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Chomicki, Guillaume (2016): Ant/plant symbioses: evolution, specialization and breakdown. Dissertation, LMU München: Fakultät für Biologie



This doctoral thesis focuses on the evolution of ant/plant symbioses, a conspicuous form of mutualism involving some 113 species of ants and 684 species of vascular plants and occurring throughout the World’s tropical zones. My thesis addresses the following questions: (i) When, how often, and where did ant-plant symbioses evolve? (ii) By which steps did ant/plant symbioses evolve and which biotic or abiotic traits have favored them? (iii) How do ant/plant symbioses negotiate the tradeoff between specialization and stabilization? (iv) How often and under which conditions do ant/plant symbioses break down? (v) Are obligate epiphytic ant/plant symbioses dispersed by their ant symbionts? And (vi) how do related species of facultative and obligate ant-plants maximize benefits from the mutualism? To address these questions, I chose a clade of Australasian Rubiaceae that includes species with facultative, obligate or no ant symbioses and inferred its species relationships and geographic history, the precondition for studying the evolution of species’ interactions with ants. To answer question (i), I performed a literature survey of ant-plants and used capture-release models to estimate the expected number of ant-plants worldwide. I found that Australasia contains about 289 ant-plants, making it equally rich in ant-plants as the Neotropics (Chapter 1). Using a 1,140 species tree with ant-plants and their non-ant-plant relatives, I estimated a minimum of 158 origins of ant domatia in vascular plants (Chapter 1). I then employed molecular clock-dated phylogenies for 56% of the World’s known ant/plant lineages and found that the extant ant/plant symbioses in the Neotropics and Australasia date back to the Middle Miocene, while those in Africa only date back to 5-10 million years (Chapter 1). To answer question (ii), I used a phylogenetic framework for the ant genus with the largest number of obligate plant-ants (Pseudomyrmex) as well as phylogenies for its main plant host lineages (Chapter 2). I showed that host and symbiont broadening, meaning one partner increases the number of partners with which it interacts, is a dominant process in the evolution of ant/plant symbioses, even in the most specialized lineages such as the Central American ant/acacia mutualism (Chapter 2). Such increased host use led to the recruitment of new ant-plant lineages by plant-nesting ants; symbiont broadening in some instances appears to have resulted in complete partner replacement (Chapter 2). Another empirical finding is that parasites (i.e., ant species benefitting from plant rewards without reciprocating) originated from free-living generalists ant species, not from mutualists evolving into cheaters as predicted by theory. Host broadening apparently also was frequent in Australasian ant-gardens and seems to have favored the evolution of domatia once plants regularly ‘find themselves’ in ant-gardens (Chapter 8). Before going to the field in Fiji, I examined the relevant collections of Australasian in several herbaria (OXF, FHO, SUVA, DUB, K, L, M, BM, P), in addition to online databases and photos from other herbaria (in particular A, GH, FI, US, BISH). I discovered three new species in Fiji, resulting in now nine species of Squamellaria in the archipelago. By generating DNA sequences from relevant type material, I enlarged the (natural, monophyletic) genus Squamellaria from three species in the last revision (Jebb, 1991) to twelve species (Chapter 3). This taxonomic framework was essential to address all subsequent questions. To answer question (iii), I performed experiments and observations during eight weeks of fieldwork in September-October 2014 and March 2015 on all nine species of Squamellaria. By using DNA and morphological traits from herbarium material, I was able to place the Squamellaria data into a much larger comparative evolutionary framework (Chapter 4). Mutualism specialization requires more investment from each partner to increase levels of rewarding and partner fidelity, which increases the exploitation potential by opportunists. I showed that obligate ant-plants negotiated this tradeoff by evolving exclusive food rewards that can only be accessed by the obligate ant mutualist (Chapter 4). To answer question (iv), I generated a phylogeny for my focal clade that includes 76 of its 102 species, including several that I discovered during my fieldwork (above). Using this phylogeny and ancestral state reconstructions, I inferred ten losses of facultative symbiosis with ants, making this system well suited to study the ecological context of mutualism breakdown. In Hydnophytinae, mutualism breakdown has been driven by shifts to montane habitats (>1500 m alt.) where ants are scarce (Chapter 6). The evolution of a key mutualistic trait – entrance hole size – tightly tracked mutualistic strategies, with obligate ant-plants undergoing little evolutionary change in hole diameter, while species that lost mutualisms were free to rapidly change this trait. This indicates that mutualistic strategies, by determining the level of stabilizing selection, drive morphological evolution in mutualism-associated traits (Chapter 6; see also Discussion). To answer question (v), I used Fijian Squamellaria to study how facultative versus obligate ant-plants are dispersed, again relying on my own field observations and experiments. Facultative ant-plants are bird-dispersed, but obligate ant-plants are dispersed by their ant symbiont, the Dolichoderinae species Philidris nagasau (Chapter 5). Obligate ant-plant species of Squamellaria and P. nagasau ants engage in a type of ant-plant mutualism that is new to science, wherein the ants farm their hosts, planting the seeds inside tree bark of preferred host tree species and fertilizing the seedlings by defecating in their tiny domatia (before these are large enough to house any ant nest) (Chapter 5). To answer question (vi), I again used the Fijian Squamellaria system and designed experiments with stable isotopes (15N) to determine how ants fertilize hosts and how nitrogen uptake differs between facultative and obligate hosts. I also used Computed-Tomography Scanning to build 3D models of ant domatia. The domatia of Squamellaria attain rugby ball to pumpkin size, and their inner structure was essentially unknown. I discovered that in the obligate symbiosis, there is a single large cavity with small (ca. 2-3 mm in diameter) hyper-absorptive structures, termed ‘warts’, that are recognized by P. nagasau ants, which exclusively defecate on them, thus maximizing nitrogen benefits to the plants (Chapter 7). By contrast, facultative hosts have several unlinked cavities and lack absorptive warts. Because there is a high ant nest turnover in the facultative ant-plant species of Squamellaria, the modular domatium limits competition between inhabitants and maximizes the time any individual plant spends with nitrogen-providing ants (Chapter 7).