Community assembly in Lake Tanganyika cichlid fish:Quantifying the contributions of both niche-based and neutral processes

The cichlid family features some of the most spectacular examples of adaptive radiation. Evolutionary studies have highlighted the importance of both trophic adaptation and sexual selection in cichlid speciation. However, it is poorly understood what processes drive the composition and diversity of local cichlid species assemblages on relatively short, ecological timescales. Here, we investigate the relative importance of niche-based and neutral processes in determining the composition and diversity of cichlid communities inhabiting various environmental conditions in the littoral zone of Lake Tanganyika, Zambia. We collected data on cichlid abundance, morphometrics, and local environments. We analyzed relationships between mean trait values, community composition, and environmental variation, and used a recently developed modeling technique (STEPCAM) to estimate the contributions of niche-based and neutral processes to community assembly. Contrary to our expectations, our results show that stochastic processes, and not niche-based processes, were responsible for the majority of cichlid community assembly. We also found that the relative importance of niche-based and neutral processes was constant across environments. However, we found significant relationships between environmental variation, community trait means, and community composition. These relationships were caused by niche-based processes, as they disappeared in simulated, purely neutrally assembled communities. Importantly, these results can potentially reconcile seemingly contrasting findings in the literature about the importance of either niche-based or neutral-based processes in community assembly, as we show that significant trait relationships can already be found in nearly (but not completely) neutrally assembled communities; that is, even a small deviation from neutrality can have major effects on community patterns

Depth-dependent abundance of Midas Cichlid fish ( Amphilophus spp: ) in two Nicaraguan crater lakes

The Midas Cichlid species complex (Amphilophus spp.) in Central America serves as a prominent model system to study sympatric speciation and parallel adaptive radiation, since small arrays of equivalent ecotype morphs have evolved independently in different crater lakes. While the taxonomy and evolutionary history of the different species are well resolved, little is known about basic ecological parameters of Midas Cichlid assemblages. Here, we use a line transect survey to investigate the depth-dependent abundance of Amphilophus spp. along the shores of two Nicaraguan crater lakes, Apoyo and Xiloá. We find a considerable higher density of Midas cichlids in Lake Xiloá as compared to Lake Apoyo, especially at the shallowest depth level. This might be due to the higher eutrophication level of Lake Xiloá and associated differences in food availability, and/or the presence of a greater diversity of niches in that lake. In any case, convergent forms evolved despite noticeable differences in size, age, eutrophication level, and carrying capacity. Further, our data provide abundance and density estimates for Midas Cichlid fish, which serve as baseline for future surveys of these ecosystems and are also relevant to past and future modeling of ecological speciatio

A chronologically reliable record of 17,000 years of biomass burning in the Lake Victoria area

Fire regimes differ across tropical and subtropical biomes depending on multiple parameters whose interactions and levels of importance are poorly understood, particularly at multidecadal and longer time scales. In the catchment of Lake Victoria, savanna, rainforest, and Afromontane vegetation have interspersed over the last 17,000 years, which may have influenced the fire regime and vice versa. However, climate and humans are most often the primary drivers of fire regime changes, and analysing their respective roles is critical for understanding current and future fire regimes. Besides a handful of radiocarbon dates on grassy charcoal, the timescales of published studies of Lake Victoria sediment chronologies rely mostly on dates of bulk sediment, and chronological disagreements persist, mainly due to variation between estimations of the 14 C reservoir effect. Here, we provide independent 14 C chronologies for three Late Glacial and Holocene lacustrine sediment cores from various water depths and compare them with the biostratigraphy to establish a new chronological framework. We present the first continuous sedimentary charcoal records from Lake Victoria; these suggest that fire activity varied substantially during the past 17,000 years. Our new pollen records reveal the long-term vegetation dynamics. The available evidence suggests that before human impact increased during the Iron Age (ca. 2400 yr BP), biomass burning was linked to climate and vegetation reorganizations, such as warming, drying, and the expansion of rainforests and savannas. Our results imply that climate can trigger substantial fire regime changes and that vegetation responses to climate change can co-determine the fire regime. For instance, biomass burning decreased significantly when the rainforest expanded in response to increasing temperatures and moisture availability. Such insights into the long-term linkages between climate, vegetation, and the fire regime may help to refine ecosystem management and conservation strategies in a changing global climate

Testing alternative hypotheses for the decline of cichlid fish in Lake Victoria using fish tooth time series from sediment cores.

Lake Victoria is well known for its high diversity of endemic fish species and provides livelihoods for millions of people. The lake garnered widespread attention during the twentieth century as major environmental and ecological changes modified the fish community with the extinction of approximately 40% of endemic cichlid species by the 1980s. Suggested causal factors include anthropogenic eutrophication, fishing, and introduced non-native species but their relative importance remains unresolved, partly because monitoring data started in the 1970s when changes were already underway. Here, for the first time, we reconstruct two time series, covering the last approximately 200 years, of fish assemblage using fish teeth preserved in lake sediments. Two sediment cores from the Mwanza Gulf of Lake Victoria, were subsampled continuously at an intra-decadal resolution, and teeth were identified to major taxa: Cyprinoidea, Haplochromini, Mochokidae and Oreochromini. None of the fossils could be confidently assigned to non-native Nile perch. Our data show significant decreases in haplochromine and oreochromine cichlid fish abundances that began long before the arrival of Nile perch. Cyprinoids, on the other hand, have generally been increasing. Our study is the first to reconstruct a time series of any fish assemblage in Lake Victoria extending deeper back in time than the past 50 years, helping shed light on the processes underlying Lake Victoria's biodiversity loss

A continuous fish fossil record reveals key insights into adaptive radiation.

Adaptive radiations have been instrumental in generating a considerable amount of life's diversity. Ecological opportunity is thought to be a prerequisite for adaptive radiation1, but little is known about the relative importance of species' ecological versatility versus effects of arrival order in determining which lineage radiates2. Palaeontological records that could help answer this are scarce. In Lake Victoria, a large adaptive radiation of cichlid fishes evolved in an exceptionally short and recent time interval3. We present a rich continuous fossil record extracted from a series of long sediment cores along an onshore-offshore gradient. We reconstruct the temporal sequence of events in the assembly of the fish community from thousands of tooth fossils. We reveal arrival order, relative abundance and habitat occupation of all major fish lineages in the system. We show that all major taxa arrived simultaneously as soon as the modern lake began to form. There is no evidence of the radiating haplochromine cichlid lineage arriving before others, nor of their numerical dominance upon colonization; therefore, there is no support for ecological priority effects. However, although many taxa colonized the lake early and several became abundant, only cichlids persisted in the new deep and open-water habitats once these emerged. Because these habitat gradients are also known to have played a major role in speciation, our findings are consistent with the hypothesis that ecological versatility was key to adaptive radiation, not priority by arrival order nor initial numerical dominance

Long-term ecological successions of vegetation around Lake Victoria (East Africa) in response to latest Pleistocene and Early Holocene climatic changes

Reconstructions of ecosystem dynamics in tropical East Africa during the latest Pleistocene and the Holocene provide important long-term ecological insights, but so far, only a few, sometimes incomplete terrestrial records exist. In this paper, we present a new high-resolution palynological record from the Lake Victoria basin, covering the period from 16,600 to 9000 cal yr BP, when Afromontane forests and tropical rainforests gradually replaced the savanna. We discuss this dataset in the context of published palaeoclimate data, TEX86 inferred temperature and δD leaf wax inferred precipitation records, to assess long-term ecological successions and their potential causes. By ca. 16,500 cal yr BP, the movement of the Afrotropical rainbelt, not only brought an increase in temperature and moisture into the Lake Victoria basin, but also promoted the spread of arboreal taxa, such as Celtis and Podocarpus, at the expense of the savanna. At that time, fires were prominent in the sparse Afromontane vegetation. Later from ca. 15,500–15,000 cal yr BP, temperature and humidity rose and Afromontane trees such as Olea and Macaranga spread slightly, while grasses were burning in the savanna. During the period from 13,250 to 10,700 cal yr BP, Afromontane vegetation dominated by Olea became more prominent and expanded towards the lowlands where the tropical rainforest or gallery forest established; however, the savanna only marginally retreated. An initial spread of tropical rainforests occurred from ca. 11,500–11,100 cal yr BP during the onset of the Holocene, when temperatures and moisture further increased. Subsequently, between 10,700 and 10,300 cal yr BP the tropical savanna was largely replaced by the tropical rainforest, while the Afromontane forest likely spread to higher elevations, similar to the patterns observed today. Our high-resolution record demonstrates the dynamic response of African tropical ecosystems to major temperature and humidity variations from 16,600 to 9000 cal yr BP, including some of the most important landscape transformations in East Africa in the past 20,000 years

Ancient DNA is preserved in fish fossils from tropical lake sediments

Tropical freshwater lakes are well known for their high biodiversity, and particularly the East African Great Lakes are renowned for their adaptive radiation of cichlid fishes. While comparative phylogenetic analyses of extant species flocks have revealed patterns and processes of their diversification, little is known about evolutionary trajectories within lineages, the impacts of environmental drivers, or the scope and nature of now-extinct diversity. Time-structured palaeodata from geologically young fossil records, such as fossil counts and particularly ancient DNA (aDNA) data, would help fill this large knowledge gap. High ambient temperatures can be detrimental to the preservation of DNA, but refined methodology now allows data generation even from very poorly preserved samples. Here, we show for the first time that fish fossils from tropical lake sediments yield endogenous aDNA. Despite generally low endogenous content and high sample dropout, the application of high-throughput sequencing and, in some cases, sequence capture allowed taxonomic assignment and phylogenetic placement of 17% of analysed fish fossils to family or tribe level, including remains which are up to 2700 years old or weigh less than 1 mg. The relationship between aDNA degradation and the thermal age of samples is similar to that described for terrestrial samples from cold environments when adjusted for elevated temperature. Success rates and aDNA preservation differed between the investigated lakes Chala, Kivu and Victoria, possibly caused by differences in bottom water oxygenation. Our study demonstrates that the sediment records of tropical lakes can preserve genetic information on rapidly diversifying fish taxa over time scales of millennia

Adaptive phenotypic plasticity in the Midas cichlid fish pharyngeal jaw and its relevance in adaptive radiation

Phenotypic evolution and its role in the diversification of organisms is a central topic in evolutionary biology. A neglected factor during the modern evolutionary synthesis, adaptive phenotypic plasticity, more recently attracted the attention of many evolutionary biologists and is now recognized as an important ingredient in both population persistence and diversification. The traits and directions in which an ancestral source population displays phenotypic plasticity might partly determine the trajectories in morphospace, which are accessible for an adaptive radiation, starting from the colonization of a novel environment. In the case of repeated colonizations of similar environments from the same source population this "flexible stem" hypothesis predicts similar phenotypes to arise in repeated subsequent radiations. The Midas Cichlid (Amphilophus spp.) in Nicaragua has radiated in parallel in several crater-lakes seeded by populations originating from the Nicaraguan Great Lakes. Here, we tested phenotypic plasticity in the pharyngeal jaw of Midas Cichlids. The pharyngeal jaw apparatus of cichlids, a second set of jaws functionally decoupled from the oral ones, is known to mediate ecological specialization and often differs strongly between sister-species. We performed a common garden experiment raising three groups of Midas cichlids on food differing in hardness and calcium content. Analyzing the lower pharyngeal jaw-bones we find significant differences between diet groups qualitatively resembling the differences found between specialized species. Observed differences in pharyngeal jaw expression between groups were attributable to the diet's mechanical resistance, whereas surplus calcium in the diet was not found to be of importance. The pharyngeal jaw apparatus of Midas Cichlids can be expressed plastically if stimulated mechanically during feeding. Since this trait is commonly differentiated - among other traits - between Midas Cichlid species, its plasticity might be an important factor in Midas Cichlid speciation. The prevalence of pharyngeal jaw differentiation across the Cichlidae further suggests that adaptive phenotypic plasticity in this trait could play an important role in cichlid speciation in general. We discuss several possibilities how the adaptive radiation of Midas Cichlids might have been influenced in this respect

Convergence and plasticity in the adaptive radiation of cichlid fishes

Ever since Charles Darwin and Alfred Wallace (1858) propelled our understanding about the importance of natural selection in the transformation of species, researchers endeavoured to use this intellectual foundation to explain larger patterns of biodiversity. One pattern emerging from the observation of phylogenetic relationships and ecological adaptations of species is the abundance of lineages, which are apparently rapidly diversifying, resulting in ecologically diverse clades of species. Most of the biodiversity we know is made up by such clades, being the result of so-called adaptive radiations. Phenotypic diversification and lineage accumulation in adaptive radiations have received considerable attention and great progress has been made in understanding these aspects. Adaptive radiations can be triggered by an ecological opportunity, i.e. a newly formed or colonized habitat lacking competing species or the formation of a key-innovation, a novel trait that allows for the invasion of a completely novel set of niches. The radiation of East African cichlid fishes, and other groups of fishes, are hypothesized to have been triggered by a key-innovation, namely a reorganisation of the pharyngeal jaw apparatus (Liem 1973). Liem’s hypothesis attributes the evolutionary success of groups with certain pharyngeal jaw modifications to an increased versatility in exploiting resources. Although morphological descriptions of the pharyngeal jaw apparatus for many taxa of fishes abound in the literature, and studies with functional, biomechanical or ecological perspectives are numerous as well, as of yet no concise treatise about the evolutionary implications of the different aspects and characteristics of the pharyngeal jaw has been published. This gap I thrive to close with the first chapter of this thesis. The course of adaptive radiations might be influenced by a phenomenon only little studied in this context so far. Phenotypic plasticity, the ability of a genotype to produce different phenotypes depending on environmental cues, might increase a founding populations chance of persistence. Novel niches might also be invaded more quickly, since the phenotypic shift due to plasticity might place a population in the ‘realm of attraction’ of a peak on the adaptive landscape. If plasticity is only exhibited in some directions in morphospace, but not in others it has the potential of biasing evolutionary trajectories in adaptive radiations. To better understand if phenotypic plasticity in the pharyngeal jaw might have influenced the adaptive radiations of cichlids, I studied the Nicaraguan Midas cichlid in a common garden experiment. My demonstration of plasticity in the cichlids’ pharyngeal jaw, reported in chapter 2, suggests it as a factor to be considered in answering the question of why there are so many cichlid species. The concept of adaptive radiation is intimately related to ecological adaptation by means of natural selection. Thus, one would not be surprised if phenomena indicative of natural selection would be common in adaptive radiations. One of the strongest cases for the action of natural selection, since the birth of the idea, has been made with the argument of convergent evolution. Separation in time or by geography was, however, assumed to be necessary due to competitive exclusion (Osborn 1902). This principle, later formulated by Gause (1934), was questioned to be applicable to some communities of organisms, one of them being the cichlid species flocks of East Africa. Ernst Mayr (1984) asked: “The coexistence of hundreds of closely related species in the same lake poses some fundamental questions concerning competition and resource utilization. To what extent, if any, is the existence of fish flocks in freshwater lakes in conflict with the concept of competitive exclusion?” This question is investigated in chapter 3, which is concerned with convergence within the cichlid radiation in Lake Tanganyika. The revealed abundance of ecomorphological convergence without geographical or chronological separation indeed seems to defy Gause’s principle. Furthermore, it suggests the facility of coexistence of convergent species to be another key factor for the cichlids’ species richness that has been previously overlooked. The large overlap in morpho- and ecospace between subclades of Tanganyikan cichlids is not unique, but emerges as a common feature of adaptive radiations. This is exemplified by the adaptive radiation of Antarctic notothenioid fishes, the topic of chapter 4, comprising several families, which diversified in parallel along the benthic-pelagic axis. Thus, an adaptive radiation of fishes, taking place in a most different setting than the tropical, confined, freshwater environment in which cichlids diversified, nevertheless exhibits intriguing parallels in subclade overlap. Convergence might hence be a feature of radiations in general

Evolution: An Archipelago Replete with Replicates

Adaptive radiations, in which repeated bouts of diversification lead to phenotypically similar species, highlight the power of natural selection and predictability in evolution. A newly discovered radiation of stick spiders on Hawaii helps shed new light on this phenomenon