Iraq native; Irkutsk native; Japan native (Hokkaido native, Honshu native, Kyushu native, Shikoku native); Kamchatka native; Kazakhstan native; Khabarovsk native; Kirgizistan native; Korea native (North Korea native); Krasnoyarsk native; Kuril Is. native; Lebanon-Syria (Lebanon native, Syria native); Magadan native; Manchuria (Heilongjiang native, Jilin native, Liaoning native); Mongolia native; Nansei-shoto native; North Caucasus native (Chechnya native, Dagestan native, Kabardino-Balkariya native, Karacheyevo-Cherkessiya native, Krasnodar native, Severo-Osetiya native, Stavropol native); Ogasawara-shoto native: doubtfully native; Oman native; Palestine (Israel native, Jordan native); Primorye native; Qinghai native; Sakhalin nativenative; Saudi Arabia native; Sinai native; Tadzhikistan native; Taiwan native; Tibet nativenative; Transcaucasus (Abkhaziya native, Adzhariya native, Armenia native, Azerbaijan native, Georgia native, Nakhichevan native); Turkey nativenative; Turkmenistan native; Tuva native; Uzbekistan native; West Siberia native; Xinjiang native; Yakutskiya native; Yemen (North Yemen native, South Yemen native) Asia-Tropical: Assam (Assam native, Manipur native, Meghalaya native, Mizoram native, Nagaland native); East Himalaya (Arunachal Pradesh native, Bhutan native, Darjiling native, Sikkim native); India (Delhi native, Haryana native, Kerala native, Madhya Pradesh native, Punjab native, Rajasthan native, Tamil Nadu native, Uttar Pradesh native, West Bengal native); Jawa native; Laos nativenative; Malaya (Peninsular Malaysia native: doubtfully native); Myanmar native; Nepal native; New Guinea (Irian Jaya native, Papua New Guinea native); Pakistan nativenative; Philippines native; Sumatera native; Thailand native; Vietnam native; West Himalaya (Himachal Pradesh native, Jammu-Kashmir native, Uttaranchal native) Australasia: New South Wales (Australian Capital Territory introduced, New South Wales introduced); New Zealand North introduced; New Zealand South introduced; Northern Territory introduced; Queensland (Queensland introduced); South Australia introduced; Tasmania introduced; Victoria introduced; Western Australia (Ashmore-Cartier Is. introduced, Western Australia introduced) Europe: Albania nativenative; Austria native (Austria native, Liechtenstein native); Baleares nativenative; Baltic States (Estonia native, Kaliningrad native, Latvia native, Lithuania native); Belarus native; Belgium native (Belgium native, Luxembourg native); Bulgaria native; Central European Russia native; Corse native; Czechoslovakia native (Czech Republic native, Slovakia native); Denmark native; East European Russia native; Finland native; France native; Germany native; Great Britain native; Greece native; Hungary native; Iceland introduced; Ireland introduced (Ireland introduced, Northern Ireland introduced); Italy native; Kriti native; Krym native; Netherlands native; North European Russia native; Northwest European Russia native; Norway native; Poland native; Portugal nativenative; Romania native; Sardegna native; Sicily native (Malta native, Sicily native); South European Russia native; Spain native (Andorra native, Gibraltar native, Spain native); Sweden native; Switzerland native; Turkey-in-Europe native; Ukraine (Moldova native, Ukraine native); Yugoslavia (Bosnia-Herzegovina native, Croatia native, Macedonia native, Montenegro native, Serbia native, Slovenia native) Northern America: Alabama native; Alaska native; Alberta native; Arizona native; Arkansas native; British Columbia native; California native; Colorado native; Connecticut native; Delaware native; District of Columbia native; Florida native; Georgia, U.S.A. native; Idaho native; Illinois native; Indiana native; Iowa native; Kansas native; Kentucky native; Labrador native; Louisiana native; Maine native; Manitoba native; Maryland native; Massachusetts native; Mexico Central native (Mexico Distrito Federal introduced, México State native, Puebla native); Mexico Gulf (Veracruz native); Mexico Northeast (Chihuahua native, Coahuila native, Guanajuato native, Hidalgo native, Nuevo León native, Querétaro native, San Luis Potosí native, Tamaulipas native); Mexico Northwest (Baja California introduced, Sonora native); Mexico Southeast (Chiapas native); Mexico Southwest (Michoacán native, Oaxaca native); Michigan native; Minnesota native; Mississippi native; Missouri native; Montana native; Nebraska native; Nevada native; New Brunswick native; New Hampshire native; New Jersey native; New Mexico native; New York native; Newfoundland (Newfoundland native, St.Pierre-Miquelon native); North Carolina native; North Dakota native; Northwest Territories native: doubtfully native; Nova Scotia native; Ohio native; Oklahoma native; Ontario native; Oregon native; Pennsylvania native; Prince Edward I. native; Québec native; Rhode I. native; Saskatchewan native; South Carolina native; South Dakota native; Tennessee native; Texas native; Utah native; Vermont native; Virginia native; Washington native; West Virginia native; Wisconsin native; Wyoming native; Yukon introduced Southern America: Argentina Northeast (Argentina Distrito Federal introduced, Buenos Aires introduced, Chaco introduced, Corrientes introduced, Córdoba introduced, Entre Ríos introduced, La Pampa introduced); Argentina Northwest (Catamarca introduced, Jujuy introduced, La Rioja introduced, Mendoza introduced, San Juan introduced, San Luis introduced); Argentina South (Chubut introduced, Neuquén introduced, Rio Negro introduced, Santa Fé introduced); Bahamas native; Brazil South (Paraná introduced, Rio Grande do Sul introduced, Santa Catarina introduced); Brazil Southeast (Rio de Janeiro introduced, São Paulo introduced); Chile Central (Biobío introduced, Coquimbo introduced, La Araucania introduced, Maule introduced, O'Higgins introduced, Santiago introduced, Valparaíso introduced); Chile North (Antofagasta introduced, Tarapaca introduced); Cuba introduced; Dominican Republic native; Ecuador introduced; Galápagos introduced; Guatemala nativenative; Haiti (Haiti native); Honduras introduced; Jamaica native; Leeward Is. (British Virgin Is. native); Paraguay introduced; Puerto Rico native; Uruguay introduced