Botanical Journal of the Linnean Society, 2016, 182, 719722.

EDITORIAL
Towards stable classifications
MICHAEL F. FAY1,2
1
2

Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK

School of Plant Biology, University of Western Australia, Crawley, WA 6009, Australia

Classifications of plants and other organisms were

historically compiled by one or a few people, who
often disagreed with each other about which characters should be emphasized. Technological improvements in DNA sequencing in the 1990s allowed
systematists to break away from this tradition and,
for flowering plants, this led to the Angiosperm Phylogeny Group (APG) system, the fourth iteration of
which was published earlier this year (APG IV,
2016).
In the two and a half centuries following the publication of Species Plantarum (Linnaeus, 1753), many
botanists endeavoured to come up with more natural
systems, using more characters, with the intention of
recognizing groups that more closely reflected relationships. However, even readily diagnosable groups
such as orchids or legumes were treated as one family in some classifications and as several families in
others.
In the early 1990s, the first large analyses of
angiosperms based on DNA sequences were published. These had become possible due to major
developments in DNA sequencing technology and
computing power in the late 20th century. Flowering
plants were the first major group on which a large
group of scientists collaborated in comprehensive
analyses of this type, collecting sequences for the
same genes, so that the data could be combined. A
landmark paper with an analysis of 500 flowering
plants and with > 40 co-authors was published by
Chase et al. (1993), based on sequences of rbcL,
revealing that, whereas the monocots were monophyletic, dicots were not. At lower levels, the phylogenetic trees also proved to be a mix of the expected
and the unexpected, with, for example, Nelumbonaceae, Platanaceae and Proteaceae forming a
clade, despite the lack of obvious shared characters.
Following the collection of data sets for several
additional loci (revealing similar patterns of

relationships), the first version of the APG classification was published (APG, 1998) in the Annals of the
Missouri Botanical Garden, with three compilers and
26 contributors from five countries. Three further
versions of the APG classification have since been
published (APG II, 2003; APG III, 2009; APG IV,
2016), each with multiple compilers and contributors.
The most recent version, APG IV, had ten compilers
and 15 contributors from six countries, and followed
an online survey (Christenhusz et al., 2015) and a
workshop held at Kew.
With each version of the APG classification, the
list of families and/or genera of uncertain position
has become shorter, with only seven genera being
listed in 2016. This is a result of the increase in our
understanding of angiosperm relationships as more
plants have been sampled and more DNA regions
have been investigated. Changes in APG IV on the
basis of published studies include placement of Petenaea Lundell in its own family (Petenaeaceae; Christenhusz et al., 2010) and recognition of Kewaceae for
the genus Kewa Christenh. (previously included in
Hypertelis E.Mey ex Fenzl in Molluginaceae; Christenhusz et al., 2014), but with each iteration, the
classification is becoming more and more stable.
Many botanic gardens and herbaria (including Kew)
have adopted the APG system (e.g. Wearn et al.,
2013); APG IV will not be the final version, but the
decreasing number of changes means that reorganizing collections to reflect changes is becoming less
arduous. The resulting system allows greater predictability than previous classifications, because the
groups that are recognized reflect evolutionary relationships of the flowering plants.
Such developments are also taking place with
other groups of organisms and Botanical Journal of
the Linnean Society has published papers clarifying
relationships among fungi and lichens (Divakar
et al., 2016; Smith, 2016; Widhelm et al., 2016; this

2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 182, 719722

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M. F. FAY

issue), algae (Maggs & Saunders, 2016), mosses

(Bisang et al., 2014; Caparr
os et al., 2016; Fedosov
et al., 2016; Vigalondo et al., 2016) and ferns (Rumsey
et al., 2014), in addition to angiosperms.
Fossil taxa present some particular challenges due
to the lack of complete specimens and the inability to
use molecular techniques, as illustrated by recent
papers by Carpenter et al. (2014) and Smith (2016)
and the comment on the latter by Auxier et al.
(2016; this issue). However, fossils also provide
opportunities for dating the origin of extant groups
of organisms (e.g. Iles et al., 2015; Smith & Gandolfo,
2015).
For extant taxa, molecular analyses allow for
studies of anatomical, chemical and cytogenetic
characters, among others, in a phylogenetic framework, and these studies in turn provide additional
information that helps in the placement of problematic taxa and informs inference of evolutionary
pathways. Among angiosperms, taxa that have been
studied in this way include Trithuria (Hydatellaceae; Sokoloff et al., 2014), Alismatales (Sokoloff,
von Mering & Remizowa, 2015), Arecaceae (Balslev,
Bernal & Fay, 2016; and references therein),
Bromeliaceae (Crayn et al., 2015; Palma-Silva et al.,
2016; and references therein), Poaceae (Arthan
et al., 2016), Xyridaceae (Oriani & Scatena, 2014),
Vitaceae (Ickert-Bond et al., 2015), Buxaceae (Oskolski et al., 2015), Icacinaceae (Byng et al., 2014),
Ericales (Lofstrand, von Balthazar & Sch
onenberger, 2015; Schneider et al., 2015), Gelsemiaceae
(Struwe et al., 2014), Apocynaceae (Surveswaran
et al., 2014) and Solanaceae (Aubriot, Singh &
Knapp, 2016a; Zamberlan et al., 2015).
In combination, phylogenetic and other studies are
leading to the placement of previously enigmatic
taxa including Cotylolabium Garay (Orchidaceae:
Borba et al., 2014), generic recircumscriptions (e.g.
Global Carex Group, 2015) and higher level reclassifications (e.g. Bone, Cribb & Buerki, 2015; Chase
et al., 2015). Finally, in this issue, we present papers
on fungi and lichens (Auxier et al., 2016; Widhelm
et al., 2016), Alismatales (Platonova et al., 2016;
Volkova et al., 2016), Amaryllidaceae (Souza et al.,
2016), Ranunculaceae (Lehtonen, Christenhusz &
Falck, 2016), Malvales (Aubriot, Singh & Knapp,
2016b; Aubriot et al., 2016b) and Malpighiales (Ghislain
et al., 2016). These and other similar papers are
leading towards ever more stable classifications.

REFERENCES
APG. 1998. An ordinal classification for the families of
flowering plants. Annals of Missouri Botanical Garden 85:
531553.

APG II. 2003. An update of the Angiosperm Phylogeny

Group classification for the orders and families of flowering
plants. Botanical Journal of the Linnean Society 141: 399
436.
APG III. 2009. An update of the Angiosperm Phylogeny
Group classification for the orders and families of flowering
plants: APG III. Botanical Journal of the Linnean Society
161: 105121.
APG IV. 2016. An update of the Angiosperm Phylogeny
Group classification for the orders and families of flowering
plants: APG IV. Botanical Journal of the Linnean Society
181: 120.
Arthan W, Traiperm P, Gale SW, Norsaengsri M,
Kethirun L. 2016. Re-evaluation of the taxonomic status
of Hackelochloa (Poaceae) based on anatomical and phenetic analyses. Botanical Journal of the Linnean Society
181: 224245.
Aubriot X, Singh P, Knapp S. 2016a. Tropical Asian species show that the Old World clade of spiny solanums
(Solanum subgenus Leptostemonum pro parte: Solanaceae)
is not monophyletic. Botanical Journal of the Linnean Society 181: 199223.
Aubriot X, Soulebeau A, Haevermans T, Schatz GE,
Cruaud C, Lowry II Porter P. 2016b. Molecular phylogenetics of Sarcolaenaceae (Malvales), Madagascars largest
endemic plant family. Botanical Journal of the Linnean
Society doi: 10.1111/boj.12485.
Auxier B, Bazzicalupo A, Betz E, Dee JM, Le Renard L,
Roushdy M, Schwartz C, Berbee M. 2016. No place
among the living: phylogenetic considerations place the
Palaeozoic fossil T. protuberans in Fungi but not in
Dikarya. A comment on M. Smith (2016). Botanical Journal
of the Linnean Society doi: 10.1111/boj.12479.
Balslev H, Bernal R, Fay MF. 2016. Palms emblems of
tropical forests. Botanical Journal of the Linnean Society
182: 195200.
Bisang I, Ehrl

en J, Persson C, Heden
as L. 2014. Family
affiliation, sex ratio and sporophyte frequency in unisexual
mosses. Botanical Journal of the Linnean Society 174: 163
172.
Bone RE, Cribb PJ, Buerki S. 2015. Phylogenetics of
Eulophiinae (Orchidaceae: Epidendroideae): evolutionary
patterns and implications for generic delimitation. Botanical Journal of the Linnean Society 179: 4356.
Borba EL, Salazar GA, Mazzoni-Viveiros S, Batista
JAN. 2014. Phylogenetic position and floral morphology
of the Brazilian endemic, monospecific genus Cotylolabium: a sister group for the remaining Spiranthinae
(Orchidaceae). Botanical Journal of the Linnean Society
175: 2946.
Byng JW, Bernardini B, Joseph JA, Chase MW, Utteridge TMA. 2014. Phylogenetic relationships of Icacinaceae
focusing on the vining genera. Botanical Journal of the Linnean Society 176: 277294.
Caparr

os R, Lara F, Draper I, Vicente M, Garilleti R.
2016. Integrative taxonomy sheds light on an old problem:
the Ulota crispa complex (Orthotrichaceae, Musci). Botanical Journal of the Linnean Society 180: 427451.

2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 182, 719722

TOWARDS STABLE CLASSIFICATIONS

Carpenter RJ, Bannister JM, Lee DE, Jordan GJ. 2014.
Nothofagus subgenus Brassospora (Nothofagaceae) leaf
fossils from New Zealand: a link to Australia and New
Guinea? Botanical Journal of the Linnean Society 174:
503515.
Chase MW, Cameron KM, Freudenstein JV, Pridgeon
AM, Salazar G, van den Berg C, Schuiteman A. 2015.
An updated classification of Orchidaceae. Botanical Journal
of the Linnean Society 177: 151174.
Chase MW, Soltis DE, Olmstead RG, Morgan D, Les DH,
Mishler BD, Duvall MR, Price RA, Hills HG, Qiu YL,
Kron KA, Rettig JH, Conti E, Palmer JD, Manhart
JR, Sytsma KJ, Michael HJ, Kress WJ, Karol KG,
Clark WD, Hedr

en M, Gaut BS, Jansen RK, Kim YJ,
Wimpee CF, Smith JF, Furnier GR, Strauss SH, Xiang
QY, Plunkett GM, Soltis PS, Swensen SM, Williams
SE, Gadek PA, Quinn CJ, Eguiarte LE, Golenberg E,
Learn GH Jr, Graham SW, Barrett SCH, Dayanandan
S, Albert VA. 1993. Phylogenetics of seed plants: an
analysis of nucleotide sequences from the plastid gene rbcL.
Annals of the Missouri Botanical Garden 80: 528580.
Christenhusz MJM, Brockington SF, Christin P-A, Sage
RF. 2014. On the disintegration of Molluginaceae: a new
genus and family (Kewa, Kewaceae) segregated from Hypertelis, and placement of Macarthuria in Macarthuriaceae.
Phytotaxa 181: 238242.
Christenhusz MJM, Fay MF, Clarkson JJ, Gasson P,
Morales Can J, Jim

enez Barrios JB, Chase MW.
2010. Petenaeaceae, a new angiosperm family in Huerteales with a distant relationship to Gerrardina (Gerrardinaceae). Botanical Journal of the Linnean Society 164:
1625.
Christenhusz MJM, Vorontsova MS, Fay MF, Chase
MW. 2015. Results from an online survey of family delimitation in angiosperms and ferns: recommendations to the
Angiosperm Phylogeny Group for thorny problems in plant
classification. Botanical Journal of the Linnean Society 178:
501528.
Crayn DM, Winter K, Schulte K, Smith JAC. 2015. Photosynthetic pathways in Bromeliaceae: phylogenetic and
ecological significance of CAM and C3 based on carbon
isotope ratios for 1893 species. Botanical Journal of the
Linnean Society 178: 169221.
Divakar PK, Leavitt SD, Molina MC, Del-Prado R,
Lumbsch HT, Crespo A. 2016. A DNA barcoding
approach for identification of hidden diversity in Parmeliaceae (Ascomycota): Parmelia sensu stricto as a case study.
Botanical Journal of the Linnean Society 180: 2129.
Fedosov VE, Fedorova AV, Fedosov AE, Ignatov MS.
2016. Phylogenetic inference and peristome evolution in
haplolepideous mosses, focusing on Pseudoditrichaceae and
Ditrichaceae s.l. Botanical Journal of the Linnean Society
181: 139155.
Ghislain B, Nicolini E-A, Romain R, Ruelle J, Yoshinaga A, Alford MH, Clair B. 2016. Multilayered structure of tension wood cell walls in Salicaceae sensu lato and
its taxonomic significance. Botanical Journal of the Linnean
Society doi: 10.1111/boj.12471.

721

Global Carex Group. 2015. Making Carex monophyletic

(Cyperaceae, tribe Cariceae): a new broader circumscription. Botanical Journal of the Linnean Society 179: 142.
Ickert-Bond SM, Gerrath JM, Posluszny U, Wen J.
2015. Inflorescence development in the Vitis-Ampelocissus
clade of Vitaceae: the unusual lamellate inflorescence of
Pterisanthes. Botanical Journal of the Linnean Society 179:
725741.
Iles WJD, Smith SY, Gandolfo MA, Graham SW. 2015.
Monocot fossils suitable for molecular dating analyses.
Botanical Journal of the Linnean Society 178: 346374.
Lehtonen S, Christenhusz MJM, Falck D. 2016. Sensitive
phylogenetics of Clematis and its position in Ranunculaceae. Botanical Journal of the Linnean Society doi: 10.11
11/boj.12477.
Linnaeus C. 1753. Species plantarum. Stockholm: L. Salvius.
L
ofstrand SD, von Balthazar M, Sch
onenberger J.
2015. Early floral development and androecium organization in the sarracenioid clade (Actinidiaceae, Roridulaceae
and Sarraceniaceae) of Ericales. Botanical Journal of the
Linnean Society 180: 295318.
Maggs C, Saunders G. 2016. A new monotypic family for
the enigmatic crustose red alga Plagiospora gracilis. Botanical Journal of the Linnean Society 182: 113.
Oriani A, Scatena VL. 2014. Ovule, fruit and seed development in Abolboda (Xyridaceae, Poales): implications for taxonomy and phylogeny. Botanical Journal of the Linnean
Society 175: 144154.
Oskolski A, von Balthazar M, Staedler YM, Shipunov
AB. 2015. Inflorescence and floral morphology of Haptanthus hazlettii (Buxaceae, Buxales). Botanical Journal of the
Linnean Society 179: 190200.
Palma-Silva C, Leal BSS, Chaves CJN, Fay MF. 2016.
Advances in and perspectives on evolution in Bromeliaceae.
Botanical Journal of the Linnean Society 181: 305322.
Platonova AG, Remizowa MV, Briggs BG, von Mering
S, Lock IE, Sokoloff DD. 2016. Vegetative morphology
and anatomy of Maundia (Maundiaceae: Alismatales) and
patterns of peripheral bundle orientation in angiosperm
leaves with three-dimensional venation. Botanical Journal
of the Linnean Society doi: 10.1111/boj.12478.
Rumsey FJ, Robba L, Schneider H, Carine MA. 2014.
Taxonomic uncertainty and a continental conundrum: Polypodium macaronesicum reassessed. Botanical Journal of
the Linnean Society 174: 449460.
Schneider JV, Paule J, Gita
J, Dressler S, Gusm~
ao
CLS, Benko-Iseppon AM. 2015. Divergent genome sizes
reflect the infrafamilial subdivision of the Neotropical
woody Marcgraviaceae. Botanical Journal of the Linnean
Society 177: 114.
Smith MR. 2016. Cord-forming Palaeozoic fungi in terrestrial assemblages. Botanical Journal of the Linnean Society
180: 452460.
Smith SY, Gandolfo MA. 2015. Insights and benefits from
monocot palaeobiology: DNA, fossils and phylogenetic analyses. Botanical Journal of the Linnean Society 178: 343345.
Sokoloff DD, Remizowa MV, Conran JG, Macfarlane
TD, Ramsay MM, Rudall PJ. 2014. Embryo and seedling

2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 182, 719722

722

M. F. FAY

morphology in Trithuria lanterna (Hydatellaceae, Nymphaeales): new data for infrafamilial systematics and a
novel type of syncotyly. Botanical Journal of the Linnean
Society 174: 551573.
Sokoloff DD, von Mering S, Remizowa MV. 2015. Female
flower and fruit anatomy of Tetroncium magellanicum:
implications for gynoecium evolution in the early divergent
monocot order Alismatales. Botanical Journal of the Linnean Society 179: 712724.
Souza G, Crosa O, Speranza P, Guerra M. 2016. Phylogenetic relations in tribe Leucocoryneae (Amaryllidaceae,
Allioideae) and the validation of Zoellnerallium based on
DNA sequences and cytomolecular data. Botanical Journal
of the Linnean Society 182: 811824.
Struwe L, Soza VL, Manickam S, Olmstead RG. 2014.
Gelsemiaceae (Gentianales) expanded to include the enigmatic Asian genus Pteleocarpa. Botanical Journal of the
Linnean Society 175: 482496.
Surveswaran S, Sun M, Grimm GW, Liede-Schumann S.
2014. On the systematic position of some Asian enigmatic
genera of Asclepiadoideae (Apocynaceae). Botanical Journal
of the Linnean Society 174: 601619.
Vigalondo B, Lara F, Draper I, Valcarcel V, Garilleti R,
Mazimpaka V. 2016. Is it really you, Orthotrichum acumina-

tum? Ascertaining a new case of intercontinental disjunction in

mosses. Botanical Journal of the Linnean Society 180: 3049.
Volkova OA, Remizowa MV, Sokoloff DD, Severova EE.
2016. A developmental study of pollen dyads and notes on
floral development in Scheuchzeria (Alismatales: Scheuchzeriaceae). Botanical Journal of the Linnean Society doi:
10.1111/boj.12482.
Wearn JA, Chase MW, Mabberley DJ, Couch C. 2013.
Utilizing a phylogenetic plant classification for systematic
arrangements in botanic gardens and herbaria. Botanical
Journal of the Linnean Society 172: 127141.
Widhelm TJ, Egan RS, Bertoletti FR, Asztalos MJ,
Leavitt SD, Lumbsch HT. 2016. Picking holes in traditional species delimitations: an integrative taxonomic
reassessment of the Parmotrema perforatum group
(Parmeliaceae, Ascomycota). Botanical Journal of the Linnean Society doi: 10.1111/boj.12483.
Zamberlan PM, Rodrigues IMC, M
ader G, Castro L,
Stehmann JR, Bonatto SL, Freitas LB. 2015. Re-evaluation of the generic status of Athenaea and Aureliana
(Withaniinae, Solanaceae) based on molecular phylogeny
and morphology of the calyx. Botanical Journal of the
Linnean Society 177: 322334.

2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 182, 719722