EVOLUTION OF THE HAWAIIAN VIOLETS ( VIOLA )

EVOLUTIONEVOLUTIONOF THE HAWAIIAN VIOLETS (OF THE HAWAIIAN VIOLETS (VIOLAVIOLA))

HARVEY E. BALLARD, JR.HARVEY E. BALLARD, JR.Department of Environmental and Plant Department of Environmental and Plant

Biology, andBiology, andMolecular and Cellular Biology Program, Ohio Molecular and Cellular Biology Program, Ohio

UniversityUniversity

EVOLUTION OF THE HAWAIIAN EVOLUTION OF THE HAWAIIAN VIOLASVIOLAS

Evolutionary relationships of Evolutionary relationships of

Hawaiian violetsHawaiian violets

Relationships among Relationships among

Hawaiians, Diversification Hawaiians, Diversification

and Inter-Island Dispersaland Inter-Island Dispersal

Adaptive RadiationAdaptive Radiation

Biogeographic Source and Biogeographic Source and

MechanismMechanism

GROWTH HABITS OF HAWAIIAN GROWTH HABITS OF HAWAIIAN VIOLASVIOLAS

treelet/tall shrubtreelet/tall shrub

((V. tracheliifoliaV. tracheliifolia))

creeping herb/subshrubcreeping herb/subshrub

((V. kauaensis, V. maviensisV. kauaensis, V. maviensis))

erect shruberect shrub

((V. chamissoniana,V. chamissoniana,

V. robusta, V. oahuensis, V. robusta, V. oahuensis, V. waialenalenaeV. waialenalenae))

QUESTIONS ABOUT HAWAIIAN QUESTIONS ABOUT HAWAIIAN VIOLASVIOLAS

What does DNA data reveal about What does DNA data reveal about the origin and relationships of the the origin and relationships of the Hawaiian violets that morphology Hawaiian violets that morphology cannot?cannot?

Does the evolutionary pattern of Does the evolutionary pattern of the Hawaiian violets conform to the Hawaiian violets conform to the “progression rule”?the “progression rule”?

QUESTIONS ABOUT HAWAIIAN QUESTIONS ABOUT HAWAIIAN VIOLASVIOLAS

What typical features of an What typical features of an “adaptive radiation” are “adaptive radiation” are demonstrated by Hawaiian demonstrated by Hawaiian violets?violets?

How did the ancestral seed get How did the ancestral seed get from the Arctic to Kauai?from the Arctic to Kauai?









MechanismMechanism

PHYLOGENETIC TREE PHYLOGENETIC TREE FROM DNA SEQUENCE FROM DNA SEQUENCE

DATA FOR DATA FOR GENUS GENUS VIOLA VIOLA WORLDWIDEWORLDWIDE

•Hawaiians not Hawaiians not basal w/Latin basal w/Latin AmericansAmericans

•Hawaiians form a Hawaiians form a “natural” group“natural” group

•Nearest relative is Nearest relative is Viola langsdorffiiViola langsdorffii

PREVIOUSLY PREVIOUSLY HYPOTHESIZED HYPOTHESIZED

RELATIVES OF THE RELATIVES OF THE HAWAIIAN HAWAIIAN VIOLASVIOLAS

Viola kauaensis

Viola tracheliifolia Viola waialenalenae Viola stipularis

Viola rubella

NEW DNA EVIDENCE--ARCTIC TUNDRA BOG VIOLET, NEW DNA EVIDENCE--ARCTIC TUNDRA BOG VIOLET, VIOLA VIOLA LANGSDORFFIILANGSDORFFII, IS NEAREST RELATIVE TO THE HAWAIIAN , IS NEAREST RELATIVE TO THE HAWAIIAN

VIOLASVIOLAS!!!!

•Northern Pacific Northern Pacific rather than Latin rather than Latin American origin American origin for Hawaiiansfor Hawaiians

•Herbaceous Herbaceous rather than woody rather than woody ancestryancestry

•Wetland originWetland origin









MechanismMechanism

PHYLOGENETIC TREE PHYLOGENETIC TREE FROM DNA SEQUENCE FROM DNA SEQUENCE DATA FOR HAWAIIAN DATA FOR HAWAIIAN

AND RELATED AND RELATED VIOLASVIOLAS

•Branch lengths Branch lengths shorter in Hawaiian shorter in Hawaiian violets than others violets than others in related groupsin related groups

•Short basal Short basal branches in branches in HawaiiansHawaiiansabrupt abrupt diversificationdiversification

PHYLOGENETIC TREE PHYLOGENETIC TREE SHOWING ISLAND SHOWING ISLAND

DISTRIBUTIONS AND DISTRIBUTIONS AND HABITATS OF HAWAIIAN HABITATS OF HAWAIIAN

VIOLASVIOLAS

•Basal species Basal species diversified on Kauaidiversified on Kauai

•Arctic bog violet Arctic bog violet yielded first dry-land, yielded first dry-land, then wet-land plantsthen wet-land plants

•Dispersal/diversifi-Dispersal/diversifi-cation west to eastcation west to east

INFERRED SEQUENCE OF SPECIATION AND DISPERSAL INFERRED SEQUENCE OF SPECIATION AND DISPERSAL EVENTS IN HAWAIIAN EVENTS IN HAWAIIAN VIOLAVIOLA









MechanismMechanism

CANONICAL VARIATES ANALYSIS OF HAWAIIAN CANONICAL VARIATES ANALYSIS OF HAWAIIAN VIOLAVIOLA TAXA USING LEAF CHARACTERSTAXA USING LEAF CHARACTERS

PRINCIPAL COMPONENTS ANALYSIS OF LEAF PRINCIPAL COMPONENTS ANALYSIS OF LEAF CHARACTERS SHOWING HABITAT ASSOCIATIONSCHARACTERS SHOWING HABITAT ASSOCIATIONS

PHYLOGENETIC TREE PHYLOGENETIC TREE HABITATS AND GROWTH HABITATS AND GROWTH

FORMS OF HAWAIIAN FORMS OF HAWAIIAN VIOLASVIOLAS

•Growth form not Growth form not linked to evolutionary linked to evolutionary relationshiprelationship

•Rather, growth form Rather, growth form commonly linked to commonly linked to habitathabitat

PHYLOGENETIC TREE PHYLOGENETIC TREE SHOWING LEAF TRAITS SHOWING LEAF TRAITS OF HAWAIIAN OF HAWAIIAN VIOLASVIOLAS

•Leaf morphology Leaf morphology not linked to not linked to evolutionary evolutionary relationshiprelationship

•Like growth form, it Like growth form, it is linked to habitatis linked to habitat

•Leaf anatomy Leaf anatomy similar (not shown)similar (not shown)









MechanismMechanism

SOURCE AREAS FOR WINTERING HAWAIIAN BIRDSSOURCE AREAS FOR WINTERING HAWAIIAN BIRDS

SUMMARYSUMMARY

Hawaiian Hawaiian ViolaViola is monophyletic (a “natural group”, is monophyletic (a “natural group”, recently derivedrecently derived

Biogeographic origin is Arctic/BorealBiogeographic origin is Arctic/Boreal

Woody growth and inflorescences are convergent Woody growth and inflorescences are convergent traits evolved under tropical oceanic conditionstraits evolved under tropical oceanic conditions

Initial colonization on Kaui <3.2 million years agoInitial colonization on Kaui <3.2 million years ago

Dispersal eastward, conforming to “chain rule”Dispersal eastward, conforming to “chain rule”

SUMMARYSUMMARY

Hawaiian Hawaiian ViolaViola is is monophyleticmonophyletic (“natural” group), (“natural” group), recently derivedrecently derived

Biogeographic origin is Arctic/BorealBiogeographic origin is Arctic/Boreal

Woody growth and inflorescences are convergent Woody growth and inflorescences are convergent traits evolved under tropical oceanic conditionstraits evolved under tropical oceanic conditions

Initial colonization onInitial colonization on KauiKaui ca. 3 million years agoca. 3 million years ago

Dispersal pattern conforms to “progression rule”Dispersal pattern conforms to “progression rule”

SUMMARYSUMMARY

Diversification proceeded along an environmental Diversification proceeded along an environmental gradient, from wet to dry (forest/cliff) and mesic gradient, from wet to dry (forest/cliff) and mesic habitatshabitats

Growth habit and leaf morphology (and anatomy) Growth habit and leaf morphology (and anatomy) tied closely to habitat, presumably due to strong tied closely to habitat, presumably due to strong environmental selection; led to distinctive environmental selection; led to distinctive “ecomorphic syndromes” in each “ecomorphic syndromes” in each habitathabitatadaptive radiation!adaptive radiation!

FUTURE RESEARCHFUTURE RESEARCH

Population genetic studies using highly variable Population genetic studies using highly variable molecular markersmolecular markers

Ecological characterization of microhabitats and Ecological characterization of microhabitats and habitat typeshabitat types

Investigation of potential hybridization in three Investigation of potential hybridization in three taxon pairs taxon pairs

Studies on taxonomic variation in Studies on taxonomic variation in V. maviensis, V. V. maviensis, V. kauaensis kauaensis andand V. chamissoniana-tracheliifolia V. chamissoniana-tracheliifolia

ANSWERS TO QUESTIONS ABOUT HAWAIIAN ANSWERS TO QUESTIONS ABOUT HAWAIIAN VIOLASVIOLAS

What does DNA data reveal about What does DNA data reveal about the origin and relationships of the the origin and relationships of the Hawaiian violets that morphology Hawaiian violets that morphology cannot?cannot?

Latin American violet groups are Latin American violet groups are notnot the nearest relatives; the the nearest relatives; the Hawaiians are most closely Hawaiians are most closely related to an Arctic tundra bog related to an Arctic tundra bog violet, violet, Viola langsdorffiiViola langsdorffii..


Does the evolutionary pattern of Does the evolutionary pattern of the Hawaiian violets conform to the Hawaiian violets conform to the “progression rule”?the “progression rule”?

Yes, all the most primitive violet Yes, all the most primitive violet groups grow on the oldest island, groups grow on the oldest island, Kauai (or can be interpreted to Kauai (or can be interpreted to arise there first). arise there first). Dispersal/diversification Dispersal/diversification proceeded to younger islands proceeded to younger islands further east.further east.


What typical features of “adaptive What typical features of “adaptive radiation” are demonstrated by radiation” are demonstrated by Hawaiian violets?Hawaiian violets?

•Morphology Morphology notnot reflective of reflective of evolutionary relationships—evolutionary relationships—convergence in same habitatsconvergence in same habitats

•Growth form & leaf morphology Growth form & leaf morphology linked to environment (“adaptive”)linked to environment (“adaptive”)

•Woody island species from an Woody island species from an herbaceous ancestorherbaceous ancestor


How did the ancestral seed get How did the ancestral seed get from the Arctic to Kauai?from the Arctic to Kauai?

Probably by birds, either in mud on Probably by birds, either in mud on their feet or in their digestive tract.their feet or in their digestive tract.

REFERENCESREFERENCES

Ballard, H. E., Jr., K. J. Sytsma, and R. R. Kowal. 1999. Shrinking the Ballard, H. E., Jr., K. J. Sytsma, and R. R. Kowal. 1999. Shrinking the violets: Phylogenetic relationships of infrageneric groups in violets: Phylogenetic relationships of infrageneric groups in ViolaViola (Violaceae) based on Internal Transcribed Spacer DNA Sequences. (Violaceae) based on Internal Transcribed Spacer DNA Sequences. Systematic Botany 23:439-458.Systematic Botany 23:439-458.

Ballard, H. E., Jr. and K. J. Sytsma. 2000. Evolution and biogeography Ballard, H. E., Jr. and K. J. Sytsma. 2000. Evolution and biogeography of the woody Hawaiian violets (of the woody Hawaiian violets (ViolaViola, Violaceae): Arctic origins, , Violaceae): Arctic origins, herbaceous ancestry and bird dispersal. Evolution 54:1521-1532.herbaceous ancestry and bird dispersal. Evolution 54:1521-1532.

Carlquist, S. 1992. Hawaii: A natural history. Lawai, Kauai: Pacific Carlquist, S. 1992. Hawaii: A natural history. Lawai, Kauai: Pacific Tropical Botanical Garden.Tropical Botanical Garden.

Givnish, T. J. 1998. Adaptive plant evolution on islands: Classical Givnish, T. J. 1998. Adaptive plant evolution on islands: Classical patterns, molecular data, new insights.patterns, molecular data, new insights.

Skottsberg, C. 1940. Observations on Hawaiian violets. Gothenburg. Skottsberg, C. 1940. Observations on Hawaiian violets. Gothenburg. Botaniska Tradgard. Medelanden 13:451-528.Botaniska Tradgard. Medelanden 13:451-528.

Documents

EVOLUTION OF THE HAWAIIAN VIOLETS ( VIOLA )