Systematics and evolutionary biology of the Weevils associated with cycads in Australia

Abstract

Cycads are subtropical and tropical palm-like gymnosperms, commonly known as "living fossils" as they arose in the late Paleozoic and were much more diverse and dominant during the Mesozoic. Modern cycads underwent a recent global diversification in Miocene (ca. 11-20 mya). Even though cycads were long thought to be wind-pollinated, it has been recently shown that cycads are dominantly pollinated by insects, especially beetles. Australia is one of the main centres of cycad diversity, comprising four genera and approximately 90 named species. Weevils play significant roles in pollination of Australian cycads, although some species are also pollinated or co-pollinated by some genera and species of the beetle families Boganiidae and Erotylidae and thrips. While it is now established that Australian cycads are largely weevil-pollinated, the systematics and phylogeny of the cycad-associated weevils are poorly known, and it is consequently unknown how host-specific the pollinators are and the evolution of cycad-weevil association in Australia. In this thesis, mitochondrial genomes were sequenced from museum specimens to reconstruct the first molecular phylogeny to investigate on the monophyly, systematic placement and sister groups of Australian cycad weevils and relationships among species. This phylogeny reveals that Australian cycad weevils are non-monophyletic, which are recovered located at three different clades in two subfamilies: a clade containing weevils associated with Cycas belonging to Cossoninae; trunk-boring weevils associated with Macrozamia and Lepidozamia forming a clade in Tranes group of Molytinae; and another clade in Tranes group includes weevils pollinating Bowenia, Macrozamia and Lepidozamia. Additionally, our results prefer the closer relationship among Tranes group, Pissodini, Molytini and Lixini rather than Orthorhinini suggested in previous study. The combination of morphological studies and molecular species delimitation were conducted for estimating putative species number of Australian cycad weevils, and 19 distinct species in 6 genera were recognised, including 2 new genera and 8 new species. To investigate on the origin of cycad-association of Australian cycad weevils, divergence dating using fossil calibration data was performed and the results indicate that Australian cycad weevil groups originated from the late Oligocene to middle Miocene (ca. 24.6-14.1 mya) and the main radiation of cycad-pollinating groups occurred from the middle to late Miocene (ca. 14.1-3.4 Ma), which is congruent with the diversification of Australian cycads, highlighting the temporal correlation between cycads and their associated weevils. However, on the basis of the taxonomic assessment of Australian cycad weevils, most of Australian cycad-pollinating weevils are found non-host-specific and can be associated with multiple cycad species. Additionally, co-speciation analysis also shows no extensive co-speciation pattern in the Australian cycad-weevil pollination system. Compared with the distribution pattern, it suggests the speciation in allopatry may play a more dominant role in diversification of Australian cycad weevils rather than host-associated factors. The temporal coincidence of divergence is probably due to the global post-Oligocene diversification event occurred across various groups of organisms instead of coevolutionary diversification. The present thesis also provides first-hand observations in the wild and during laboratory rearing, new host plant records and developed a method for rearing mature larvae of cycad weevils in the laboratory. This thesis improves our understanding of the phylogeny, systematics, evolution and natural history of the Australian cycad weevils, a unique group of Australia's insect fauna evolving specific mutualistic interaction with the "living fossil" plants. Show more