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The ecology, evolution, and genetics of the Hawaiian Silversword Alliance: 

The ecology, evolution, and genetics of the Hawaiian Silversword Alliance Kurt Hartman

Silversword researchers: 

Silversword researchers Gerald Carr Robert Robichaux Bruce Baldwin

Silversword researchers: 

Donald W. Kyhos Bruce Bohm Bill Crins Leslie Bohm Silversword researchers

Adaptive Radiation on Hawaii: 

Adaptive Radiation on Hawaii Bidens menziesii Geranium cuneatum Delissea undulata Campanulaceae

Adaptive Radiation on Hawaii: 

Adaptive Radiation on Hawaii Drosophilidae honeycreeper

What is the Silversword Alliance?: 

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”: 

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): 

Silversword species (3) A. caliginis Bog silversword A. kauense A. sandwicense

2 subspecies of A. sandwicence: 

2 subspecies of A. sandwicence ssp. sandwicense ssp. macrocephalum

Argyroxiphium: 

Argyroxiphium

Argyroxiphium sandwicense habitat: 

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: 

Silversword trichomes

Slide13: 

(Melcher et. al 1994)

Unusual features: 

Unusual features Pectic warts Secondary growth

Greenswords (2): 

Greenswords (2) Argyroxiphium grayanum Argyroxiphium virescens hybrid

Changes in soil characteristics below Argyroxiphium: 

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 : 

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: 

Wilkesia gymnoxiphium

Slide19: 

Wilkesia gymnoxiphium Wilkesia gymnoxiphium Inflorescence with whorls of heads, all discoid flowers

Wilkesia hobdyi: 

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: 

Wilkesia hobdyi

Genus #3 - Dubautia: 

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

Slide23: 

D. ciliolata D. plantaginea D. scabra D. latifolia

Movie Part I Dubautia species: 

Movie Part I Dubautia species

Slide25: 

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 herbstobatae

Dubatia arborea: 

Dubatia arborea

Dubautia menziesii - kupaoa : 

Dubautia menziesii - kupaoa

Dubautia waialealae: 

Dubautia waialealae

Dubatia latifolia (vine): 

Dubatia latifolia (vine)

D. laevigata : 

D. laevigata Dubautia laevigata

Dubautia pauciflorula: 

Dubautia pauciflorula

2 studies in conservation Friar et. al 2000 A. sandwicense in bad shape Friar et. al 2001 A. kauense in good shape : 

2 studies in conservation Friar et. al 2000 A. sandwicense in bad shape Friar et. al 2001 A. kauense in good shape

Habitat divergence: 

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: 

Physiological and morphological divergences Different tissue and elastic properties to maintain turgor at low water potentials (Robichaux 1985) Different cell structures - especially Dubautia, Wet environments – Thin cuticle, thin leaves, loose mesophyll Dry environments – Thick cuticle, thick leaves, compact mesophyll, extracellular mesophyll, and white hairs (Carlquist 1958) 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?: 

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”: 

What’s in a name? – “Tarweeds” Tarweed A. sandwicense Raillardiopsis muirrii

The original silversword was a polyploid… what kind of polyploid?: 

The original silversword was a polyploid… what kind of polyploid?

Hypothesis for polypolidy (n = 14): 

Hypothesis for polypolidy (n = 14)

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?: 

In what way did the silverswords move around Hawaii in terms of biogeography and habitats?

Biogeography & phylogeny: 

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?: 

How do we investigate these evolutionary relationships?

Laboratory methods of investigation: 

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?: 

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?: 

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)

Slide55: 

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)

Slide56: 

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

Slide57: 

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

Hybrids: 

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 II Hybrids: 

Movie Part II Hybrids

Hybridization: 

Hybridization

Trigeneric hybrid: 

Trigeneric hybrid

Study Carraway et. al 2001: 

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): 

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: 

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: 

The End