Evolutionary community ecology in the cichlid species-flock of the East African Lake Tanganyika

Water, a main source of all life on earth – covers over two thirds of our planets’ surface, yet contains the most unexplored ecosystems (Webb, Vanden Berghe, & O’Dor, 2010). It is little wonder that scientist around the globe are fascinated by the unknown that lies within the depth of the blue world. Fresh waters such as rivers and lakes make up only a fraction, namely 0.01% of surface waters, still, a fourth of our planet’s aquatic biodiversity is found in freshwater (Grosberg, Vermeij, & Wainwright, 2012). Although this is the equivalent to ‘only’ about 5% of the global biodiversity, we find therein an extraordinary variation of life forms.
“Almost every major mammalian clade has at least one transition event going back in the water, except the primates. Then again, Homo sapiens is hairless and with a fatty layer beneath the skin, traits often associated with living in water”
Prof. Dr. Heinrich Reichert, University of Basel
This particular statement made during my Bachelor degree, though meant as an amusing anecdote rather than a scientific hypothesis, fanned my already kindling fascination with the diversity and adaptation of life in the aquatic environment.
Since Darwin formulated his ‘mystery of mysteries’ of the origin of species (Darwin, 1859), evolutionary biologist have been trying to solve his riddle and understand how and why diversity of life emerged (e.g. Nosil, 2012). Darwin postulated the theory of natural selection based on, among others, his study of the finches on Galapagos, which since then have been studied extensively (Snow & Grant, 2006; Han et al., 2017). Speciation through natural selection can be categorised into two general ways, either mutation-order or ecological driven
speciation. Ecological speciation, where divergent selection is driven by diverging environmental conditions is thought by many to be a key trigger of speciation; it is, however, a hotly debated topic, whether ecological speciation in itself can truly be a major force for diversification of species (Schluter, 2000; Nosil, 2012). This is especially true in the case of adaptive radiations – that is rapidly diversifying lineages that exploit a variety of habitats and differ in traits to exploit these different niches, such as the Darwin finches or the Anolis Lizards found in the Caribbean (Losos, 1990; Losos, Jackman, Larson, de Queiroz, & Rodriguez- Schettino, 1998; Hertz et al., 2013).
Within teleost fish, the family Cichlidae sticks out because of particularly fast (‘explosive’) speciation events bringing forth approximately 3’000-4’000 species (Turner, Seehausen, Knight, Allender, & Robinson, 2001; Salzburger, 2018). This massive diversity makes Cichlidae the champion of species-richness within the vertebrates (Sturmbauer, Husemann, & Danley, 2011; Berner & Salzburger, 2015). In particular, the enigmatic cichlids species-flock of the East African Great Lakes exhibit diversity in morphology, behaviour, and ecology that is unrivalled, making these a prime example of an adaptive radiation (Salzburger, 2018). The oldest of these, Lake Tanganyika is home to approximately 250 endemic cichlid species belonging to 14 different lineages so-called tribes. Members of these lineages have diversified to occupy a wide variety of habitats in the lake, but not in an equal manner. To better understand the influence of the environment on the diversification within lineages, researchers began to include ecological niche modelling (ENM) into the framework of phylogenetic studies on other radiations (Knouft, Losos, Glor, & Kolbe, 2006; García-Navas & Westerman, 2018). Using ENM can give us a better insight into the ecological niche of different species and how their niches overlap. Considering that we seldom observe the fundamental niche, but rather the realized niche; we should not rely solely on the information gained through the environmental variables, but consider the community structure and co-occurrence patterns, as they influence niche occupancy as well. Taking this into account, the information gained could help our
understanding of the underlying processes of speciation; as the ecological niche that is occupied by a species will have had an apparent influence on the evolution of its morphological, physiological or behaviour traits; so, the diversification of the niche can be studied to understand the evolution of species diversity (Ackerly, Schwilk, & Webb, 2006; Knouft et al., 2006).
To be able to study the cichlid community in its entirety we first had to develop a solid approach to get reliable census data. In the first part of my thesis I tackled this challenge. In Chapter 1 (‘Point-Combination Transect (PCT): Incorporation of small underwater cameras to study fish communities’) we present a novel approach of a non-invasive method to study underwater communities based on the use of small digital cameras together with a critical assessment of its strength and flaws, including a comparison to long established underwater visual census methods (UVC). Another approach to study and monitor natural communities is the integration of genetic methods such as the use of environmental DNA (eDNA). Chapter 2 (‘Does eDNA within sediments reflect local cichlid assemblages in Lake Tanganyika?’) explores the applicability of eDNA, particularly found in the sediment, being used to assess the cichlids fish diversity at various sites at Lake Tanganyika. Compared with carefully compiled PCT data following the methodology presented in Chapter 1, we compiled an ideal data set for proof of concept of PCT and discuss the validity of eDNA as a tool for future community assessments in cichlids.
In Part Two, with the robust methodology introduced in Chapter 1, we address questions concerning the community structure and niche evolution of the adaptive radiation of Tanganyikan cichlids in Chapter 3 (‘Community assembly patterns and niche evolution in the species-flock of cichlid fishes from East African Lake Tanganyika’). In this Chapter, we describe the extensive fieldwork and visual census survey we conducted at Lake Tanganyika and analyse the community structure and patterns of assembly for the cichlid species-flock. Using
ecological niche modelling and the resulting niche overlap as a proxy, I explore the difference between the tribes and their implication for the radiation of lineages. Lastly, using phylogenetic tools, we reconstructed the niche tolerance of 94 cichlid species to study the evolution of the niche within the adaptive radiation.
In my last chapter, Chapter 4 (‘Where Am I? Niche constraints due to morphological specialisation of two Tanganyikan cichlid species’), we used reciprocal transplant experiments in a semi-natural environment to examine how the performance of distinctly different species is influenced when they are displaced from their natural niche into a “foreign” habitat. The focus lies on the capacity to deal with a new environment by studying survival, growth and phenotypic plasticity of the lower pharyngeal jaw (LPJ), a trophic structure used by cichlids for mastication (Liem, 1973).
In summary, my thesis is structured into two parts, each containing two manuscripts. The first part focuses on defining and thoroughly validating a new methodology to collect reliable census data of the cichlid species-flock of Lake Tanganyika. The second part focuses on the community structure and assembly patterns of the cichlids along the Zambian and Tanzanian coast. Followed lastly by an examination of niche evolution, through the use of ecological niche models (ENM) that are based on the cichlid census and environmental data collected during my thesis.