Botanic Gardens Trust, Sydney, Australia

Hakeinae

Molecular systematics of the subtribe Hakeinae (Proteaceae tribe Embothrieae)

Dr Peter H. Weston - Senior Principal Research Scientist

Peter Weston has been collaborating for several years with Austin Mast (Florida, U.S.A) on a project, funded by the US National Science Foundation, to reconstruct phylogenetic relationships between genera of Proteaceae subfamily Grevilleoideae and between species in selected genera. The largest genus in the Grevilleoideae, and third largest in the Australian flora, is Grevillea, with over 350 species. Together with Hakea (149 species) and the small genera Finschia (3 species), Buckinghamia (2 species) and Opisthiolepis (1 species), it makes up the subtribe Hakeinae of the tribe Embothrieae. This group is particularly interesting because of its high taxonomic and morphological diversity, its presence in most of Australia’s terrestrial environments from the arid centre to the alpine zone and its presence on other Gondwanic continental fragments such as Sulawesi, New Guinea and New Caledonia. Uneven patterns of diversification within the Hakeinae are also striking - the rainforest genera Opisthiolepis and Buckinghamia, which branch off, one after the other, at the base of the Hakeinae, are tiny compared to the massive, largely sclerophyllous radiation of the remaining three genera.

Mast, Weston and colleagues have already published a phylogenetic analysis of 55 species of Hakea (see last year’s publication list), including members of all of the infrageneric taxa informally recognized in the Flora of Australia. Mast and Weston have now extended their sampling to include a further 93 species of Grevillea, with the help of the Royal Botanic Gardens and Domain Trust Grevillea specialists Peter Olde (Honorary Research Associate) and Bob Makinson (Conservation Botanist). One representative of each of the other seven genera of tribe Embothrieae has also been sampled as outgroups. The phylogeny of the subtribe Hakeinae was reconstructed by analysing an alignment of DNA sequences for four chloroplast loci and one nuclear gene.

The tree produced from the full data set strongly supports the monophyly of many putative taxa, including the Hakeinae itself, Hakea, and the positions of Opisthiolepis and Buckinghamia as successive sister groups to the rest of the Hakeinae. However, Hakea and Finschia are deeply nested within Grevillea, rendering the latter paraphyletic and necessitating consideration of taxonomic change.

Weston and his colleagues had expected that at least some of the small number of Grevillea and Finschia species that are restricted to closed forest habitats would cluster at the base of the Grevillea-Hakea-Finschia clade but surprisingly, these were all found to be nested deeply within predominantly sclerophyllous clades. Perhaps the most surprising result was the phylogenetic position of G. endlicheriana, a rather non-descript shrub from dry sclerophyll forests of south-western Australia, which was strongly resolved as the sister of the rest of the Grevillea-Hakea-Finschia clade. These results suggest that the Hakeinae originated in rainforest habitats, and then diversified into fire-prone sclerophyllous communities but that several lineages secondarily recolonised rainforests. While some fire-adapted clades diversified spectacularly, others, most notably G. endlicheriana, did not, suggesting that sclerophylly, by itself, was not a key innovation.

A combination of traits was used to infer whether species are pollinated by insects or birds. When inferred pollinators were mapped on the tree the Hakeinae were unequivocally resolved as ancestrally insect-pollinated. Pollination by birds has evolved independently at least six times in the Hakeinae over the past 25 million years, which is consistent with what we know about the timing of the evolution and diversification of honeyeaters. Secondary reversals to insect pollination have occurred at least eleven times, a pattern that is rare amongst bird-pollinated plant groups.


PWe-IMGP6858-Hakea-strumosa-Fitzgerald-River-NP
Most species of Hakea, including Hakea strumosa, shown here, produce a woody fruit, which opens after fire. This is an adaptation that protects the seeds from fire and 'plants' them on a fertile ash-bed well after the fire has passed.

PWe-IMGP7358-Noisy-Miner-(Manorina-melanocephala)-visiting-Grevillea-petrophiloides-for-nectar
Many species of Grevillea are adapted for pollination by honeyeaters. Here a noisy miner visits a cultivated plant of Grevillea petrophiloides seeking nectar at the Australian Botanic Garden, Mount Annan.

PWe-IMGP7492-Grevillea-endlicheriana-follicles
Leathery, follicular fruits of Grevillea endlicheriana, sister species to the rest of the Grevillea-Hakea-Finschia clade. A leathery fruit wall was inferred to be ancestral in the subtribe Hakeinae.

PWe-IMGP7488-Grevillea-endlicheriana-inflorescence
Inflorescence of Grevillea endlicheriana, which was inferred from floral morphology to be insect-pollinated.

Photos: Peter Weston