Katrijn De Bock
The concept of evolutionary transitions in individuality (ETIs) was developed to explain how life has repeatedly reorganised itself through a series of successive steps in which lower-level entities that once reproduced independently became integrated into higher-level collectives on which natural selection could act. Classic transitions such as the origins of eukaryotic cells, multicellularity, and animal societies have shaped this framework, each characterised by cooperation, division of labour, and conflict suppression. Plants have been absent from discussion of transitions beyond multicellularity, raising the question of whether this absence reflects biological limits or a historical bias in how plant life has been perceived. Platycerium bifurcatum (Polypodiaceae), commonly known as the staghorn fern, is a species of epiphytic fern native to parts of Southeast Asia and eastern Australia, including Lord Howe Island. It is among the largest-growing epiphytic ferns, capable of developing considerable size. This size results from the gradual formation of a colony composed of repeated units, which arise from a single founder through asexual reproduction via root-borne buds. Each unit has its own ascending rhizome that produces two types of fronds: nest fronds, which are persistent and interlock to form a shared protective “nest” around rhizomes and roots, and strap fronds, which remain photosynthetically active until they mature, at which point they abscise; sometimes after producing reproductive structures. Both frond types are heteroblastic, with their form and size changing as the unit ages. Early observations indicate variation in both strap and nest frond morphology among units within colonies. The outcome is a long-lived collective buffered from external conditions, raising questions about how colonies are organised, how they persist, and whether frond differentiation contributes to functional specialisation; questions that remain largely unexplored. The aim of this thesis was to investigate what collective living means in P. bifurcatum and how its organisation and functioning could be understood. I asked three guiding questions: (1) whether morphological differences among fronds reflected functional specialisation within colonies; (2) whether colonies were genetically uniform, as traditionally assumed, or incorporated multiple genotypes; and (3) how colonies interacted with their environment. Each question was explored through field-based research on colonies growing in natural forest habitats on Lord Howe Island (NSW, Australia). Together, these questions structured the three empirical chapters, which focused on the biology of the species and provided a foundation for analysing colony development, functioning, and persistence. Chapter 3 investigated how colony size and unit position influence morphological differentiation and functional roles in strap fronds across the vertical profile of Platycerium bifurcatum colonies. Each colony was divided into three fixed vertical categories (top, middle, and bottom), and one unit was randomly selected from each category, resulting in 87 units measured across 29 colonies. Units located in the upper part of the colony produced rigid, curved, erect strap fronds suited to water capture, while lower units had pendulous, flattened, flexible strap fronds better adapted to enhance photosynthesis in shaded conditions. Reproductive allocation was highest in upper units, and larger colonies exhibited greater morphological differentiation, patterns that point to functional differences across colony levels and a tendency toward increased task specialisation with colony size. Chapter 4 investigated the genetic composition of colonies by collecting tissue from all units (487 in total) across 16 colonies, which were genotyped at 33 SNP loci and paired with morphological data. Results showed high variability: four colonies were clonal, whereas twelve contained between two and 23 multilocus genotypes (MLGs) in various relative frequencies. No clear spatial patterning was found with MLGs often intermingled without strong vertical or directional stratification. Consistent morphological or reproductive differences were not observed between clonal and mixed colonies, and between MLGs within mixed colonies. These findings reveal previously unrecognised genetic diversity within colonies and suggest that clonality is not required for colony persistence. Chapter 5 evaluated the ecological role of colonies as habitats for other plants by surveying 80 colonies. Many were found to host additional species rooted within nest structures, referred to here as “guests.” Guests occurred in about one-sixth of colonies and included ferns, orchids, and other vascular plants. Their presence was associated with colony size, density, and fecundity, suggesting that guests may influence colony performance. These findings provide a botanical analogue to nest–guest systems in other colonial organisms. By synthesizing the findings from Chapters 3–5 with recent biological insights into the life history of P. bifurcatum, I outline a conceptual framework for colony development. The framework proposes that colonies expand through bi-directional growth, with rhizomes from existing units elongating upward and new units forming below through root-borne propagation, thereby creating a vertical age gradient. This gradient provides a basis for understanding the morphological and functional shifts in frond traits across the colony profile. In addition to clonal propagation, genetically distinct units may establish in the shaded, moist conditions at the nest base, where spore germination and integration are favoured. A process for colony attachment was also proposed, in which nest fronds, roots, and rhizomes contribute jointly to form a cohesive structure that distributes mechanical load and supports colony persistence through collective effort. Finally, the thesis moves from biology to theory, situating P. bifurcatum within the broader framework of major evolutionary transitions and their necessary components. I address whether cooperation and division of labour occur, what individuality means for this species, and how its self-organised collective nest can be framed in ecological and evolutionary contexts. Each question is considered with care, recognising the challenges of applying animal-centric concepts to plants. By engaging with theories such as kin selection, ecological scaffolding, niche construction, and connectionism, the discussion argues that individuality in P. bifurcatum is emergent and contingent on its environment, offering a plant-based perspective that broadens the scope of ETI research beyond multicellularity.