Adaptive Radiation of the Hawaiian Silversword Alliance: Class Slides

1. Phenomenon: the Hawaiian Silversword Alliance. This group of plants exhibits enormous phenotypic diversity among species (link) and is endemic to the Hawaiian Islands. There is considerable interspecific morphological variation in stems and branches (e.g. from herbaceous mats to trees link), flowers and fruits (link), leaves (link), and ecological and physiological adaptations (link), all in spite of relatively high genetic similarity among species (link). What are their origins?

2. Hypothesis: Because the Hawaiian Islands are comparatively young, it is hypothesized that the ancestors of the Silversword alliance dispersed there from an older landmass. The high degree of genetic similarity among species suggests that they all share a single recent common ancestor, and that the evolution and adaptive radiation of this group occurred on the Hawaiian Islands.

3. Theory: If one constructs a phylogeny for this family of plants, one can infer that the closest relatives to the Hawaiian silverswords share a common ancestor with the Hawaiian silverswords.

4. Predictions: A molecular phylogenetic reconstruction of the entire family from around the Pacific rim will reveal the closest relatives of the Hawaiian silverswords. Such a phylogeny should be reproducible when constructed independently from different data sets, such as from non-coding regions from different genes. Historical geology and biogeography, and molecular clocks should give similar estimates of evolutionary time and rates of diversification.

5. Tests: Baldwin's (1992) molecular phylogeny based on nuclear rDNA says that the Hawaiian silverswords most likely came from western North America, because their closest relatives are the North American tarweeds (link). The fact that their chromosome numbers are roughly double those of the tarweeds, and the the fact that they cluster closely with two particular tarweeds, Raillardiopsis muirii and Raillardiopsis scabrida, suggests that they arose from an allopolypoid ancestor that was a hybrid from these two species (Baldwin and Sanderson 1998). Another independent data set based on chloroplast DNA also suggests a similar ancestry (link). Yet another independent set of data supports these conclusions too. Barrier, Baldwin, Robichaux and Purugganan (1998) found that two floral homeotic genes, ASAP3/TM6 and ASAP1, are found in duplicate copies within members of the Hawaiian silversword alliance. Analysis of ASAP3/TM6 indicates that the interspecific hybridization event in the ancestry of the Hawaiian silversword alliance involved members of lineages that include Raillardiopsis muirii (and perhaps Madia nutans) and Raillardiopsis scabrida. The most likely ancestor for the Hawaiian silverswords was an allopolyploid hybrid between Raillardiopsis muirii and Raillardiopsis scabrida.

This leads to a new round of phenomena, hypotheses, etc.

1. Phenomenon: Ohno 1970 noted that much of the origins of evolutionary novelties in animals was preceded phylogenetically by genome duplication, mainly ancient polyploidization events. In the case of the Hawaiian Silversword Alliance, 3 separate lines of genetic evidence strongly suggest that this species group arose from the hybridization and allopolyploidization of two North American Tarweeds. Silverswords have roughly twice the chromosome number as the Tarweeds, and they have duplicate copies of floral homeotic genes.

2. Hypothesis: Genome duplication followed by evolution of floral homeotic genes led to the evolution of new bauplans in the Hawaiian Silverswords to yield phenotypes ranging from herbs to vines to trees.

3. Theory: Ohno's (1970) hypothesis is that gene duplication of regulatory genes, combined with subsequent selection for them to acquire new functions, led to the evolution of new bauplans. The classic model of gene duplication underestimates their frequency in nature; whereas the DDC model (Force et al. 1999, Lynch and Force 2000) does not. Lynch and Conery (2000) estimate that gene duplication rates per gene are within an order of magnitude of point mutation rates per nucleotide. Lynch and Force (2001) illustrate how the DDC model also leads logically to speciation through the quick evolution of genetic incompatibilities of isolated populations.

4. Predictions: 1. If this hypothesis were true, we would expect more rapid evolution in Silversword floral homeotic genes than in those same genes in the Tarweeds. 2. If the basic Ohno (1970) thesis is correct, then we would expect more rapid evolution in Silversword regulatory genes (i.e. homeotic genes) than in their structural genes.

5. Tests: Barrier et al. (2001) corroborated both predictions. 1. Table 1 (Barrier et al. 2001) shows that for two floral homeotic genes (i.e. ASAP3/TM6 and ASAP1), Silverswords have higher numbers of nonsynonymous substitutions relative to synonymous substitutions than do the Tarweeds. 2. Also in Table 1, one structural gene (i.e. ASCAB9) also evolved faster in the Silverswords than the Tarweeds, but at a slower rate than the regulatory (i.e. homeotic) genes.

References:

Baldwin BG. 1992. Phylogenetic utility of the internal transcribed spacers of nuclear ribosomal DNA in plants: an example from the compositae. Mol Phylogenet Evol 1992 Mar;1(1):3-16 (link)

Bruce G. Baldwin, and Michael J. Sanderson 1998. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). Vol. 95, Issue 16, 9402-9406, August 4, 1998 (PubMed, PNAS)

Baldwin BG, Wessa BL. 2000. Origin and relationships of the tarweed-silversword lineage (Compositae-Madiinae). Am J Bot 2000 Dec;87(12):1890-1908. (link, pdf)

Barrier M, Baldwin BG, Robichaux RH, Purugganan MD. 1999. Interspecific hybrid ancestry of a plant adaptive radiation: allopolyploidy of the Hawaiian silversword alliance (Asteraceae) inferred from floral homeotic gene duplications. Mol Biol Evol 1999 Aug;16(8):1105-13 (PubMed, pdf)

Marianne Barrier, Robert H. Robichaux, and Michael D. Purugganan, 2001. Accelerated regulatory gene evolution in an adaptive radiation. Proc. Natl. Acad. Sci. USA, Vol. 98, Issue 18, 10208-10213, August 28, 2001 (PNAS)

Allan Force, Michael Lynch, F. Bryan Pickett, Angel Amores, Yi-lin Yan, and John Postlethwait 1999. Preservation of Duplicate Genes by Complementary, Degenerative Mutations. Genetics, Vol. 151, 1531-1545, April 1999, Copyright © 1999 (link)

Lynch, M., Conery, J. S. (2000). The Evolutionary Fate and Consequences of Duplicate Genes. Science 290: 1151-1155 (PubMed, Science, requires subscription)

Lawton-Rauh A, Robichaux RH, Purugganan MD. Patterns of nucleotide variation in homoeologous regulatory genes in the allotetraploid Hawaiian silversword alliance (Asteraceae). Mol Ecol. 2003 May;12(5):1301-13. (pdf)

Michael Lynch and Allan G. Force 2001. The Origin of Interspecific Genomic Incompatibility via Gene Duplication. Am. Nat. 2000. Vol. 156, pp. 590-605 (link, requires subscription)

Ohno, S. (1970) Evolution by Gene Duplication (Springer, New York).

Vargas P, Baldwin BG, Constance L. 1998. Nuclear ribosomal DNA evidence for a western North American origin of Hawaiian and South American species of Sanicula (Apiaceae). Proc Natl Acad Sci U S A 1998 Jan 6;95(1):235-40 (PubMed, PNAS)

David L. Remington and Michael D. Purugganan. GAI Homologues in the Hawaiian Silversword Alliance (Asteraceae-Madiinae): Molecular Evolution of Growth Regulators in a Rapidly Diversifying Plant Lineage. Mol Biol Evol 2002 19: 1563-1574. (link)

Baldwin and Sanderson estimate a minimum diversification rate of 0.56 +/- 0.17 species per million years, which they say, "This exceeds average rates of more ancient continental radiations and is comparable to peak rates in taxa with sufficiently rich fossil records that changes in diversification rate can be reconstructed.