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* {{cite journal |first=F. |last=Buxbaum |title=Die Entwicklungslinien der Lilioideae. I. Die systematische Stellung der gattung ''Gagea'' |journal=Botanisches Archiv |volume=38 |year=1936 |pages=213–293 |language=German|ref=harv}}
* {{cite journal |first=F. |last=Buxbaum |title=Die Entwicklungslinien der Lilioideae. I. Die systematische Stellung der gattung ''Gagea'' |journal=Botanisches Archiv |volume=38 |year=1936 |pages=213–293 |language=German|ref=harv}}
* {{cite journal |first=F. |last=Buxbaum |title=Die Entwicklungslinien der Lilioideae. II. Die Wurmbaeoideae |journal=Botanisches Archiv |volume=38 |year=1937 |pages=305–398 |language=German|ref=harv}}
* {{cite journal |first=F. |last=Buxbaum |title=Die Entwicklungslinien der Lilioideae. II. Die Wurmbaeoideae |journal=Botanisches Archiv |volume=38 |year=1937 |pages=305–398 |language=German|ref=harv}}
* {{cite journal |last=Rudall |first=P. |last2=Furness |first2=C.A. |last3=Chase |first3=M.W. |last4=Fay |first4=M.F. |title=Microsporogenesis and pollen sulcus type in Asparagales (Lilianae) |journal=[[Canad. J. Bot.]] |year=1997 |volume=75 |issue=3 |pages=408–430 |id={{INIST|10769694}} |issn=0008-4026 |doi=10.1139/b97-044|ref={{harvid|Rudall et al|1997a}}}}
* {{cite book |last=Chase |first=M.W. |last2=Soltis |first2=D. E. |last3=Soltis |first3=P. S. |last4=Rudall |first4=P. J. |last5=Fay |first5=M. F. |last6=Hahn |first6=W. H. |last7=Sullivan |first7=S. |last8=Joseph |first8=J. |last9=Molvray |first9=M. |last10=Kores |first10=P. J. |last11=Givnish |first11=T. J. |last12=Sytsma |first12=K. J. |last13=Pires |first13=J. C. |authorlink=Mark Chase|title=Monocots: Systematics and evolution |year=2000 |publisher=[[CSIRO]] |location=Collingwood, Australia |pages=3–16 |editor-last=Wilson |editor-first=K.L. |editor2-last=Morrison |editor2-first=D.A. |chapter=Higher-level systematics of the monocotyledons: An assessment of current knowledge and a new classification|ref={{harvid|Chase et al|2000}}}}
* {{cite book |last=Chase |first=M.W. |last2=Soltis |first2=D. E. |last3=Soltis |first3=P. S. |last4=Rudall |first4=P. J. |last5=Fay |first5=M. F. |last6=Hahn |first6=W. H. |last7=Sullivan |first7=S. |last8=Joseph |first8=J. |last9=Molvray |first9=M. |last10=Kores |first10=P. J. |last11=Givnish |first11=T. J. |last12=Sytsma |first12=K. J. |last13=Pires |first13=J. C. |authorlink=Mark Chase|title=Monocots: Systematics and evolution |year=2000 |publisher=[[CSIRO]] |location=Collingwood, Australia |pages=3–16 |editor-last=Wilson |editor-first=K.L. |editor2-last=Morrison |editor2-first=D.A. |chapter=Higher-level systematics of the monocotyledons: An assessment of current knowledge and a new classification|ref={{harvid|Chase et al|2000}}}}
* {{cite journal |last=Hilu |first=K. |last2=Borsch |first2=T. |last3=Muller |first3=K. |last4=Soltis |first4=D.E. |last5=Soltis |first5=P.S. |last6=Savolainen |first6=V. |last7=Chase |first7=M.W. |last8=Powell |first8=M.P. |last9=Alice |first9=L.A. |last10=Evans |first10=R. |last11=Sauquet |first11=H. |last12=Neinhuis |first12=C. |last13=Slotta |first13=T.A.B. |last14=Rohwer |first14=J.G. |last15=Campbell |first15=C.S. |last16=Chatrou |first16=L.W. |title=Angiosperm phylogeny based on ''<011>'' ''matK'' sequence information |journal=[[American Journal of Botany]] |date=December 2003 |volume=90 |issue=12 |pages=1758–1766 |doi=10.3732/ajb.90.12.1758 |url=http://www.amjbot.org/cgi/content/full/90/12/1758 |accessdate=4 January 2014|ref={{harvid|Hilu et al|2003}}}}
* {{cite journal |first=Mark W. |last=Chase |first2=James L. |last2=Reveal |first3=Michael F. |last3=Fay |authorlink=Mark Chase|title=A subfamilial classification for the expanded asparagalean families Amaryllidaceae, Asparagaceae and Xanthorrhoeaceae |journal=Botanical Journal of the Linnean Society |volume=161 |issue=2 |pages=132–136 |year=2009|doi=10.1111/j.1095-8339.2009.00999.x|ref={{harvid|Chase et al|2009}}}}
* {{cite journal |first=Mark W. |last=Chase |first2=James L. |last2=Reveal |first3=Michael F. |last3=Fay |authorlink=Mark Chase|title=A subfamilial classification for the expanded asparagalean families Amaryllidaceae, Asparagaceae and Xanthorrhoeaceae |journal=Botanical Journal of the Linnean Society |volume=161 |issue=2 |pages=132–136 |year=2009|doi=10.1111/j.1095-8339.2009.00999.x|ref={{harvid|Chase et al|2009}}}}
* {{cite journal |last=Davis |first=J.I. |last2=Stevenson |first2=D.W. |last3=Petersen |first3=G. |last4=Seberg |first4=O. |last5=Campbell |first5=L.M. |last6=Freudenstein |first6=J.V. |last7=Goldman |first7=D.H. |last8=Hardy |first8=C.R. |last9=Michelangeli |first9=F.A. |last10=Simmons |first10=M.P. |last11=Specht |first11=C.D. |last12=Vergara-Silva |first12=F. |last13=Gandolfo |first13=M. |title=A phylogeny of the monocots, as inferred from ''rbcL'' and ''atpA'' sequence variation, and a comparison of methods for calculating jacknife and bootstrap values |journal=[[Syst. Bot.]] |date=July–September 2004 |volume=29 |issue=3 |pages=467–510 |url=http://www.ingentaconnect.com/content/aspt/sb/2004/00000029/00000003/art00001 |accessdate=4 January 2014 |doi=10.1600/0363644041744365|ref={{harvid|Davis et al|2004}}}}
* {{cite journal |last=Davis |first=J.I. |last2=Stevenson |first2=D.W. |last3=Petersen |first3=G. |last4=Seberg |first4=O. |last5=Campbell |first5=L.M. |last6=Freudenstein |first6=J.V. |last7=Goldman |first7=D.H. |last8=Hardy |first8=C.R. |last9=Michelangeli |first9=F.A. |last10=Simmons |first10=M.P. |last11=Specht |first11=C.D. |last12=Vergara-Silva |first12=F. |last13=Gandolfo |first13=M. |title=A phylogeny of the monocots, as inferred from ''rbcL'' and ''atpA'' sequence variation, and a comparison of methods for calculating jacknife and bootstrap values |journal=[[Syst. Bot.]] |date=July–September 2004 |volume=29 |issue=3 |pages=467–510 |url=http://www.ingentaconnect.com/content/aspt/sb/2004/00000029/00000003/art00001 |accessdate=4 January 2014 |doi=10.1600/0363644041744365|ref={{harvid|Davis et al|2004}}}}
* {{cite journal |last=Chase |first=M. W. |last2=Fay |first2=M. F. |last3=Devey |first3=D. S. |last4=Maurin |first4=O |last5=Rønsted |first5=N |last6=Davies |first6=T. J |last7=Pillon |first7=Y |last8=Petersen |first8=G |last9=Seberg |first9=O |last10=Tamura |first10=M. N. |last11=Asmussen |first11=C. B. |last12=Hilu |first12=K |last13=Borsch |first13=T |last14=Davis |first14=J. I |last15=Stevenson |first15=D. W. |last16=Pires |first16=J. C. |last17=Givnish |first17=T. J. |last18=Sytsma |first18=K. J. |last19=McPherson |first19=M. A. |last20=Graham |first20=S. W. |last21=Rai |first21=H. S. |authorlink=Mark Chase|title=Multigene analyses of monocot relationships : a summary |pages=63–75 |url=http://www.faculty.biol.vt.edu/hilu/Hilu_Lab_Website/Pictures/Hilu%20paper%20pdf/Chaseetal2006Monoct.pdf |accessdate=19 May 2015 |issn=00656275|ref={{harvid|Chase et al.|2006}}}} In {{Harvtxt|Columbus|Friar|Porter|Prince|2006}}
* {{cite journal |last=Chase |first=M. W. |last2=Fay |first2=M. F. |last3=Devey |first3=D. S. |last4=Maurin |first4=O |last5=Rønsted |first5=N |last6=Davies |first6=T. J |last7=Pillon |first7=Y |last8=Petersen |first8=G |last9=Seberg |first9=O |last10=Tamura |first10=M. N. |last11=Asmussen |first11=C. B. |last12=Hilu |first12=K |last13=Borsch |first13=T |last14=Davis |first14=J. I |last15=Stevenson |first15=D. W. |last16=Pires |first16=J. C. |last17=Givnish |first17=T. J. |last18=Sytsma |first18=K. J. |last19=McPherson |first19=M. A. |last20=Graham |first20=S. W. |last21=Rai |first21=H. S. |authorlink=Mark Chase|title=Multigene analyses of monocot relationships : a summary |pages=63–75 |url=http://www.faculty.biol.vt.edu/hilu/Hilu_Lab_Website/Pictures/Hilu%20paper%20pdf/Chaseetal2006Monoct.pdf |accessdate=19 May 2015 |issn=00656275|ref={{harvid|Chase et al.|2006}}}} In {{Harvtxt|Columbus|Friar|Porter|Prince|2006}}
* {{cite journal|last1=Gao|first1=Yun-Dong|last2=Zhou|first2=Song-Dong|last3=He|first3=Xing-Jin|last4=Wan|first4=Juan|title=Chromosome diversity and evolution in tribe Lilieae (Liliaceae) with emphasis on Chinese species|journal=Journal of Plant Research|date=11 May 2011|volume=125|issue=1|pages=55–69|doi=10.1007/s10265-011-0422-1|ref={{harvid|Gao et al|2012}}}}
* {{cite journal |last=Hilu |first=K. |last2=Borsch |first2=T. |last3=Muller |first3=K. |last4=Soltis |first4=D.E. |last5=Soltis |first5=P.S. |last6=Savolainen |first6=V. |last7=Chase |first7=M.W. |last8=Powell |first8=M.P. |last9=Alice |first9=L.A. |last10=Evans |first10=R. |last11=Sauquet |first11=H. |last12=Neinhuis |first12=C. |last13=Slotta |first13=T.A.B. |last14=Rohwer |first14=J.G. |last15=Campbell |first15=C.S. |last16=Chatrou |first16=L.W. |title=Angiosperm phylogeny based on ''<011>'' ''matK'' sequence information |journal=[[American Journal of Botany]] |date=December 2003 |volume=90 |issue=12 |pages=1758–1766 |doi=10.3732/ajb.90.12.1758 |url=http://www.amjbot.org/cgi/content/full/90/12/1758 |accessdate=4 January 2014|ref={{harvid|Hilu et al|2003}}}}
* {{cite journal |last=Givnish |first=T.J. |last2=Pires |first2=J.C. |last3=Graham |first3=S.W. |last4=McPherson |first4=M.A. |last5=Prince |first5=L.M. |last6=Patterson |first6=T.B. |last7=Rai |first7=H.S. |last8=Roalson |first8=E.R. |last9=Evans |first9=T.M. |last10=Hahn |first10=W.J |last11=Millam |first11=K.C. |last12=Meerow |first12=A.W. |last13=Molvray |first13=M. |last14=Kores |first14=P. |last15=O'Brien |first15=H.E. |last16=Kress |first16=W.J. |last17=Hall |first17=J. |last18=Sytsma |first18=K.J. |title=Repeated evolution of net venation and fleshy fruits among monocots in shaded habitats confirms ''a priori'' predictions: evidence from an ''ndhF'' phylogeny |journal=Proceedings of the Royal Society of London, Series B| year=2005| volume=272 |pages=1481–1490 |pmc=1559828 |pmid=16011923 |doi=10.1098/rspb.2005.3067|ref={{harvid|Givnish et al|2005}}}}
* {{cite journal |last=Givnish |first=T.J. |last2=Pires |first2=J.C. |last3=Graham |first3=S.W. |last4=McPherson |first4=M.A. |last5=Prince |first5=L.M. |last6=Patterson |first6=T.B. |last7=Rai |first7=H.S. |last8=Roalson |first8=E.R. |last9=Evans |first9=T.M. |last10=Hahn |first10=W.J |last11=Millam |first11=K.C. |last12=Meerow |first12=A.W. |last13=Molvray |first13=M. |last14=Kores |first14=P. |last15=O'Brien |first15=H.E. |last16=Kress |first16=W.J. |last17=Hall |first17=J. |last18=Sytsma |first18=K.J. |title=Repeated evolution of net venation and fleshy fruits among monocots in shaded habitats confirms ''a priori'' predictions: evidence from an ''ndhF'' phylogeny |journal=Proceedings of the Royal Society of London, Series B| year=2005| volume=272 |pages=1481–1490 |pmc=1559828 |pmid=16011923 |doi=10.1098/rspb.2005.3067|ref={{harvid|Givnish et al|2005}}}}
* {{cite journal |last=Graham |first=S.W. |last2=Zgurski |first2=J.M. |last3=McPherson |first3=M.A. |last4=Cherniawsky |first4=D.M. |last5=Saarela |first5=J.M. |last6=Horne |first6=E.S.C. |last7=Smith |first7=S.Y. |last8=Wong |first8=W.A. |last9=O'Brien |first9=H.E. |last10=Biron |first10=V.L. |last11=Pires |first11=J.C. |last12=Olmstead |first12=R.G. |last13=Chase |first13=M.W. |last14=Rai |first14=H.S. |title=Robust inference of monocot deep phylogeny using an expanded multigene plastid data set |pages=3–21 |url=http://depts.washington.edu/phylo/OlmsteadPubs/Graham.2006.Aliso.pdf |accessdate=4 January 2014|ref={{harvid|Graham et al|2006}}}} In {{Harvtxt|Columbus|Friar|Porter|Prince|2006}}
* {{cite journal |last=Graham |first=S.W. |last2=Zgurski |first2=J.M. |last3=McPherson |first3=M.A. |last4=Cherniawsky |first4=D.M. |last5=Saarela |first5=J.M. |last6=Horne |first6=E.S.C. |last7=Smith |first7=S.Y. |last8=Wong |first8=W.A. |last9=O'Brien |first9=H.E. |last10=Biron |first10=V.L. |last11=Pires |first11=J.C. |last12=Olmstead |first12=R.G. |last13=Chase |first13=M.W. |last14=Rai |first14=H.S. |title=Robust inference of monocot deep phylogeny using an expanded multigene plastid data set |pages=3–21 |url=http://depts.washington.edu/phylo/OlmsteadPubs/Graham.2006.Aliso.pdf |accessdate=4 January 2014|ref={{harvid|Graham et al|2006}}}} In {{Harvtxt|Columbus|Friar|Porter|Prince|2006}}
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* {{cite journal |last=Pires |first=J.C. |last2=Maureira |first2=I.J. |last3=Givnish |first3=T.J. |last4=Sytsma |first4=K.J. |last5=Seberg |first5=O. |last6=Petersen |first6=G. |last7=Davis |first7=J.I. |last8=Stevenson |first8=D.W. |last9=Rudall |first9=P.J. |last10=Fay |first10=M.F. |last11=Chase |first11=M.W. |title=Phylogeny, genome size, and chromosome evolution of Asparagales |year=2006 |volume=22 |pages=278–304 |id={{INIST|18269727}}|ref={{harvid|Pires et al|2006}} }}
* {{cite journal |last=Pires |first=J.C. |last2=Maureira |first2=I.J. |last3=Givnish |first3=T.J. |last4=Sytsma |first4=K.J. |last5=Seberg |first5=O. |last6=Petersen |first6=G. |last7=Davis |first7=J.I. |last8=Stevenson |first8=D.W. |last9=Rudall |first9=P.J. |last10=Fay |first10=M.F. |last11=Chase |first11=M.W. |title=Phylogeny, genome size, and chromosome evolution of Asparagales |year=2006 |volume=22 |pages=278–304 |id={{INIST|18269727}}|ref={{harvid|Pires et al|2006}} }}
* {{cite journal|last=Rønsted|first=N. |first2=S.|last2=Law |first3=H. |last3=Thornton |first4=M. F. |last4=Fay |first5=M. W. |last5=Chase|title=Molecular phylogenetic evidence for the monophyly of ''Fritillaria'' and ''Lilium'' (Liliaceae; Liliales) and the infrageneric classification of ''Fritillaria''|journal=Molecular Phylogenetics and Evolution|year=2005|volume=35|pages=509–527|pmid=15878122|doi=10.1016/j.ympev.2004.12.023|issue=3|ref={{harvid|Rønsted et al|2005}}}}
* {{cite journal|last=Rønsted|first=N. |first2=S.|last2=Law |first3=H. |last3=Thornton |first4=M. F. |last4=Fay |first5=M. W. |last5=Chase|title=Molecular phylogenetic evidence for the monophyly of ''Fritillaria'' and ''Lilium'' (Liliaceae; Liliales) and the infrageneric classification of ''Fritillaria''|journal=Molecular Phylogenetics and Evolution|year=2005|volume=35|pages=509–527|pmid=15878122|doi=10.1016/j.ympev.2004.12.023|issue=3|ref={{harvid|Rønsted et al|2005}}}}
* {{cite journal |last=Rudall |first=P. |last2=Furness |first2=C.A. |last3=Chase |first3=M.W. |last4=Fay |first4=M.F. |title=Microsporogenesis and pollen sulcus type in Asparagales (Lilianae) |journal=[[Canad. J. Bot.]] |year=1997 |volume=75 |issue=3 |pages=408–430 |id={{INIST|10769694}} |issn=0008-4026 |doi=10.1139/b97-044|ref={{harvid|Rudall et al|1997a}}}}
* {{cite journal|last =Shinwari|first= Z. K.|last2=Terauchi|first2=R. |last3=Hteck|first3= F. H. |last4=Kawano|first4=S. |year=1994|title=Recognition of the New World ''Disporum'' section ''Prosartes'' (Liliaceae) based on the sequence data of the ''rbcL'' gene.|journal=Taxon|volume=43|issue=3|pages=353–366|jstor=1222713|doi=10.2307/1222713|ref={{harvid|Shinwari et al|1994}}}}
* {{cite journal|last =Shinwari|first= Z. K.|last2=Terauchi|first2=R. |last3=Hteck|first3= F. H. |last4=Kawano|first4=S. |year=1994|title=Recognition of the New World ''Disporum'' section ''Prosartes'' (Liliaceae) based on the sequence data of the ''rbcL'' gene.|journal=Taxon|volume=43|issue=3|pages=353–366|jstor=1222713|doi=10.2307/1222713|ref={{harvid|Shinwari et al|1994}}}}
* {{cite journal |last=Soltis |first=D. E. |last2=Soltis |first2=P.S. |last3=Chase |first3=M.W. |last4=Mort |first4=M.E. |last5=Albach |first5=D.C. |last6=Zanis |first6=M. |last7=Savolainen |first7=V. |last8=Hahn |first8=W.H. |last9=Hoot |first9=S.B. |last10=Fay |first10=M.F. |last11=Axtell |first11=M. |last12=Swensen |first12=S.M. |last13=Prince |first13=L.M. |last14=Kress |first14=W.J. |last15=Nixon |first15=K.C. |last16=Farris |first16=J.S. |title=Angiosperm phylogeny inferred from 18S rDNA, rbcL, and ''atpB'' sequences |journal=Bot. J. Linn. Soc. |year=2000 |volume=133 |issue=4 |pages=381–461 |doi=10.1006/bojl.2000.0380|ref={{harvid|Soltis et al|2000}}}}
* {{cite journal |last=Soltis |first=D. E. |last2=Soltis |first2=P.S. |last3=Chase |first3=M.W. |last4=Mort |first4=M.E. |last5=Albach |first5=D.C. |last6=Zanis |first6=M. |last7=Savolainen |first7=V. |last8=Hahn |first8=W.H. |last9=Hoot |first9=S.B. |last10=Fay |first10=M.F. |last11=Axtell |first11=M. |last12=Swensen |first12=S.M. |last13=Prince |first13=L.M. |last14=Kress |first14=W.J. |last15=Nixon |first15=K.C. |last16=Farris |first16=J.S. |title=Angiosperm phylogeny inferred from 18S rDNA, rbcL, and ''atpB'' sequences |journal=Bot. J. Linn. Soc. |year=2000 |volume=133 |issue=4 |pages=381–461 |doi=10.1006/bojl.2000.0380|ref={{harvid|Soltis et al|2000}}}}

Revision as of 11:26, 11 August 2015

Lilium candidum growing in Sardinia
Type species: Lilium candidum

The taxonomy of Liliaceae has had a complex history since the first description of this flowering plant family in the mid-eighteenth century. Originally, the Liliaceae or Lily family were defined as having a "calix" (perianth) of six equal-coloured parts, six stamens, a single style, and a superior, three-chambered (trilocular) ovary turning into a capsule fruit at maturity. The taxonomic circumscription of the Liliaceae family progressively expanded until it became the largest plant family and also extremely diverse, being somewhat arbitrarily defined as all species of plants with six tepals and a superior ovary. It eventually came to encompass about 300 genera and 4,500 species, and was thus a "catch-all" and hence paraphyletic taxon. Only since the more modern taxonomic systems developed by the Angiosperm Phylogeny Group (APG) and based on phylogenetic principles, has it been possible to identify the many separate taxonomic groupings within the original family and redistribute them, leaving a relatively small core as the modern Liliaceae family, with fifteen genera and 600 species.

The Liliaceae arose in Eurasia, around 68 million years ago with the development of two main evolutionary clades, the Lilieae (Lilium, Fritillaria) from the Himalayas, and the Tulipeae (Erythronium, Tulipa), (Gagea) from East Asia. Clintonia-Medeola may have appeared in North America but was subsequently dispersed, as may have the Calochortaceae sensu Tamura. Divergence amongst the Liliales probably occurred around 36 million years ago. Liliaceae fossils have been dated to the Paleogene and Cretaceous eras in the Antarctic.

The redefined Liliaceae ("Core Liliales") probably arose as shade plants, with subsequent evolution to open areas including deciduous forest in the more open autumnal period. This was accompanied by a shift from rhizomes to bulbs, to more showy flowers, the production of capsular fruit and narrower parallel-veined leaves.

While the suprageneric (above genus level) structure of the family has varied greatly with its ever-changing circumscription, as currently constituted it consists of three subfamilies, of which the Lilioideae is further divided into tribes, with fifteen genera and approximately 600 species.

History

Pre-Darwinian

The type genus, Lilium, from which the name of the family was derived, was described by Carl Linnaeus in 1753, with seven species.[1] He placed Lilium within the Hexandria Monogynia (six stamens, one carpel) in his sexual classification in the Species Plantarum.[2]

The Liliaceae family was first described by Michel Adanson in 1763,[3][4] but formally named by Antoine Laurent de Jussieu in 1789.[5] Adanson described eight subfamilies with seventy eight genera, however the subfamily he described as "Lis" (Lilies) had seven genera (Uvularia, Mithridatium, Mendoni, Lilium, Imperialis (Fritillaria), Fritillaria and Tulipa) of which four are in the modern genus.[6] De Jussieu placed them as the fourth Ordo (Order: Lilia) of the third class (Stamina Perigyna) of Monocots, with eight genera (Tulipa, Erythronioum, Methonica, Uvularia, Fritillaria, Imperialis, Lilium, Yucca) only four of which remain in the family. However the use of the term Ordo at that time was closer to what we now understand as Family, rather than Order.[7][8] Although Jussieu used the term "Lilia" in his Genera Plantarum, elsewhere he used the French term "Liliacées",[9] as had Adanson before him using both French and Latin, and the word "Liliaceae" was soon widely used by botanists such as Samuel Frederick Gray,[10] John Lindley,[11] and Pierre-Joseph Redouté[12] in the early nineteenth century. Jussieu defined this grouping as having a "calyx" of six equal coloured parts (perianth), six stamens, a superior ovary, single style, and trilocular capsule. Gray (1821) provided the first description of Jussieu's scheme in English, identifying two genera occurring in Britain (Tulipa, Fritillaria), distinguished by the absence or presence of basal nectaries. His key used the presence of six stamens, a single style, equal stamina, a simple petaloid perianth and a trilocular capsule with flat seeds to identify the family.[13] Although De Candolle (1813) had not explicitly described the Liliaceae, his overall classification scheme influenced many later writers including Gray.[14] In this scheme, [15] the Liliaceae were considered a family within the Endogenæ phanerogamæ, that is those vascular plants (Vasculares) whose vascular bundles were thought to arise from within (Endogènes, endogenous), a term he preferred to monocots (Monocotylédonés). Of these, the true monocots of Jussieu became the Phanerogams or Phanérogames (Phenogamae in Gray), hence Endogenæ phanerogamæ.[16] Candolle also instituted the concept of ordered ranks, based on classes, subclasses, familles (Latin: ordines naturales) and tribus (tribes),[8] subdividing the Liliaceae.

Lindley was the first English systematist, publishing his work in 1830,[17] and following the reasoning of Jussieu he used the term tribe to describe the Liliaceae as a division of the hexapetaloid monocots, characterised by a superior ovary, highly developed perianth, inward turning anthers, a trilocular polyspermous capsule and seeds with a soft spongy coat. He offered seven genera as examples (Erythronium, Lilium, Calochortus, Blandfordia, Polianthes, Hemerocallis and Funkia). By 1846, in his final work, he refined and greatly expanded his taxonomy further favouring the term Alliances of Endogens over monocots, as a class, with eleven alliances including the Liliales. This includes four Orders (families) including Liliaceae which he referred to as lilyworts in the vernacular. In this work he unhappily acknowledged the great diversity in the circumscription of the order, and that it had expanded vastly, with many subdivisions. As he saw it, the Liliaceae were already paraphyletic ("catch-all"),[18] being all Liliales not included in the other orders, but hoped that the future would reveal some characteristic that would group them better. He recognised 133 genera and 1200 species.[19] By the time of the next major British classification, that of Bentham and Hooker in 1883 (published in Latin) several of Lindley's other families had been absorbed into the Liliaceae.[20] This was the last major classification using the natural approach.[21]

Post-Darwinian

Although Charles Darwin's Origin of Species (1859) preceded Bentham and Hooker's publication, the latter project was commenced much earlier and Bentham was initially sceptical of Darwinism.[21] The new phyletic approach changed the way that taxonomists considered plant classification, incorporating evolutionary information into their schemata, but this did little to further define the circumscription of Liliaceae.[22] The major works in the late nineteenth and early twentieth century employing this approach were German, those of Eichler (1875–1886), Engler and Prantl (1886–1924) and Wettstein (1901–1935). These placed the Liliaceae into one of the major subdivisions of the monocotyledons, the Liliiflorae.[23][24][25]

Fritillaria ophioglossifolia, R Wettstein Handbuch der Systematischen Botanik 1901–1924

In the English literature, Bessey (1915) followed Engler in defining Liliaceae as "Pistil mostly 3-celled; stamens 6; perianth of two similar whorls, each of three similar leaves", although placing the Liliales in a novel subclass of monocots, the Strobiloideae,[26] while from Hutchinson (1959) onwards the Liliaceae were treated as part of the Liliales.

Over time the Liliaceae became increasingly broadly, and somewhat arbitrarily defined as all species of plants with six tepals and a superior ovary. They eventually came to encompass about 300 genera and 4,500 species, within the order Liliales in the scheme of Arthur Cronquist (1981) who merged it with the Amaryllidaceae.[27] Later similar schemes include the system of Robert F. Thorne[28] and that of Armen Takhtajan.[29] They were characterised as petaloid monocots, characterised by showy flowers with tepals and without starch in the endosperm. Cronquist had placed most flowering petaloid monocots with six stamens in this very broad (and clearly polyphyletic) family.[30][31] He rejected the importance of ovary position and thus included the Amarylloidaceae, some species of which had an inferior ovary, and which others separated into a distinct family,[32] although this then created other problems.[33] The Liliaceae were one of the major families in the Cronquist system which considerably broadened the circumscription to include 22 families in addition to Liliaceae s.s..[34]

Deconstructing Liliaceae

Other botanists in the twentieth century echoed Lindley's concerns about the phylogeny of the Liliaceae. The earliest of these was Johannes Paulus Lotsy,[35] (1911) building on Wettstein's work. Lotsy suggested four separate families, Liliaceae, Alliaceae, Agapanthaceae and Gilliesiaceae, within the Liliifloren. This recognised the major groupings that would later be transferred to Amaryllidaceae as subfamilies Allioideae and Agapanthoideae, with Gilliesieae as a tribe within the Allioideae. This approach was later followed by Huber in 1969.[36] These various proposals to separate small groups of genera into more homogeneous families made little impact until Dahlgren (1985) developed a system incorporating new information, including synapomorphic characters (i.e., shared characters believed to have evolved from a common ancestor).[30][31] Where Cronquist saw one family, Dahlgren saw forty distributed over three orders (predominantly Liliales and Asparagales).[37][38] Over the 1980s, in the context of a more general review of the classification of angiosperms, the Liliaceae were subjected to more intense scrutiny. By the end of that decade, the Royal Botanic Gardens at Kew, the British Museum of Natural History and the Edinburgh Botanical Gardens formed a committee to examine the possibility of separating the family into smaller taxa, at least for the purpose of organizing their herbaria. That committee finally recommended that 24 new families be created in the place of the original broad Liliaceae, largely by elevating subfamilies to the rank of separate families.[39]

The 1990s saw considerable progress in plant phylogenetics and cladistic theory, enabling a phylogenetic tree to be constructed for the flowering plants. The establishment of major new clades necessitated a departure from the older but widely used classifications such as Cronquist and Thorne, based largely on morphology rather than genetic data. These developments complicated discussions on plant evolution and necessitated a major taxonomic restructuring.[40] rbcL gene sequencing and cladistic analysis of monocots in 1995 had redefined the Liliales order[41] out of four original morphological orders sensu Dahlgren. The largest clade, representing the Liliaceae, had all previously been included in the Liliales, but also included both the Calochortaceae and Liliaceae sensu Tamura. This redefined Liliaceae, that became referred to as "core Liliales", corresponded to the emerging circumscription of the family in the Angiosperm Phylogeny Group system (1998).[42]

Modern APG classification

To meet the need for a thorough revision of the taxonomy of the flowering plants (angiosperms), systematists formed the Angiosperm Phylogeny Group (APG), resulting in a new classification published in 1998.[43] The scheme was largely based on the work of Kåre Bremer and colleagues at Uppsala and Stockholm universities in the late 1970s,[44][45][46] which became available on the internet in 1996.[47] It was an ordinal system, concentrating on orders rather than families, prioritising monophyly. However progress was rapid and the modern era of the taxonomy of the Liliaceae family comes from Walter S. Judd and colleagues[33] (second edition 2002), the APG II (2003[48]) and APG III (2009[40]), while the Linear APG III assigned it the family number 61.[49] While the original APG did not specifically address the issues of the polyphyly within Liliaceae, APG II did so within the two closely morphologically related orders, Liliales and Asparagales[50] recognising the continued common use of Liliaceae in the broad sense (sensu lato, s.l.).

These studies of DNA and morphological data (particularly reproductive morphology) together with phylogenetic analyses, allowed the conclusion that the "petaloid monocots" do not belong to one botanical family but rather are distributed across two separate orders, the Asparagales and Liliales. The monophyly of these newly defined orders is supported by cladistic analysis based on morphology, 18S rDNA, the plastid gene rbcL, and other DNA sequences.[51][52][53][54][55][56][57][58][59][60][61][62][63][64][65][66][67][68][69]

These studies, together with other analyses within each of these two orders, allowed the redistribution of the original genera of Liliaceae sensu lato into a variety of families, as illustrated in the cladogram of the Liliales and Asparagales shown below.[70] This redistribution resulted in considerable changes both in the suprafamilial positioning of Liliaceae within the overall APG classification (as shown in Table 1 below), as well as the subfamilial structure (see Suprageneric subdivisions).

Table 1: Evolution of placement of Liliaceae in different taxonomic schemes[22]
Rank Bentham and Hooker (1883)[20] Cronquist (1981)[27] Takhtajan (1980)[71] Dahlgren (1985)[30][31] Thorne (1992)[28] APG (2003-9)[48][40]
Division Magnoliophyta Magnoliophyta
Class Monocotyledons Liliopsida Liliopsida Liliopsida Angiospermae
Subclass Liliidae Liliidae Liliidae Liliidae
Superorder (Series) Coronarieæ Dioscoreanae Liliiflorae Lilianae Monocots
Order Liliales Liliales Liliales Liliales Liliales
For a comparison of the classifications of genera from 1959 (Hutchinson)[72] to 2000 (Wilson and Morrison),[73] see Table 1 in Fay et al. 2006[74] and Table 1 in Peruzzi et al. 2009.[75]

Cladistic analysis of Liliales and families within former Liliaceae

Cladogram I: Phylogeny of Liliaceae and related families in Liliales and Asparagales
Phylogenetic tree reflecting relationships based on molecular phylogenetic evidence.[50][76] L denotes families that have traditionally been placed in Liliaceae, A those formerly placed in Amaryllidaceae, itself sometimes treated as part of the Liliaceae. Agavaceae has been included in either of the two.O families originally in other orders

Within the Liliales, cladistic analysis revealed the Liliaceae as one of four main groupings.[50] The original Liliaceae family in the broad sense (sensu lato, s.l.), which encompassed a large number of differing groups of genera, was highly polyphyletic (see cladogram). This led to botanists increasingly adopting a more narrow monophyletic concept, i.e. strict sense (sensu stricto, s.s.) of the family based on molecular phylogenetic relationships, as expressed in the 2009 APG III system, rather than the older broad (sensu lato) one. Former members of the Liliaceae are now principally classified in different families and subfamilies of the Liliales and Asparagales as shown in the cladogram. Other families and orders containing former Liliaceae taxa are the Nartheciaceae (Dioscoreales), Tofieldiaceae (Alismatales), Tecophilaeaceae (Asparagales) and the former Uvulariaceae.

Changes to family structure in APG III

The APG III system when it was published in 2009, greatly expanded the families Xanthorrhoeaceae, Amaryllidaceae, and Asparagaceae.[77] Thirteen of the families of the earlier APG II system were thereby reduced to subfamilies. The APG II families and their equivalent APG III subfamilies are as follows:

Phylogeny

Sequencing of the rbcL and matK chloroplast genes of Lilium and related genera[78] confirmed the circumscription of the family in the sensu stricto usage of Tamura (1998).[79] Chloroplast ndhF gene sequencing also supported Liliaceae monophyly, reuniting the Liliaceae and Calochortaceae sensu Tamura.[42][74]

Despite establishing this relative degree of monophyly for the Liliaceae family,[41][80] morphology remains diverse,[79] and there exists within the Liliaceae clade a number of subclades. Particularly enigmatic were Clintonia, Medeola, Scoliopus, and Tricyrtis. Clintonia, with a disjunct distribution involving East Asia and North America, and the closely related Medeola form one of those subclades and are now considered a separate tribe (Medeoleae) within the Lilioideae, although at different times they have been considered a separate subfamily (Medeoloideae) or family (Medeolaceae). Sequencing of the rbcL and matK chloroplast genes established monophyly for Clintonia, but with separate clades corresponding to the two areas of distribution.[81]

Characteristics

The diversity of characteristics complicates description of Liliaceae morphology, and confused taxonomic classification for centuries. The diversity is also of considerable evolutionary significance(see Evolution).[42] The Liliaceae family are characterised as monocotyledonous, perennial, herbaceous, bulbous (or rhizomatous in the case of Medeoleae)[79] flowering plants with simple trichomes (root hairs) and contractile roots.[82] The flowers may be arranged (inflorescence) along the stem, developing from the base, or as a single flower at the tip of the stem, or as a cluster of flowers. They contain both male (androecium) and female (gynoecium) characteristics and are symmetric radially, but sometimes as a mirror image. Most flowers are large and colourful, except for Medeoleae. Both the petals and sepals are usually similar and appear as two concentric groups (whorls) of 'petals', that are often striped or multi-coloured, and produce nectar at their bases. The stamens are usually in two groups of three (trimerous) and the pollen has a single groove (monosulcate). The ovary is placed above the attachment of the other parts (superior). There are three fused carpels (syncarpus) with one to three chambers (locules), a single style and a three-lobed stigma. The embryo sac is of the Fritillaria type. The fruit is generally a wind dispersed capsule, but occasionally a berry (Medeoleae) which is dispersed by animals. The leaves are generally simple and elongated with veins parallel to the edges, arranged singly and alternating on the stem, but may form a rosette at the base of the stem.

The ten genera of the Lilioideae subfamily are characterised by contractile bulbs and roots and a megagametophyte (embryo-sac) of the Fritillaria-type with four megaspores. The five genera constituting the Streptopoideae and Calochortoideae subfamilies form another distinct group, previously characterised under the Calochortoideae alone. These have creeping rhizomes, styles divided at their apices, and an embryo-sac of the Polygonum-type with a simple megaspore and triploid endosperm. At times, these genera were considered as a separate family (Calochortaceae; e.g. Tamura) or even placed in the more heterogeneous Uvulariaceae sensu Dahlgren. However most of the latter had low morphological similarity to the Liliaceae, and Uvularia and Disporum are now classified in the Colchicaceae. Disporum contained both Asian and North American species which had always been distinguishable. Following molecular analysis, the North American species were restored to the genus Prosartes and retained in Liliaceae, subfamily Streptopoideae, while the Asian species were moved to Colchicaceae.[83]

Evolution

Angiosperms (flowering plants) date to the Early Cretaceous period, about 100 million years ago (mya).[65] The development of a phylogenetic approach to taxonomy, starting with Charles Bessey's The phylogenetic taxonomy of flowering plants (1915) suggested the Liliales formed some of the earliest monocots,[26] with an estimated date of origin of 82 mya.[65] Molecular analysis suggests that Liliaceae arose in Eurasia, around 68 mya during the late (Maastrichtian) Cretaceous to early (Paleocene) Paleogene periods as part of one of the four major clades of Liliales, that would later diverge with the separation of this clade into Liliaceae sensu Tamura and its sister clade Smilaceae at 52 mya.[65][84]

Within the Liliaceae there developed two main evolutionary clades, The first of these, characterised as Lilieae (Lilium, Fritillaria, Nomocharis), Cardiocrinum), Notholirion) from the Himalayas, and the second, the Tulipeae (Erythronium, Tulipa), (Gagea) from East Asia. On the other hand, Clintonia-Medeola may have appeared in North America but was subsequently dispersed, as may have the Calochortaceae sensu Tamura. Divergence amongst the Liliales probably occurred around 36 mya, with the Liliaceae sensu Tamura emerging at 27 mya, Liliaceae sensu stricto (s.s) and Lilioideae at 20 mya (Miocene), Lilieae 12 mya and Calochortus 7 mya.[42][84] Liliaceae fossils have been dated to the Paleogene[85] and Cretaceous periods.[86]

Core Liliales probably arose as shade plants, with subsequent evolution of Liliaceae s.s. and Calochortus to open areas including deciduous forest in the more open autumnal period, but then a return of some species (e.g. Cardiocrinum). This was accompanied by a shift from rhizomes to bulbs, to more showy flowers, the production of capsular fruit and narrower parallel-veined leaves. Again, some reversal to the broader reticulate-veined leaves occurred (e.g. Cardiocrinum). [42]

Subdivisions and genera

Leaves and fruit of Clintonia, an example of Medeolae
Leaves and fruit of Clintonia borealis (Medeoleae) growing in Canada
Flower of Nomocharis, an example of Lilieae
Flower of Nomocharis aperta (Lilieae) growing in China
Flower of Calochortus, an example of Calochortoideae
Flower of Calochortus catalinae (Calochortoideae) growing in California
Leaves and fruit of Streptopus, an example of Streptopoideae
Leaves and berries of Streptopus lanceolatus, North America (Streptopoideae)

Suprageneric subdivisions

Due to the diversity of the originally broadly defined Liliaceae s.l., many attempts have been made to form supageneric classification systems, organizing the genera into subfamilies, tribes, or other suprageneric taxa (taxonomic groupings between genus and family).[75] By 1813, Candolle recognised five subdivisions which he called tribes (Asparagées, Trilliacées, Asphodelées, Bromeliées, Tulipacées),[15] all of which Jussieu had made separate families, with the exception of Tulipa, which was a genus within the Liliaceae. By 1845, John Lindley observed that the family had become extremely diverse, ill-defined and unstable, not only by its overall circumscription, but also by its subdivisions. For the 133 genera he included, he described eleven suborders.[19]

In 1879, a revision of the North American Liliaceae by Sereno Watson described sixteen tribes,[87] Bentham and Hooker described twenty tribes in 1883, and Engler and Prantl in their extensive description of the Liliaceae in 1899 identified 31 tribes distributed over 11 subfamilies.[88] In 1936, Franz Buxbaum undertook a major revision of the Liliaceae and among others described the subfamily Lilioideae with three tribes: Lloydieae, Tulipeae and Lilieae.[89][90][91] The complex rearrangements of the various genera, tribes and subfamilies over a 30 year period from 1985, discussed by Peruzzi and colleagues (2009),[75] are partly summarised in Table 2 below.

Classifications published since the use of molecular phylogenetics have taken a narrower view of the Liliaceae. In 1998, Tamura considered Calochortus sufficiently distinct to elevate the subfamily Calochortoideae to family status as Calochortaceae.[79][92] In 2009, Takhtajan used a very narrow definition (see the table below).[71] As of January 2014, the Angiosperm Phylogeny Website (APweb)[76] included four of Takhtajan's families in Liliaceae, recognizing three subfamilies, one of which is divided into two tribes.[93]

Table 2: Comparison of Four 21st Century Classifications of the Liliaceae
Tamura[79] Takhtajan[71] Taxonomicon[94] APweb[93]
Family Subfamily Tribe Family Tribe Family Subfamily Tribe Family Subfamily Tribe
Liliaceae Lilioideae Lilieae Liliaceae Lloydieae Liliaceae Lilioideae Lloydieae Liliaceae Lilioideae Lilieae
Lilieae Lilieae
Tulipeae Tulipeae Tulipeae
Medeoloideae Medeolaceae Medeola, Clintonia Medeoleae
Calochortaceae Calochorteae Scoliopaceae Calochortoideae Calochortoideae
Tricyrtideae Tricyrtidaceae Streptopoideae Streptopoideae

Genera

History

The Cronquist system (1981) had nearly 300 genera in Liliaceae. Most of those have been reassigned to other families, as shown here, following ITIS, together with their disposition as APG III transfers to other families (including subfamilies and orders other than Liliales where applicable) in brackets (Family: Subfamily, Order). Current members of Liliaceae in bold:

Template:Multicol

(Asian species. N American species restored as Prosartes D. Don)

Template:Multicol-break

(Asparagaceae: Nolinoideae, Asparagales)

|}

The following includes other genera that have historically been classified in family Liliaceae s.l.:

Modern classification

Various authorities (e.g. ITIS 16,[95] GRIN 27,[96] WCSP,[97] NCBI,[98] DELTA[99]) differ on the exact number of genera included in Liliaceae s.s., but generally there are about fifteen to sixteen genera, depending on whether or not Amana is included in Tulipa and Lloydia in Gagea. For instance Amana is still listed separately in WCSP.

Currently the APWeb lists fifteen genera, arranged as follows:[76]

AP WEB Distribution of Subfamilies, Tribes and Genera of Liliaceae
Subfamily Tribe Genus
Lilioideae Eaton Medeoleae Benth. (synonyms: Medeolaceae Takht., Medeoloideae Benth.) Clintonia Raf. - bead lilies
Medeola Gronov. ex L. - Indian cucumber-root
Lilieae Ritgen (synonyms: Erythroniaceae Martinov, Fritillariaceae Salisb., Liriaceae Borkh., Tulipaceae Borkh.)






(Some classifications place Tulipa and Erythronium into a separate tribe: Tulipeae)[75]
Cardiocrinum (Endl.) Lindl. - giant lilies
Fritillaria Tourn. ex L. – fritillary or mission bells
Gagea Salisb. (including Lloydia Salisb. ex Rchb.)
– yellow star-of-Bethlehem
Lilium Tourn. ex L. – lily
Nomocharis Franch.
Notholirion Wall. ex Boiss.
Tulipa L. (including Amana Honda) – tulip
Erythronium L. – trout lily
Calochortoideae Dumort. (synonyms: Calochortaceae Dumort., Compsoaceae Horan., nom. illeg., Tricyrtidaceae Takht., nom. cons.) Calochortus Pursh - mariposa, globe lilies
Tricyrtis Wall. – toad lily
Streptopoideae (synonym: Scoliopaceae Takht.) Prosartes D.Don – drops of gold
Scoliopus Torr. – Fetid Adder's Tongue
Streptopus Michx. – twistedstalk
Cladogram II: Phylogeny of the genera of the Liliaceae
Phylogenetic tree reflecting relationships based on molecular phylogenetic evidence.[65][75][84][100][101]

The largest genera are Gagea (200),[102] Fritillaria (130), Lilium (110), and Tulipa (75 species), all within the Lilieae tribe.

Etymology

From Lilium the type genus which is Latin for Lily, which in turn came from the Greek λείριον (leírion).

References

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Bibliography

Books

  • Goin, Francisco; Hospitaleche, Carolina Acosta; Dutra, Tania; Marenssi, Sergio (2012). Late Cretaceous/Paleogene West Antarctica Terrestrial Biota and its Intercontinental Affinities. Springer. ISBN 94-007-5491-4. Retrieved 28 January 2014.
  • Mabberley, David J (2013). Mabberley's Plant-Book (3 ed.). Cambridge University Press. ISBN 1-107-78259-7. Retrieved 8 January 2014. {{cite book}}: Invalid |ref=harv (help)
  • Redouté, P. J. (1802–1816). Les liliacées. Paris: Redouté. Retrieved 2 February 2014. {{cite book}}: Invalid |ref=harv (help)
  • Stilwell, Jeffrey D.; Feldmann, Rodney M., eds. (2000). Paleobiology and Paleoenvironments of Eocene Rocks: McMurdo Sound, East Antarctica. American Geophysical Union. ISBN 0-87590-947-7. {{cite book}}: Invalid |ref=harv (help)
  • Kamenetsky, Rina; Okubo, Hiroshi, eds. (2012). Ornamental Geophytes: From Basic Science to Sustainable Production. CRC Press. ISBN 1-4398-4924-2. {{cite book}}: Invalid |ref=harv (help)

Systematics and taxonomy

Taxonomic classifications

Table of 58 families, Part II: Page 1
Table of 1615 genera, Part II: Page 8

Articles

APG

Symposia

Websites

Databases

Template:Taxonids

  • The dictionary definition of Liliaceae at Wiktionary
  • Media related to Liliaceae at Wikimedia Commons