Phylogenetic studies in Apiaceae tribe Oenantheae: circumscription

and relationships

Stephen R. Downie

Krzysztof Spalik

Mark F. Watson

Deborah S. Katz-Downie

Outline of Presentation• To highlight the results of previous molecular systematic

investigations that led to the recent and modified circumscription of tribe Oenantheae

• To reveal the composition of the tribe and indicate provisional generic-level relationships based on preliminary phylogenetic analysis of rDNA ITS data

• To introduce several major genera (reduced morphology, taxonomic problems, biogeography) and discuss the implications of the phylogenetic results obtained to date

• To discuss our plans for the future

BiforaNeogoeziaSiumOenanthePerideridia90988397matK (Plunkett et al. 1996)528957100CryptotaeniaSiumBerulaCicutaOenanthePerideridiacpDNA restriction sites (Plunkett & Downie 1999)CryptotaeniaOxypolisSiumCicutaOenanthePerideridia786191rpoC1 intron(Downie et al. 1998)ITS (Downie et al. 1998, 2000)HelosciadiumBerulaSiumCryptotaeniaCicutaOenanthePerideridia<5094936010070

Molecular studies reveal a strongly supported Oenanthe clade

Region

ITS

ITS

cpDNA sites

rpl16 intron

matK

rpoC1 intron

rps16 intron

rbcL

Bootstrap (%)

100

100

100

100

97

91

86

65

Genera in Clade

Berula, Cicuta, Cryptotaenia, Oenanthe, Oxypolis, Perideridia, Sium

Berula, Cicuta, Cryptotaenia, Helosciadium, Oenanthe, Sium

Berula, Cicuta, Cryptotaenia, Oenanthe, Perideridia, Sium

Cicuta, Cryptotaenia, Oenanthe, Oxypolis Perideridia, Sium

Bifora, Neogoezia, Oenanthe, Perideridia, Sium

Cicuta, Cryptotaenia, Oenanthe, Oxypolis, Perideridia, Sium

Berula, Cicuta, Cryptotaenia, Helosciadium, Oenanthe, Sium

Cicuta, Cryptotaenia, Oenanthe, Sium

Oenanthe Clade: Composition and Support

Lilaeopsis, a simple apioid umbellifer

MP analysis of rbcL, matK, & rpoC1 intron data(Petersen et al. 2002)

Lilaeopsis brasiliensis (Affolter 1985)

Lilaeopsis mauritiana

L. mauritiana

Entire, simple, linear to spatulate, septate leavesHorizontal creeping stems

Simple, few-flowered umbels

Damp, marshy or truly aquatic habitatsThick, corky ribs; no carpophore

798694CryptotaeniaSiumNeogoeziaLilaeopsisOenanthePerideridia

The Oenanthe Clade recognized as Tribe Oenantheae Dumort.

(emend. M. F. Watson & S. R. Downie; Downie et al. 2000, 2001)

• Berula• Cicuta• Cryptotaenia• Cynosciadium• Helosciadium• Lilaeopsis• Limnosciadium

• Neogoezia• Oenanthe• Oxypolis• Perideridia• Ptilimnium• Sium

Oenantheae Dumort. (1827)• Aethusa• Coriandrum• Oenanthe

Seseleae subtribe Oenanthinae Bentham (1867)• Aethusa• Astydamia• Capnophyllum• Choritaenia• Cymbocarpum• Eurytaenia• Polemannia• Siler• Cynosciadium• Discopleura (=Ptilimnium)• Crantzia (=Lilaeopsis)• Oenanthe

Oenantheae Dumort. emend. Koso-Poljansky (1916)• Apodicarpum• Cicuta• Cymbocarpum• Cynosciadium• Cyssopetalum (=Oenanthe)• Ducrosia• Hohenackeria• Johrenia• Krubera• Oenanthe• Ptilimnium• Platylophium (=Ferulago)• Rhabdosciadium• Rhysopterus (=Cymopterus)• Stenocoelium• Thecocarpus• Trepocarpus

Red Highlight: Oenantheae emend. M.F. Watson & S.R. Downie

A comparison of three systems of classification

Fruits radiately ribbed

Ribs raised, broadly thickened at margin, corkyFruits subterete to dorsally compressedVallecular vittae solitary

Fruit anatomy(relative placement of aerenchyma)

Distribution of Oenantheae Genera in the Nomenclator of Pimenov & Leonov (1993)

(classification modified from Drude 1898)

Echinophoreae

Scandiceae

Caucalideae

Coriandreae

Smyrnieae (1)

Hohenackerieae

Pyramidoptereae

Apieae (11)

Angeliceae

Peucedaneae (1)

Tordylieae

Laserpitieae

Oenantheae Genera, Species & Distribution

Genus No. Species Distribution

Berula 2 Widespread

Cicuta 4 3 NA; 1 circumboreal

Cryptotaenia 6 Widespread

Cynosciadium 1 USA

Helosciadium 5 Eurasia

Lilaeopsis 13 New World, Australasia

Limnosciadium 2 USA

Neogoezia 5 Mexico

Oenanthe 40 Widespread

Oxypolis 7 NA

Perideridia 14 13 NA; 1 Asian

Ptilimnium 5 USA

Sium 14 Widespread

Tribe Oenantheae

Attributes of tribe Oenantheae

Lilaeopsis (Affolter 1985)

Perideridia gairdneri(Oregon State University)

Cicuta (TAMU)

Limnosciadium (TAMU)

Globose to broadly ovate fruits

Cicuta virosa

Preference for wet or aquatic habitats

Fascicled fibrous or tuberous roots

Entire, simple, septate leaves

Corky-thickened ribs(spongy cells; storage tracheids)

Lilaeopsis brasiliensis

Glabrous stems & leaves

Oxypolis greenmanii

Oxypolis filiformis

Lilaeopsis occidentalisLilaeopsis carolinensis

Linear, septate leaves are homologous to the rachis of a normal compound leaf, with the position of septae corresponding to the position of pinnae insertion (rachis-leaves; phyllodes) The size & shape of these leaves are readily modified by the environment (Affolter 1985)

In Apiaceae, linear, septate leaves occur in: Cynosciadium, Eryngium, Lilaeopsis, Limnosciadium, Oenanthe, Ottoa, Oxypolis, Perissocoeleum & Ptilimnium

Hollow leaves with transverse septae

Materials and Methods> 260 Accessions Examined, including comprehensive representation of all 13 genera unambiguously included within tribe Oenantheae

> 60 Additional Accessions, representing taxa provisionally included within the tribe (i.e., Bifora) or those having one to several similar ecological or morphological traits (moist/wet habitat; fruits having spongy tissue; fascicled or tuberous-like roots; linear, septate or finely dissected leaves; simple umbels)

As putative outgroups, we included representation of the tribe Pleurospermeae (i.e., Aulacospermum, Physospermum, & Pleurospermum), the Komarovia clade (i.e., Hansenia, Komarovia, & Parasilaus), and Erigenia

18S nrDNA26S nrDNAITS 5ITS 3ITS 4ITS 2ITS 2ITS 15.8S215 bp224 bpITS region

Phylogenetic Analysis:• Maximum Parsimony (PAUP*)

Provisional Generic-Level Relationships in Oenantheae(strict consensus tree based on MP analysis of ITS data)

No. Species(examined / total)No. AccessionsExamined721983514CynosciadiumLimnosciadiumPtilimniumLilaeopsisBifora americanaTrepocarpusNeogeoziaAfrocarumHelosciadiumCryptotaeniaOenantheOxypolisPerideridiaBerulaSiumCicuta25823314241/11/23/55/131/11/15/51/12/214/144/43/715/409/145/55/613724= Genus is not monophyletic

Perideridia is sister to all other examined OenantheaeA possible NA origin of the tribe?

CynosciadiumLimnosciadiumPtilimniumLilaeopsisBifora americanaTrepocarpusNeogeoziaAfrocarumHelosciadiumCryptotaeniaOenantheOxypolisPerideridiaBerulaSiumCicutaUSAUSAUSANew World, AustralasiaUSAUSAMexicoAfricaEurasiaOld WorldOld WorldNANAOld WorldOld WorldNA, Circumboreal

Afrocarum imbricatum (Africa)Sium repandum (Africa)Berula thunbergii (Africa)Sium bracteatum (St.Helena)Berula erecta (Africa)Berula erecta (Europe & NA)Sium sisarumSium latifoliumSium suaveSium frigidumSium ninsiSium tenue

Berula erecta

Afrocarum imbricatumSium repandum

Townsend, 1989, Flora of Tropical East Africa

Berula, Sium & Afrocarum are similar morphologically

Cryptotaenia canadensisMissouri Flora Website

Cryptotaenia, 4-7 species

Oenantheae•N. America•Europe•Asia

Scandiceae subtribe Daucinae •Canary Islands

Pimpinella clade•Africa

“African species of Cryptotaenia are extremely close to Pimpinella” (Townsend 1989)

AfrocarumHelosciadiumCryptotaenia canadensisOenantheBerulaSiumCryptotaenia elegansMoniziaDaucusCryptotaenia africanaCryptotaenia calycinaPimpinellaCryptotaenia japonica

Oenanthe: 40 species; Helosciadium: 5 species

Oenanthe nodiflora in Apium clade

= Sclerosciadium nodiflorum

Helosciadium nodiflorumOenanthe aquatica ??Helosciadium repensHelosciadium bermejoiHelosciadium inundatumHelosciadium crassipesCryptotaeniaOenanthe (13 spp.)Oenanthe nodifloraAmmi majus

Oenanthe aquaticaC.A.M. Lindman FloraHelosciadium nodiflorum

Helosciadium was included in Apium s. lat. It comprises wetland species, with aerenchymatic tissue in its mericarps (the latter is not present in Apium s. str.)

Cynosciadium, Limnosciadium & Ptilimnium

Glabrous annuals, with compound umbelsFascicled, fibrous rootsInhabits wet places in south-central and SE USAOvoid fruits with corky thickened lateral ribsLeaves entire to compound with elongate, narrow or filiform divisions. Some species linear septateCynosciadium (BONAP)

Limnosciadium (BONAP) Ptilimnium costatumPtilimnium

Cynosciadiumdigitatum

Limnosciadiumpinnatum

CynosciadiumLimnosciadiumPtilimniumLilaeopsis

Bifora + Neogoezia(Plunkett et al. 1996)

Digital Flora of Texas (TAMU)

Bifora americana (BONAP) Trepocarpus aethusae (BONAP)

Bifora americana

Bifora americana & Trepocarpus:South-eastern USAGlabrous annuals; wetland habitatsCorky fruits in Trepocarpus (that float!)Lvs pinnately decompound

Bifora americana

Trepocarpus aethusae

Bifora americanaTrepocarpus aethusaeNeogoezia gracilipesNeogoezia breedloveiNeogoezia minorNeogoezia planipetalaNeogoezia macvaughii

Neogoezia: 5 species endemic to MexicoConstance 1987

NYBG Type Catalog

Neogeozia macvaughii

N. macvaughii

N. gracilipes

N. macvaughii

Simple, many-flowered umbels

Fascicled fleshy-tuberous roots

Acaulescent, scapose habit

Ovoid, globose fruits

Usually moist habitats

Perideridia: delicious tuberous roots P. gairdneri

P. kelloggii (Lee Dittmann)

• 14 species of glabrous perennials• Late summer to fall flowering• Unique polystelic vascular structure

(the fusion product of several

individual roots)• Moist or xerophytic habitats• Broad corky or filiform fruit ribsP. kelloggii

P. howellii

P. oregana

Perideridia is Indigenous to USA

Number of species per state:1-3 4-5 6-7 8-9 10-11

BONAP

P. neurophylla

• Strict consensus of MP trees

• Perideridia neurophylla allies with Pternopetalum & Spuriopimpinella (therefore maintain as Pterygopleurum neurophyllum)

P. bacigalupiiP. erythrorhizaP. bolanderiP. parishiiP. lemmoniiP. californicaP. pringleiP. kelloggiiP. gairdneriP. oreganaP. leptocarpaP. americanaP. howellii

A possible addition to tribe Oenantheae?(based on partial ITS sequence data)

Lichtensteinia• 6 spp. South Africa • 1 sp. St. Helena)

Burtt, 1991, Edinb. J. Bot. 48(2): 225

Lichtensteinia obscura

Additional genera examined (or will be examined) for possible placement in tribe Oenantheae

ApiumApodicarpumAsciadiumChamaeleCrenosciadiumLichtensteiniaNiphogeton

OreoschimperellaOttoaPterygopleurumPternopetalumRutheopsisSpuriopimpinellaStoibrax

Material of any of these genera would be appreciated, as well as suggestions of other taxa to survey!

Summary• Tribe Oenantheae Dumort. is a strongly supported monophyletic

group in all molecular analysis to date

• While these plants may share several morphological attributes (such as those acquired through existence in a wet environment), no unique morphological synapomorphy supports their monophyly. Some species with simplified vegetative morphology confound cladistic analysis

• Afrocarum, Trepocarpus and, possibly, Lichtensteinia, are recent additions to the tribe. The placement of Bifora americana within the tribe is confirmed

• Old World genera Berula, Cryptotaenia, Oenanthe, and Sium, as currently circumscribed, are each not monophyletic

Summary cont’d.

• The USA endemic genus Perideridia is sister taxon to all other examined Oenantheae (suggestive of a NA origin of the tribe?)

• Phytogeographical discussions based on distribution patterns of certain Oenantheae (i.e., Cryptotaenia, Perideridia & Sium) should be treated with caution prior to phylogenetic study

• Phylogenetic analysis of rDNA ITS sequences often results in fully resolved phylogenies with well-supported clades

Major Goals of Ongoing Research

• To produce a comprehensive estimate of phylogenetic relationships within tribe Oenantheae using molecular and morphological data

• To use the resultant phylogeny to elucidate patterns in the evolution of specific phenotypic characters and to explain many interesting disjunct geographic distributions

• To revise generic circumscriptions and to produce a modern classification for the group that reflects its evolutionary history. Collaborations are welcome!

Acknowledgements• Feng-Jie Sun• Mary Ann Feist• Changshook Lee• Carolina Calviño• Gina Colletti• NSF Grants 9407712

& 0089452• Jean-Pierre Reduron

(for material)

Krzysztof Spalik Deborah Katz-Downie

Mark F. WatsonCo-conspirators in tribe Oenantheae