The ecology, evolution, and genetics of the

Hawaiian Silversword

Alliance

Kurt Hartman

Silversword researchers

Gerald Carr

Robert Robichaux

Bruce Baldwin

Donald W. Kyhos

Bruce Bohm

Bill Crins

Leslie Bohm

Silversword researchers

Adaptive Radiation on Hawaii

Bidens menziesii Geranium cuneatum Delissea undulata Campanulaceae

Adaptive Radiation on Hawaii

Drosophilidae

honeycreeper

What is the Silversword Alliance?

• 28 species endemic to Hawaii

• 3 genera– Argyroxiphium

(5 spp.)– Dubautia (21 spp.)– Wilkesia (2 spp.)

Genus #1 - Argyroxiphium = the “silverswords” & “greenswords”

• Most recognized genus of silversword alliance

• Capitulum with ray flowers (contrast with Wilkesia & Dubautia which only have disk flowers)

• Hybrid between Argyroxiphium, Wilkesia, and Dubautia species

• Found on Maui and Hawaii

Silversword species (3)

A. caliginis Bog silverswordA. kauense

A. sandwicense

2 subspecies of A. sandwicencessp. sandwicense

ssp. macrocephalum

Argyroxiphium

Argyroxiphium sandwicense habitat

• Habitat on cinder cone– 7000 to 10000 feet – intense sunlight– Hot in summer day & below freezing in winter

night – Snowfall, zero humidity, low ppt = alpine

desert

Silversword trichomes

(Melcher et. al 1994)

Unusual features• Pectic warts

• Secondary growth

Greenswords (2)

Argyroxiphium grayanum

Argyroxiphium virescens hybrid

Changes in soil characteristics below Argyroxiphium

• Soil below silversword increased in water and nutrient retention, lower temperature (18C), greater nutrient concentration for up to 7-9 yrs post mortum.

• Therefore good for current survival and future offspring who may be close in proximity to parent.

(Perez 2001)

Genus #2 - Wilkesia

W. gymnoxiphium – grows on pockets

in eastern Kaua’i (oldest high island) and may prefer certain soil types

– Dry, shrubby forest

•2 species: Wilkesia gymnoxiphium & Wilkesia hobdyi

Wilkesia gymnoxiphium

– Seldom branching stems (branch if injured), ≳ 10 ft

– Flat, fibrous leaves in whorls that are strictly parallel with few crosscutting veinlets

– Monocarpic

Wilkesia gymnoxiphium Wilkesia gymnoxiphium

Inflorescence with whorls of heads, all discoid flowers

Wilkesia hobdyi

Freely branching, decumbent to erect, endangered, grows only on Kaua’i, restricted to very dry ridges (75 - 100cm ppt / yr, elevation 275 - 400m)

Wilkesia hobdyi

Genus #3 - Dubautia

• Most “recent” genus• 21 species with differential spatial and

habitat distribution• Found on Kaua’i, O’ahu, Moloka’i, Lana’i,

Maui, Hawai’i• 2 other mainland islands have no Dubautia• 17 out of 21 species of Dubautia are single-

island endemics

D. ciliolata

D. plantaginea

D. scabra

D. latifolia

Movie Part IDubautia species

D. latifolia (vine) – “reticulate vein pattern with polygonal areoles containing numerous free-terminating veins”

D. microcephala (left)

D. linearis (right)

W. gymnoxiphium

(Carlquist 1959)

Veination patterns in Dubautia and Wilkesia

Dubatia herbstobatae

Dubatia arborea

Dubautia menziesii - kupaoa

Dubautia waialealae

Dubatia latifolia (vine)

D. laevigata

Dubautia laevigata

Dubautia pauciflorula

2 studies in conservation

Friar et. al 2000A. sandwicense in bad shape

Friar et. al 2001A. kauense in good shape

Habitat divergence

• Elevation from 75 to 3750m

• Habitats of dry shrublands, dry forests, subalpine shrublands, subalpine forests, alpine deserts, mesic forests, wet forests, bogs, young lava flows (Carr 1985)

Physiological and morphological divergences

1. Different tissue and elastic properties to maintain turgor at low water potentials (Robichaux 1985)

2. Different cell structures - especially Dubautia, a. Wet environments – Thin cuticle, thin leaves, loose

mesophyllb. Dry environments – Thick cuticle, thick leaves, compact

mesophyll, extracellular mesophyll, and white hairs (Carlquist 1958)

3. Veination –Dubautia latifolia – highly reticulate; Wilkesia – monocot-like veination with few crosscutting veinlets; Others – subparallel or longitudinally directed veins (Givnish & Sytsma 1997)

Who are the ancestors of

silversword alliance?

• Tarweeds found in California “floristic province” = CA and Mex.

• Shrubby, sprawling plants• Similar in floral

morphology and anatomy to silverswords

• Sticky substance on flowers and fruits

• Arrived in Hawaii on bird feathers (most likely) roughly 5 mya (Baldwin & Robichaux 1995)

What’s in a name? – “Tarweeds”

Tarweed

A. sandwicenseRaillardiopsis muirrii

The original silversword was a polyploid… what kind of

polyploid?

Hypothesis for polypolidy (n = 14)

Hypothesis for polypolidy (n = 14)

Best explanation

In what way did the silverswords move around Hawaii in terms of

biogeography and habitats?

Biogeography & phylogeny

• Minimum inter-island dispersal and large ecological divergence

• Generally westward to eastward movement

• Kaua’i, Oahu, Maui Nui – once contiguous islands facilitated this movement

How do we investigate these evolutionary relationships?

Laboratory methods of investigation

• Cytogenetic & hybridization analysis

• Nuclear DNA (nDNA)

• Chloroplast DNA (cpDNA)

• Mitochondrial DNA (mDNA)

• Ribosomal DNA (rDNA)

• Isozymic analysis

Q: How do silverswords evolve so fast?

• Problem: rates of morphological evolution are generally not correlated with rates of molecular evolution… how is this possible?

• ASAP3/TM6 – controls petal and stamen development

• ASAP 1 – controls floral primordia and sepal and petal identity

• Rapid regulatory gene mutations relative to the number of mutations of structural genes.(Baldwin & Sanderson 1998)

Q: How fast do silverswords evolve relative to continental groups?

• Kure 29 mya = oldest island• Actually Compositae is more recent (mid-oligocene ca.

25 mya)• Shift about 15 mya from wet summer to dry summer• Tarweeds begin to diverge• Used ITS (internal transcribed spacer) region of

nuclear DNA• Excluded annuals in analysis b/c higher rate of

evolution(Baldwin & Sanderson 1998)

• Found silverswords are “well nested” in tarweeds because left N. America after tarweeds diverged

• Today tarweeds ca. 114 species in 17 genera

• Estimated age of arrival in Hawaii to be 5.2 ± 0.8 mya which is age of Kaua’I (5.1 ± 0.2 mya; is the oldest high island)

• Other species are older on Hawaii– Drosophila > 10 mya– Lobelioids 15 mya– Honeycreepers 7-8 or 15-20 mya

• Older ancestor is possible from N. Am, but only one lineage survived at 5.2 mya

• Divergence rate is 0.56 ± 0.17 species / million yrs– Angiosperm families (0.12 species / million yrs)– Rodent families (0.22 to 0.35 species / million yrs)– African large mammals (0.0 to 0.39 species / million

yrs)

• However early Neocene horses show 0.5 to 1.4 species / million yrs) which indicates fast radiation then slow. Similar to above rate for silverswords.

• Likely that early radiation is very fast then slows

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Hybrids

• Today’s silverswords are polyploid

• Most silverswords are n=14 with few n=13 in Dubautia subgroup

• Was original ancestor a hybrid derived from allopolyploid or autopolyploid individual?

Movie Part IIHybrids

Hybridization

Trigeneric hybrid

Study Carraway et. al 2001

• D. ciliolata – 1855 lava flow• D. scabra – 1935 lava flow• Hybrids and introgression of only D.

ciliolata. • D. ciliolata genes in hybrid swarm able to

colonize 1935 lava flow.• I.e. occupy new habitat with hybridization

and genetic restructuring.

Why is silversword alliance a “textbook” example of adaptive radiation? (Raven et. al 1992)

• Includes ecology – long distance and local dispersal; morphology; physiology and adaptation

• Includes evolution – phylogeny; hybridization; rates of evolution

• Includes genetics – cpDNA; nrDNA; rDNA; isozyme; congruencies and incongruencies

• Conservation – population dynamics; extinction; positive and negative human influences

Summary

• Single colonist (allopolyploid) – 3 genera today

• Biogeographical movement west to east (mostly)

• Most are single-island endemics

• Radiate to different habitats on islands

• Morphological and physiological adaptation

• Systematics are well studied

• Needs protection from humans and grazing

The End