Evolution and Ecology of the Parasitic Order Santalales

Chlamydophytum aphyllum (Balanophoraceae)

Ecology and Evolution of

Outline

1.Placement of Santalales

Modes of parasitism

2.Phylogenetics of SantalalesEvolution of parasitic modes

Ecology

3.SummaryParasitic angiosperms

Where is Santalales?

Laurales

Piperales

Saxifragales

Zygophyllales

Malpighiales

Cucurbitales

Malvales

Santalales

Ericales

Boraginales

Laminales

Solanales

?

HoloparasitescpDNA?

Degree

Hemiparasitehost

Root R

Connection

StemS

Altered from Nickrent 2008

Altered from Nickrent 2008

Mode

Non-parasitic

Root parasitic

Stem parasitic

N

R

S

Types of haustorial connections

Striga

hermonthica

on corn root

Thismia (Burmanniaceae)

vs. mycoheterotrophic

Haustorial parasitism

Dörr 1997.

Haustorial connection: “wood roses”

Santalales

non-parasitic

hemiparasitic

holoparasitic

Degree

Thesium clade

Comandra clade

Santalum clade

Root hairs absent(unclear if present in

Erythropalaceae)

Mycorrhizae

generally absent(Erythropalaceae and a few

species in “Olacaceae”)

+/- 9 families151 genera

1985 species

Balanophoraceae

R

“Viscaceae”

Greek: balanos - acorn

holoparasitic

Thesium clade

Comandra clade

Santalum clade

Cynomorium

?

“Balanophorales”: Balanophoraceae + Cynomoriaceae?

Balanophoraceae

+ Santalales BS = 94

Cynomorium in

Saxifragales BS = 98

Nickrent et. al. 2005rDNA + cpDNA + mtDNA

“Balanophorales”: Balanophoraceae + Cynomoriaceae?

Su et. al. 2008

B-class floral genes Balanophoraceae basal within

Santalales(unpublished)

Balanophoraceae: Balanophora laxiflora, Vietnam

synandrium, extrafloral nectary

Hong Kong

volva

Balanophoraceae: Helosis cayennensis, Brazil

peltate scales

synandrium

“silky” styles

Balanophoraceae: Chlamydophytum aphyllum, Congo

“little or hardly stinking” Halle 1978

Balanophoraceae: Chlamydophytum aphyllum, Congo

Volva: saclike membranous envelope

anther

stigma

stylar

channeland

ovule in

longitudinal

section

anthers

capitulum

Halle 1978

Balanophoraceae: Chlamydophytum aphyllum, Congo

“old desiccated and parasitized male spike”

Cochineal scale

Dipteran larvae

Mite

Mite

Halle 1978

Balanophoraceae: Langsdorffia hypogaea

Infructescence

Propithecus diadema, Madagascar

Irwin et. al., 2006. Diademed sifakas (Propithecus diadema) use

olfaction to forage for the inflorescences of subterranean

parasitic plants (Balanophoraceae: Langsdorffia sp., and Cytinaceae:

Cytinus sp.)

Balanophoraceae: Langsdorffia

Lophophytum leandrii, Brazil

Greek lophos - crest or tuft

Monoecious Balanophores:

Balanophora fungosa ssp. fungosa, Philippines

?

Balanophoraceae: Lophophytum mirabile, Brazil; Latin mirabilis - marvelous

Borchsenius 1990Host: Pithecellobium

pollen-robbing bee:

Subfamily Meliponidae

Beetle pollinated (generalist)

Borchsenius 1990

Balanophoraceae: Lophophytum mirabile, Brazil; Latin mirabilis - marvelous

Balanophoraceae: Dactylanthus taylorii, New Zealand

Host: Schefflera digitata

Māori : pua reinga - "flower of the underworld“

waewae atua - "feet of gods”

“threatened species” as of 2004

1. Harvesting for sale

- New Zealand Department of Conservation, 2009

Balanophoraceae: Dactylanthus taylorii

Lesser Short-tailed Bat Mystacina tuberculata

(1 of 2 native NZ mammals)

Peter Schouten

2. Pollinator declineEcroyd 1996

3. Invasive species

Norway rat Rattus norvegicus

Australian brush-tailed

possum Trichosurus vulpecula

plants in cages, New Zealand Department of

Conservation

Balanophoraceae: Dactylanthus taylorii

Ecroyd 1996

Balanophoraceae: Corynaea crassa, Costa Rica

Balanophora reflexa, Borneo Balanophora wrightii, Japan

More Balanophoraceae

Rhopalocnemis phalloides, Vietnam

ErythropalaceaeN

Santalum clade

Scorodocarpus

borneensis, Indonesia

Erythropalum scandens, Borneo

Erythropalaceae: Heisteria

Heiseria latifolia, Ecuador

N

Heisteria scandens, Costa Rica

calyx cupular

Heisteria macrophylla Heisteria sp.

calyx

+

hypanthium

Thesium clade

Comandra clade

Santalum clade

R

R

R

Anacalosoideae

“Olacaceae”

“Olacaceae”

Olax phyllanthii, Australia

Olax scandens, Thailand

daSilva et al., 2009. MK801- and

scopolamine-induced amnesias are

reversed by an Amazonian herbal locally

used as a “brain tonic”

Ptychopetalum

olacoides

Ximenia americana var.

americana, Bahamas

Minquartia guianensis, French Guiana

R

Thesium clade

Comandra clade

Santalum clade

S R

Loranthaceae 950 species

Loranthaceae: Nuytsia floribunda “Western Australian Christmas tree"R

Root parasite

S Loranthaceae

Loranthaceae: bird pollinationS

Loranthaceae :Tristerix aphyllus on Echinopsis chilensis, ChileS

S

Monito del Monte

"little mountain

monkey”Dromiciops gliroides

Loranthaceae: Tristerix corymbosus, Argentina

S Loranthaceae :Tristerix verticillatus, Chile

vivipary

Ormiscodes, Saturniidae

S Loranthaceae :Tristerix verticillatus, Chile

Mathania

Lysiana exocarpi – “harlequin mistletoe” on Pittosporum angustifolium, Melaleuca sp.

Loranthaceae: Lysiana Ehleringer et. al., 1986. Mistletoes: a hypothesis

concerning morphological and chemical avoidance of

herbivory.

S

mistletoe bird

Dicaeum hirundinaceum

Loranthaceae, Amyema pendula, AustraliaS

Loranthaceae, Plicosepalus

Host: Acacia raddiana

S

Loranthaceae: Amyema

Comocrus behri – the

mistletoe moth

Delias harpalyce – imperial white

Amyema artensis

Amyema fasciculata

S

Loranthaceae: Lysiana murrayiS

Ogyris amaryllis

(Lycaenidae)

mistletoe butterfly

Tolypanthus lagenifer, India

Tolypanthus pustulatus, Thailand

More Loranthaceae

SchoepfiaceaeR

Schoepfia schreberi, Florida

Quinchamalium chilense, Argentina

Arjona patagonica, Chile

MisodendraceaeS

R

S

Thesium clade

Comandra clade

Santalum clade

Opiliaceae

Misodendraceae

R

S

R

S

“Santalaceae”

Thesium clade

Comandra clade

Santalum clade

Comandra umbellata - bastard toadflax , Virginia

Acanthosyris spinescens

R

R

Buckleya distichophylla on

Tsuga, North Carolina

Thesium euphorbioides

“Santalaceae”: Comandra, Thesium clades

Nanodea muscosa, Argentina

“Santalaceae”: Santalum clade

Exocarpus cupressiformis,Tasmania

Exocarpos casuarinoides, New Caledonia

RS S

“Santalaceae”: Santalum clade: Santalum - sandalwoodR

$1500/kg

Santalum album, Indian Sandalwood

Santalum spicatum, Australian sandalwood.

“Santalaceae”, Amphorogyne clade:

Choretrum pauciflorum

Dendrotrophe sp. Daenikera corallina, New Caledonia

S

Viscaceae

Arceuthobium vaginatum

Helixanthera wallichiana

S

Arceuthobium

minutissimumon Pinus wallichiana, Bhutan

endoparasiteworld’s smallest

dicot

Summary: Parasitic modes of Santalales

N

Thesium clade

Comandra clade

Santalum clade

R

R

R

R

R

R

R

R

R

“Viscaceae”

Mode

Non-parasitic

Root parasitic

Stem parasitic

N

R

S

R

S

S

S

S

S

≥5

Summary: How did parasitism evolve in this group?

N

Thesium clade

Comandra clade

Santalum clade

R

R

R

R

R

R

R

R

R

“Viscaceae”

Mode

Non-parasitic

Root parasitic

Stem parasitic

N

R

S

R

S

S

S

S

S

+

-

+Santalales +

Balanophorales?“unlikely that parasitism is a

reversible trait”Barkman 2007

12

Summary: 11-13 origins of haustorial parasites

+ Podocarpaceae?Parasitaxus usta

New Caledonia(appears mycoheterotrophic)

11: Saxifragales +

Santalales?

13: Santalales +

Balanophorales?Barkman 2007

Malvales: Cytinaceae: Cytinus

Future research: Horizontal gene transfer of atp1 from host to endoparasite

Barkman 2007

Ericales: Mitrastemonaceae: Mitrastema

SantalalesViscaceae: Arceuthobium

minutissimum + host

not sampled

Additional references: http://www.mobot.org/MOBOT/research/APWeb/

http://www.parasiticplants.siu.edu/