Evolution of Melicope J.R.Forst & G.Forst (Rutaceae), the largest adaptive radiation of woody plants on the Hawaiian Islands.
by Claudia Pätzold
Date of Examination:2020-02-18
Date of issue:2020-11-27
Advisor:Prof. Dr. Elvira Hörandl
Referee:Prof. Dr. Elvira Hörandl
Referee:Prof. Dr. Alexander Schmidt
Referee:Prof. Dr. Hermann Behling
Referee:Prof. Dr. Bleidorn Christoph
Referee:Prof. Dr. Oliver Gailing
Referee:Prof. Dr. Holger Kreft
Files in this item
EnglishAdaptive radiation describes the divergence of an ancestral taxon into multiple, phenotypically diverse species, adapted to a range of ecological niches by means of natural selection. The process is recognized as a fundamental reason for the origin of biodiversity. The main driver of adaptive radiation is ecological opportunity, though the specific agents are often poorly understood with the exception of some iconic lineages. Many well-studied adaptive radiations are island endemics, which makes island systems an ideal study system for adaptive radiation. Oceanic islands represent discrete replicates of the evolutionary process, as they are isolated, comparatively small, and often topographically complex. Species communities are formed by colonization and in situ diversification. The Hawaiian Islands are the most isolated archipelago on earth and home to a range of adaptively radiating lineages. The islands form as the Pacific plate passes over a magmatic hotspot with the eight current high islands originating within the last ca. 5-6 million years and the majority of the native biodiversity diverging within that time. The genus Melicope colonized numerous archipelagos throughout the Pacific including the Hawaiian Islands, where the lineage comprises currently 54 endemic species and represents the largest radiation of woody plants on the islands. Most species are single-island endemics and adapted to a variety of habitat types and elevational ranges. The lineage is monophyletic with an estimated crown age predating the rise of the current high islands, the oldest of which originated approximately 5 million years ago. As for many adaptively radiating lineages, phylogenetic inference based on Sanger sequencing has not been sufficient to resolve species or deeper level relationships in Hawaiian Melicope. Recent years have seen development of high throughput sequencing methods and their increasing application to solve recalcitrant relationships. In this thesis, I examined the evolutionary trajectory of the Hawaiian Melicope adaptive radiation. I investigated the so-called ‘island syndrome’, which describes a set of traits commonly characterizing successful island colonizers, including recent polyploidy and shifts associated with subsequent establishment, in Hawaiian Melicope. I utilized restriction site-associated high throughput sequencing (RAD-seq) to reconstruct species relationships and historical biogeography in the lineage and estimate diversification rates and the impact of habitat adaption on species divergence. RAD-seq datasets provided unprecedented resolution of species relationships in Hawaiian Melicope. However, the size and complexity of high throughput sequencing datasets require a high computational effort, which currently limits the applicability of algorithms for phylogenetic inference to concatenated analysis or site-specific coalescence-based methods. I employed both methods and found them to result in incongruent relationships for the backbone of the Hawaiian Melicope topology. Concatenation violates the assumptions of the multispecies coalescent model, while site-based methods are statistically inconsistent but less accurate in simulated and empirical datasets. Considering the increased accuracy of the concatenated approaches as evaluated by quartet concordance methods and the synergistic effect of concatenation, I concluded that results of concatenated analysis reflect the relationships of Hawaiian Melicope best. Results of flow cytometric screening of 32 Hawaiian species, representing 66% of the described diversity, and literature searches indicate that the ancestor of Hawaiian Melicope did not show traits associated with successful colonizers. The genus seemingly retained colonization success while exhibiting a combination of traits that typically characterize well-established island specialists. In particular, the ancestral Melicope colonist was not a recent polyploid. Neopolyploidy increases evolutionary flexibility and thus enhances chances for establishment and adaption. In Hawaiian Melicope flexibility is possibly facilitated by introgressive hybridization events. Phylogenetic reconstruction based on RAD-seq datasets provides evidence for two ancient and several recent introgression events. Extant Hawaiian Melicope are divided into five fully supported main clades, two of which correspond to morphologically circumscribed infrageneric groups, whereas three morphologically defined taxonomic units are not monophyletic. All in all, 24 species were included with multiple samples, four of which were resolved as non-monophyletic. Finally, I confirmed that the Melicope radiation endemic to the Marquesas Islands originated from the Hawaiian radiation. These results highlight the necessity for a taxonomic revision in the lineage. Estimated divergence times revealed that the Hawaiian archipelago was colonized prior to the origin of the current high islands. Inter-Island colonization patterns largely follow the progression rule from older to younger islands, but back colonizations to older islands occurred. Extant diversity results from recent divergence of a small number of taxa prevailing through the bottlenecks represented by the origin and colonization of the high islands. Long internal branches and estimated diversification rates indicate a high extinction rate, possibly related to the consequences of volcanic activity and the impact of glacial cycles. Consequently habitat types that are more vulnerable to climatic changes, i.e. dry ranges and bogs show high speciation and extinction rates. Increased rates of diversification are linked to habitat dissection and frequent ecological trait shifts.
Keywords: Melicope; Rutaceae; RAD-Sequencing; Phylogeny; Divergence Times; Historical Biogeography; Ploidy; Diversification; Hawai'i; Pacific